SMITHSONIAN CONTRIBUTIONS TO BOTANY NUMBER 73 

Phylogenetic Systematics as the Basis 

of Comparative Biology 

KA. Funk and Daniel R. Brooks 

SMITHSONIAN INSTITUTION PRESS 

Washington, D.C. 

1990 
ABSTRACT 

Funk, V.A. and Daniel R. Brooks. Phylogenetic Systematics as the Basis of Comparative 

Biology. Smithsonian Contributions to Botany, number 73, 45 pages, 102 figures, 12 tables, 

199O.-Evolution is the unifying concept of biology. The study of evolution can be approached 

from a within-lineage (microevolution) or among-lineage (macroevolution) perspective. 

Phylogenetic systematics (cladistics) is the appropriate basis for all among-liieage studies in 

comparative biology. 

Phylogenetic systematics enhances studies in comparative biology in many ways. In the study 

of developmental constraints, the use of such phylogenies allows for the investigation of the 

possibility that ontogenetic changes (heterochrony) alone may be sufficient to explain the 

perceived magnitude of phenotypic change. Speciation via hybridization can be suggested, 

based on the character patterns of phylogenies. Phylogenetic systematics allows one to examine 

the potential of historical explanations for biogeographic patterns as well as modes of speciation. 

The historical components of coevolution, along with ecological and behavioral diversification, 

can be compared to the explanations of adaptation and natural selection. Because of the 

explanatory capabilities of phylogenetic systematics, studies in comparative biology that are 

not based on such phylogenies fail to reach their potential. 

OFFICIAL PUBLICATION DATE is handstamped in a limited number of initial copies and is 

recorded in the Institution's annual report, Srnithonhn Year. SERIES COVER DESIGN: Leaf 

clearing from the katsura tree Cercidiphyllum japonicum Siebold and Zuccarini. 

Library of Cmgrcss Cataloging-in-Publication Diaa 

Funk, V.A (Vicki A.), 1947- 

PhylogmttiC ryrtcmatics as tk basis of canpamtive biology / V.A. Fbk and Daniel R. Brocks 

Included bibliogrcrphical refez- @. ) 

1. F'hylogmy. 2 Evdution-RdM&cdoIogy. 3. Cladistic analysis. I. Brooks, DR. (Daniel R), 1951-. 

QKlS2747 no. 73 a fQH367.51 581 pdcu) [575] 89-600291 

p. crn.+Smithsonh cor*ributiom to botany : no. 73) 

Sufi of Docs. no.: SI 1.29:n 

IL Title. IIL Saics. 
Contents 

Page 

Introduction ........................................ 1 

Acknowledgments ................................... 2 

Comparative Methods ................................... 3 

Consensus Analysis ................................... 6 

Character Coding .................................... 6 

Methods and Research Programs in Macroevolution ................... 8 

Developmental Constraints .............................. -8 

Hybridization ..................................... 12 

Biogeography ..................................... 15 

Sympatric Speciation ................................ 25 

Allopatric Speciation. Model I ........................... 25 

Allopatric Speciation. Model I1 .......................... 27 

Parapatric Speciation ................................ 29 

Historical Ecology ................................... 29 

Coevolution ..................................... 29 

Ecological and Behavioral Diversification ..................... 36 

Concluding Statement .................................. 42 

Literature Cited ...................................... 43 

Speciation ....................................... 25 

iii 

Phylogenetic Systematics as the Basis 

of Comparative Biology 

V.A. Funk and Daniel R. Brooks 

Introduction 

Along with virtually all biologists we consider evolution to 

be the unifying concept of biology. It follows that a wide 

variety of biological explanations would benefit from reference 

to evolutionary relationships and that studies without such a 

basis are missing an element that would greatly increase their 

information content. 

The study of evolution can be viewed from a within-lineage 

or among-lineage perspective. Within-lineage patterns, resulting from processes operating on time scales less than the 

duration of indvidual species, are referred to as “microevolution.” This is the focus of population genetics and population 

There seems to be general agreement that evolutionary 

patterns exist among-lineages. These are frequently identified 

as macroevolutionary patterns, and are usually the focus of 

systematic analyses. Macroevolutionary patterns include a 

variety of phenomena such as increasing morphological 

complexity over time, morphological trends, repeating biogeographic patterns, and developmental and phylogenetic constraints. Controversy remains about the processes responsible 

for these patterns and, by extension, about the best methods 

for detecting them (see Cracraft, 1985a, and references therein). 

In the past, two positions have been set forth. Goldschmidt 

(1940) and Eldredge and Cracraft (1980), among others, 

championed the view that macroevolutionary processes were 

qualitatively different from microevolutionary processes, and 

were independent of them. In contrast, Dobzhansky (1937), 

Mayr (1942), and Simpson (1944) forged a consensus that 

macroevolutionary patterns are simply microevolutionary 

patterns “writ large”; hence, there are only microevolutionary 

VA. Funk, Department of Botany, National Museum of Natural 

History, Smithsonian Institution, Washington, D.C. 20560, USA, and 

Daniel R. Brook, Department of Zoology, University of Toronto, 

Toronto, Ontario, M5S 1AI Canada. 

Review Chairman: L. Skog. Smithonian Institution. 

ecology. 

processes. They argue that perception of macroevolutionary 

patterns is merely a result of the coarse scale of systematic 

studies: “There is only a difference in degree, not one of kind, 

between the two phenomena. They gradually merge into each 

other and it is only for practical reasons that they are kept 

separate” (Mayr, 1942:291). Eldredge (1985) termed this the 

“extrapolationist model of macroevolution.” 

A viewpoint that borrows from these two extremes is now 

emerging. Under this view, evolution results from a variety of 

interacting processes, variously construed as forces or constraints. These processes operate on differing time scales, so 

their expression may be found in within-lineage patterns or in 

among-lineages patterns. Microevolution and macroevolution 

are parts of a more inclusive whole represented by the 

hierarchical nature of biological systems (e.g., Salthe, 1985; 

Eldredge, 1985; Brooks and Wiley, 1986, 1988). From this 

perspective, macroevolutionary patterns are those that are 

better explained by reference to phylogeny than by reference 

to local environmental conditions; microevolutionary patterns 

refer primarily to local adaptive responses. 

Macroevolutionary processes, because they operate so 

slowly, define the boundaries within which microevolution 

takes place. That is, macroevolutionary properties constrain the 

way in which, and the extent to which, populations can respond 

to local selection pressures over short time periods. The 

emphasis is not on a reductionist explanation but on a more 

holistic interpretation-on the relative contributions of processes operating at different rates rather than on the ability of 

one process to account for everything. 

If there are macroevolutionary processes, or if there are 

microevolutionary processes having among-lineage effects 

(such as selection or competition acting in the past), it is 

important to estimate just how prevalent and influential these 

are. Macroevolutionary patterns, no matter what causes them, 

are manifested by persistent ancestral traits in descendant 

species. The current jargon for such occurrences is phylogenetic constraints, or historical constraints (or even phylo1 
2 SMITHSONIAN CONTRIBUTIONS TO BOTANY 

genetic inertia). Phylogenetic trees produced by phylogenetic 

systematic analysis provide explicit summaries of putative 

historical constraints. Phylogenetic systematics refers to the 

method of Hennig (1966), which builds patterns of relationship 

among taxa based on shared derived characters. This method 

contrasts with traditional systematics, which has no specific 

method of determining relationship. The trees produced by this 

method can be used to partition out within-species and 

among-species evolutionary patterns. 

The systematist’s null hypothesis is the assumption that as 

more and more characters are sampled, no consistent pattern 

of relationships will emerge; as more and more characters are 

added to the tree you will continue to fail to have any resolution 

of the tree and the polytomies will persist. When a consistent 

pattern (or group of similar patterns) does emerge, the 

systematist rejects the null hypothesis in favor of the pattern(s) 

discovered. The accepted pattern, described in a cladogram, is 

the working hypothesis of historical order among species that 

can be used in macroevolutionary studies. 

If one is skeptical about the existence of macroevolutionary 

processes, or of microevolutionary processes having amongspecies effects, the appropriate null hypothesis is that no causal 

agents (processes: forces or constraints) will show amongspecies correlations with the group being studied. That is, the 

cladogram is only a record of microevolutionary processes 

having no macroevolutionary effects. The template for 

comparisons with respect to this null hypothesis is the 

cladogram; the putative micro- and macroevolutionary processes are mapped onto the cladogram. Any autapomorphy can 

be investigated as a microevolutionary process. Any putative 

causal agents that behave like synapomorphies on the 

cladogram refute the null hypothesis. 

Alternatively, if one thinks that phylogenetic constraints 

play a major role in evolution, the appropriate null hypothesis 

is one of historical structuralism (Brooks and Wiley, 1986, 

1988). Under this view, putative causal agents that show 

homoplasious or autapnorphous correlations with the phylogeny of the taxa being studied refute the null hypothesis and 

lead one to accept current microevolutionary causes as 

explanatory. In this case, the template for comparisons with 

the null hypothesis is also the cladogram. 

If one adopts the evolutionary view just discussed, it is more 

important to be able to document the influences of a variety 

of causal agents at particular points in the phylogeny than it is 

to rry to reduce all of phylogeny to “microevolutionary” or 

“macroevolutionary ” processes. 

Evolutionary explanations that make explicit reference to 

phylogeny are not widely used today. One reason is the belief 

that there is an inherent circularity in the methods of producing 

estimates of evolutionary relationships from which such 

explanations would be drawn. Specifically, it is homologous 

traits that indicate phylogenetic relationships and yet it is 

phylogenies that are used to determine homology. Phylogenetic 

systematics (Hennig, 1966) represents an approach to reconstructing phylogeny that avoids this circularity. One must only 

assume the existence of “descent with modification.” 

There are several components to the methodology developed 

by Hennig (1950, 1966). Initially, nonphylogenetic criteria 

(such as those of Remane, 1956; see Wiley, 1981) are used to 

determine homology. One asks whether two traits that look 

“the same” are “the same,” and one assumes homology 

whenever possible. Having used nonphylogenetic reasoning 

to postulate homology, taxa are grouped according to the 

homologies they share. The result is a phylogenetic tree with 

various groupings of taxa diagnosed by the appearance of a 

homologous trait. For virtually every study, most presumed 

homologies conform, to a greater or lesser degree, to a 

predominant pattern, which then provides the phylogenetic 

hypothesis. Those traits originally thought to be homologous 

that do not conform to the accepted tree are reinterpreted as 

nonhomologies. That is, presumed homologies are determined 

by nonphylogenetic methods, and are used to construct 

phylogenetic trees that in turn determine which of the presumed 

homologies are not evolutionary homologies. By avoiding 

methodological circularity, phylogenetic systematics produces 

patterns of evolutionary relationships that can serve as 

independent explanatory templates for other evolutionary 

studies. As a result, we think phylogenetic systematics bridges 

the disciplines of developmental biology, ecology, evolution, 

and systematics. Indeed, it is our contention that phylogenetic 

systematics is the appropriate context for all studies in 

comparative biology. 

It is not our intention here to provide an introduction to 

phylogenetic systematics. The three central terms of phylogenetic methodology-apomorphy, monophyly, and parsimonyhave been clearly discussed elsewhere (e.g., Eldredge and 

Cracraft, 1980; Farris, 1974,1983; Funk, 1984; Humphries and 

Funk, 1984; Oosterbrock, 1987; Platnick, 1977a, 1979; Wiley 

1981). 

In this paper, we first present several relatively new 

techniques for comparing phylogenies. However, the major 

intention of this paper is to show how phylogenetic systematics 

can be used in comparative methods that have been developed 

for documenting macroevolutionary patterns. 

ACKNOWLEDGMENTS 

The authors thank the Smithsonian Institution Short-Term 

Visitor Program, which allowed the junior author (DRB) to 

travel to the Smithsonian to begin this manuscript; the Natural 

Sciences and Engineering Research Council (NSERC) of 

Canada for grant A7696 (to DRB); the Smithsonian Institution 

Research Opportunitites Fund, which enabled the senior author 

(VAF) to travel to the University of British Columbia; and the 

following individuals for their reviews of various drafts: G. 

Bern, P. Cannell, G. Deets, K. Fauchald, D. Mcknnan, R. 

Mooi, J. Nix, R. O’Grady, S. Salthe, C. Starr, E. Wiley; plus 

J. Savage and D. Hillis and the University of Miami, 

Department of Biology staff and graduate students. Also, a 
NUMBER 73 

P 

3 

R P 

FIGURES 1-2.--Examples of two equally parsimonious distributions of the 

same apomorphic character. 1, The apomorphy gained and subsequently lost. 

2, The character gained twice. In the PAUP computer program for generating 

phylogenies, the accelerated transformation option will produce Figure 1 and 

the decelerated transformation option will yield Figure 2. 

ABCD 

3 ++oo 

+ + 0 0 + + 0 0 

A B C D A B C D 

FIGURES 3-5.--Cladognims demonstrating the diffemce between independent 

origin and mapping of characters. 3, Distribution of two traits (0, t) among 

four species (A-D). 4, Cladogram if each trait occurred independently in each 

species. 5, Cladogram if trait ”+” occurred in common ancestor of all four 

species, and trait “0” arose in common ancestor of C and D. 

special thanks to D. Futuyma and B. Simpson for reviewing 

the completed manuscript and providing numerous corrections, 

additions, and comments. The listing of these reviewers names 

is not meant to imply their agreement with the various 

assertions in this paper. 

Comparative Methods 

There are two kinds of “comparative methods.” The first 

consists of finding a trait of interest in a particular species, 

then examining unrelated species having similar ecological 

requirements to see if any of them have evolved similar traits. 

If they have, that lrait may be considered to be a convergent 

adaptive response to a common selection regime (see Alcock, 

1984). An example is the succulent nature of the stems and/or 

leaves of many unrelated plants that grow in deserts. Another 

is the blindness of many animals that live in perpetual darkness. 

The second comparative method is rooted in the discipline 

of systematics. It consists of documenting genealogical 

6 / 

FIoURE 6.-Phylogeny of ground squirrels plus prairie dogs showing 

distribution of run-jump behavior. As represented on this tree, the m-jump 

behavior arose in common ancestor of Richardson’s ground squirrels (R) and 

prairie dogs (P). All other ground squirrels (G) lack this behavior. (After 

Dobson. 1985.) 

relationships and then asking if shared traits arose in a common 

ancestor and have persisted, or if they arose independently in 

the species of interest. This method can be referred to as the 

phylogenetic comparative form. 

For the first kind of comparative method, an assumption is 

made that similarities arise through adaptive response to 

common selection pressures. No provision, however, is made 

for animals that live in darkness but can still see and for plants 

that grow in the desert and are not succulent. Also, no explicit 

provision is made for explaining some similarities as persistent 

ancestral traits, although such “phylogenetic constraints” are 

sometimes explained post hoc as the result of selection in the 

past. And yet, if replication rates are higher than mutation rates 

(a microevolutionary observation), we might expect more 

persistent ancestral traits than newly evolved traits to be 

expressed in similarities among related species (a macroevolutionary pattern). Therefore, we believe that the appropriate 

general comparative method for evolutionary biology, and 

certainly for studies in macroevolution, is the second type, the 

phylogenetic form. This agrees with the argument of Hennig 

(1966), who asserted that the preferred “general system” for 

biology should be one based on phylogeny. 

There are two general ways to use comparative phylogenetics to examine macroevolutionary patterns. One way to 

use cladograms involves comparing more than one cladogram 

to see if there is evidence of processes affecting more than one 

lineage at a time. Within this realm of comparing cladograms, 

we may ask two different types of questions. 
4 SMITHSOMAN CONTRIBUTIONS TO BOTANY 

TABLE 1.4omponents for Figures 7 and 8. 

Figure 7 Figure 8 

EFG 

CD 

CDEFG 

BCDEFG 

ABCDEFG 

EF 

EFG 

CDEFG 

BCDEFG 

ABCDEFG 

A B C D E F G 

TABLE Z.-Canpents for Figures 14 and 15. 

Figure 14 Figure 15 

AF 

AB AFB 

ABC AFBC 

FG 

EFG EG 

DEFG DEG 

ABCDEFG AFBCDEG 

A B C D E F G 

7 / 

A B C D E F G A C D E F G 

FIGURES 7-10.40nsensus Trees. 7 and 8, Two alternative cladograms for the same seven ma. 9, Adams 

consensus tree for Figures 7 and 8. 10, Strict consensus tree for Figures 7 and 8. (See Table 1.) 
NUMBER 73 5 

A B C D A C B D A B C D 

FIGURES ll-13.-Consensus trees. 11 and 12. Two dadograms for the same four ma. 13, Adams and strict 

consensus trees identical for Figures 11 and 12 

A B C D E F G A F B C D E G 

14 

A B C 

16 

F D E G A B C D E F G 

17 

FIGURES 14-17.-Consensus trees. 14 and 15, Two dadograms for the same swen taxa. 16, Adams consensus 

tree for Figures 14 and 15. 17, Strict consensus tree for Figures 14 and 15. (See Table 2.) 
6 SMITHSONAN CONTRIBUTIONS TO BOTANY 

We may ask what parts of different cladograms agree with 

each other (or conversely, what parts of cladograms are 

responsible for any ambiguity). Alternatively, we may ask how 

the history of one clade or of a set of areas explains the history 

of another clade or clades. Portions of the cladograms that 

behave as homologies are the historically determined variation 

(macroevolutionary contribution) and portions that behave as 

homoplasies are the proximally determined variation (microevolutionary contribution). 

The second way is to map a trait of interest on the cladogram 

(Figures 1 and 2) and to estimate both when, and how many 

times, a trait arose in the group being studied (Figures 3-5). 

Macroevolutionary patterns that emerge from this level of 

analysis are those affecting particular clades. Dobson (1985) 

used just such a procedure when commenting on the evolution 

of the “run-jump” behavior found only in prairie dogs and the 

Richardson’s ground squirrel. His hypothesis was that the 

run-jump behavior is a result of a common history of the two 

groups. He tested the hypothesis by mapping it on the 

phylogeny for ground squirrels and prairie dogs. Dobson found 

that Richardson’s ground squirrel is more closely related to the 

prairie dog than to other ground squirrels (Figure 6), thereby 

supporting, through parsimony, the common history hypothesis. 

CONSENSUS ANALYSIS 

Consensus trees provide a summary when more than one 

cladogram is available. Sometimes the topology of the 

consensus tree will be the Same as one of the original 

cladograms, but it often contains branching sequences not 

found in any of the original ones. Although consensus trees are 

not a valid summary of the data and should not be used as 

such (Miyamoto, 1983), they are an excellent way to locate 

problem taxa and characters and to illustrate areas of agreement 

and nonagreement. 

For our purposes there are two basic types of consensus 

trees: Adams consensus trees (ACT, Adams, 1972) and strict, 

or Nelson, consensus trees (NCT, Nelson, 1979, 1983). They 

differ in the manner in which they handle conflicting data. An 

Adams tree will give the highest resolution possible when there 

is no conflict in the data and a strict consensus tree will give 

only the branching sequences that are identical on all 

cladograms under consideration. For instance, Figures 7 and 8 

are two alternative cladograms for the same seven taxa, A-G. 

The Adams tree (Figure 9) is better resolved than either of the 

cladograms because neither 7 nor 8 conflicts with the other. 

The NCT (Figure 10) recognizes only clades that are present 

in both trees. In some cases the Adams tree and the strict 

consensus tree will produce the Same result (Figures 11-13). 

In other cases they will be very different. For instance, Figures 

14 and 15 have one taxon that changes position (taxon F); in 

doing this it changes all of the monophyletic groups on the 

cladogram so that the Adams tree (Figure 16) has a trichotomy 

at the base but the strict consensus tree has no resolution 

possible (Figure 17). These two types of consensus analysis 

do not give conflicting information, they answer different 

questions. An Adams tree answers those questions about which 

the clades are not in conflict, while a strict consensus tree 

provides information only on those areas of the cladograms 

that are identical. 

Alternative trees can be compared by “matching” the 

“components” (sensu Nelson, 1983) of the different trees. A 

component is any monophyletic group on the cladogram. Table 

1 provides the components for Figures 7 and 8. There are five 

components, four of which are identical in the two lists (EFG, 

CDEFG, BCDEFG, and ABCDEFG). A strict consensus tree 

contains only the four identical components (Figure 10). An 

Adams tree contains these four components as well as 

components EF and CD because they do not conflict with each 

other. Table 2 provides the components for Figures 14 and 15. 

Even though there are no identical components, it is clear from 

the listing that taxon F is causing the lack of agreement, 

demonstrating that even when the strict consensus tree 

approach does not produce a tree, it can indicate the 

problematic taxa. 

CHARACTER CODING 

Species co-occur in various kinds of associations. Geographically co-occuring species are sympatric, ecologically 

associated ones can be synecological, syntopic, or even 

symbiotic. Each of these association is thus diagnosed by its 

component species. If the associations play a role in the 

evolution of any of these diagnostic species, the phylogenies 

of the various groups will covary with respect to the 

associations. 

In terms of phylogenetic analysis, this is accomplished by 

treating each cladogram as a multistate character of the 

association (considered “taxa,” be they areas, communities, 

hosts, etc.). Brooks (1981) first proposed this approach for 

studies in coevolution. All “characters” (cladograms coded as 

multistate characters) are then placed in a common data matrix. 

The data matrix can be handled in one of two ways. (1) Either 

it can be mapped onto the host phylogeny, in which case 

characters that covary (act as homologues) share a common 

history with respect to the taxa, or (2) a phylogenetic systematic 

analysis can be performed. In the latter approach, a cladogram 

(or cladograms) of “taxa” is produced with portions of the 

various phylogenies used as characters (for examples see 

“Biogeography,” below). 

There are general methods available for converting a 

phylogenetic tree into a matrix of unit characters: Additive 

Binary Coding (ABC), Redundant Linear Coding (RLC), and 

Nonredundant Linear Coding (NLC). For a more complete 

treatment, including assessments of the strengths and drawbacks of the methods, see O’Grady and Deets (1987) and 

O’Grady et al. (in press). 

In ABC every node on the vee is labeled. In Figure 18 there 

are four terminal taxa (A-D) and three internal nodes @a). 
NUMBER 73 

Taxa 

A B C D 

Codes 

AB CD E F G 

7 

A 

B 

C 

D 

A 0 C D A B C D A B C D 

10 0 0 0 0 1 

01 0 0 0 1 1 

00 1 0 1 1 1 

00 0 1 1 1 1 

21 / 

Taxa 

FIGURES 18-21.-Three ways of ”mapping.” 18, Phylogeny with nodes labeled. 19, Tree constructed from ABC 

representation. 20, Tree constructed from RE representation. 21, Tree constructed from NLC representation. 

(See Tables 3-5.) 

Codes 

A B C D 

TABLE 3.-ABC coding for Figure 18. 

TAELE 4.-RLC coding for Figure 18. 

I 

TABLE 5.--NLC coding for Figure 18. 

~~ 

Codes 

Taxa A B C D ~ ~ 

A 1 0 0 1 

B 0 1 0 2 

C 0 0 1 3 

D 0 0 0 4 

The matrix values are determined by assigning a “1” code to 

every state lying along the minimum path between each taxon 

and the base of the tree. For example the minimum path for 

taxon D passes through D, E, F, and G, and each of those is 

coded as “1” for taxon D (see Table 3). The data matrix can 

be checked by using it to produce a tree (Figure 19), which 

indeed is identical to Figure 18, with each branch point 

supported by “characters.” In RLC each terminal branch on 

the tree becomes the terminal state in a linear transformation 

series constructed as the minimum path from the base of the 

tree. Every transformation series starts as a “1” state at the 

bottom node of the tree and changes at every nonterminal 

branch as it passes up the tree to the terminal state. For 

example, in RLC coding of Figure 18, taxon D has a code of 

“4” for D because there are three internodes between D and the 

base; it also shares three internodes with taxon C so C has a 

“3”; it shares two internodes with taxon B so it has a “2“ for 

B; and it shares one internode with A so it has a “1” for A. 

The code for taxon D is, therefore, “1234.” Taxon B has a “1” 

for A because it shares one internode with A; it has a “3” for 

B because it shares three internodes with taxon B; and it has a 

“2” for C and a “2” for D because it shares two internodes with 

both. The code for taxon B is “1322” (Table 4). Figure 20 is 

the diagram produced from the RLC data matrix (Table 4). 

NLC is similar to RLC in that each terminal branch on the 

tree becomes the terminal state in a linear transformation series 

construed as the minimum path. However, it differs in that 

only one of the terminal taxa goes all the way to the base of 

the tree. This is referred to as the major axis and it can involve 

any one of the terminal taxa. The other transformation series 

(minor axes) start from the point at which they branch off from 

the major axis. In Figure 18, if D is the major axis it would 

be the only taxon coded all the way up the tree, so D would 

have a “4.” Because A, B, and C are coded only from the point 

that they intersect with this axis, taxon D would have a “0” for 

all three of these and the code for taxon D would be ‘W 

(Table 5). Taxon B would have a “2“ for D because it shares 

two internodes with taxon D and a “1” for B because it has 

one internode between taxon B and the point at which it 

intersects the main axis. The code for taxon B would be “0102” 
8 SMITHSONIANCONTRIBUTIONS TO BOTANY 

(Table 5). Figure 21 is the tree resulting from Table 5. 

According to O’Grady and Deets (1987) the NLC method is 

more difficult to understand but eliminates the large data sets 

resulting from ABC and avoids the weighting of the RLC 

method. The ABC and the NLC give the same results, with the 

ABC being easier to use and the NLC being more economical. 

Once a cladogram has been converted into a data matrix, it 

can be mapped (placed as characters) on an existing phylogeny 

(the existing phylogenetic pattern is maintained and data from 

the matrix are placed on it in the most parsimonious manner), 

or on an area or host cladogram, or it can be combined with 

data from other trees to produce a summary diagram. We will 

show applications of such analyses in studies involving 

questions on biogeography and coevolution. 

An important consideration in interpreting the results of 

mapping phylogenies concerns homoplasies. Homoplasious 

Occurrences can be interpreted either as similar but separately 

derived origins of a trait (parallelism) or as a single origin of 

the derived trait with a secondary appearance of the 

plesiomorphic condition (character loss or reversal). When 

heritable traits of organisms are used to construct phylogenetic 

trees, parallelisms sometimes can be distinguished from 

reversals by developmental studies. For example, all cases of 

paedomorphosis will appear on the phylogeny as character 

lossesheversals, but not all character losses are a result of 

paedomorphosis (see “Developmental Constraints,” below). 

In other cases, a preference for parallel origins or losses can 

be made on empirical grounds using optimality measures like 

the F-ratio or the D-measure (Brooks, O’Grady, and Wiley, 

1986). However, when phylogenies are mapped together, as 

in biogeographic or coevolutionary studies, parallelisms and 

losses imply different evolutionary stories. Parallelisms in such 

cases are instances of colonization or host-switching, dispersal 

from original environmental contexts to new environmental 

contexts. Reversals imply episodes of extinction or loss of 

ecological association. We believe that the most conservative 

approach to take in this regard is one of providing explanations 

based on what we observe directly as often as possible. Only 

when other additional data are available, or when more efficient 

mapping can be obtained by postulating Occurrences for which 

we have no observations, should we involve such explanations. 

This means that in general we advocate interpretations of 

parallelisms over interpretations of losses (Figures 1 and 2) in 

all cases except when additional data are available or a more 

efficient mapping (i.e., a shorter tree) can be obtained by 

postulating reversals. 

Cases for which unrestricted interpretations of extinctions 

are appropriate involve groups that are “numerical relicts” 

(Simpson, 1944), remnants of once more diverse groups. 

Brooks and Bandoni (1988) have outlined phylogenetic, 

biogeographic, and ecological conditions which should be 

satisfied before one postulates that a given group is a numerical 

relict. Of course, one is also free to provide solution trees based 

on the maximum and the minimum number of extinctions 

consistent with the shortest solution tree, and conclude that the 

real story probably lies somewhere between the two extremes. 

In this regard, the different solution trees would be used in a 

manner similar to that of establishing confidence intervals. 

To summarize this discussion of consensus and the mapping 

method: (1) strict consensus illustrates which portions of the 

various cladograms are identical; Adams consensus highlights 

the portions of different trees that are consistent with each 

other, but not necessarily identical. Having performed a 

consensus analysis, one cannot then recapture the initial trees 

nor in most circumstances can one provide explanations for the 

conflicting portions of the trees. (2) Mapping methods are 

designed to provide explanations for all portions of the 

different trees. However, there is often more than one possible 

explanation for portions of phylogenies that do not covary. 

Accordingly, the results of mapping analysis may be less clear 

than those of consensus analysis, even though they encompass 

more of the available observations. 

Methods and Research Programs in Macroevolution 

DEVELOPM EWTAL CONSTRAINTS 

This topic encompasses the study of biases in the production 

of phenotypes that are not directly attributable to natural 

selection (Maynard Smith et al., 1985). Such biases can range 

from traits that are invariant in all viable members of a species 

to nonhomogeneous frequencies of occurrence of phenotypes 

characteristic of simple Mendelian loci. At the microevolutionary level, generally unacknowledged acceptance of developmental constraints allows prediction of expected phenotypic 

frequencies for particular traits, encompassing simple Mendelian ratios (where either a 3:l or 1:2:1 phenotypic bias is 

expected) to pleiotropic effects manifested in patterns of 

genetic variance/covariance. At the macroevolutionary level, 

developmental constraints are important sources of information 

about discontinuities in variation and about differences in 

magnitudes of phenotypic change during evolution (see e.g., 

Maynard Smith et al., 1985; Brooks and Wiley, 1986). 

Attempts have been made to explain biased phenotypic 

frequency by extrapolating from within-species processes to 

macroevolutionary, i.e., among-species, patterns. These attempts involve questions of developmental constraints versus 

selection. One solution is to identify all invariant traits (among 

species) and conclude that they are due to developmental 

constraints. This does not address the possibility that their 

invariance is due to selection operating in the past. Or, one 

could look for selectionist explanations for the frequencies of 

each trait, and assume developmental constraints only for those 

for which selectionist explanations cannot be found. This 

approach is vulnerable to the problem of assuming that because 

something functions it has been produced by selection, 

providing a “selectionist” explanation for everything (for a 

discussion, see O’Grady, 1984, 1986). Charlesworrh, Lande, 

and Slatkin (1982) have proposed that the influence of 

developmental constraints at the population biological level 
NUMBER 73 9 

can be documented by looking for correlations in genetic 

variance/covariance matrices. But even this advance does not 

address the questions of the origins of developmental 

Constraints, either in particular or as a general phenomenon, 

or of possible macroevolutionary effects of such constraints. 

Microevolutionary explanations can only explain persistence 

(stasis) rather than origin and modification (diversification). 

At the microevolutionary level, developmental constraints tell 

us only that the range of variation upon which selection acts 

is not the full range of possibilities, all equally represented. 

They are part of the explanation for the arena in which selection 

operates. 

As indicated above, there are two macroevolutionary 

questions that involve developmental constraints. The first is 

the question of discontinuous variation and the second is the 

question of differences in magnitudes of phenotypic change 

during evolution. These questions can be investigated fruitfully 

if phylogenies are available, because one can then estimate the 

meaning of “discontinuous” or “of great magnitude” with 

respect to closest phylogenetic relatives. Alberch et al. (1979) 

asserted that macroevolution is the relatively rapid attainment 

of significant morphological differences in evolving lineages. 

If some intermediate phenotypic states or combinations of 

states are unattainable due to developmental constraints, 

ascribing all discontinuities in variation to natural selection 

would overestimate the power of selection and would provide 

no reasons to consider other possible causal agents. References 

to a number of developmental studies that predict observed 

discontinuities without selection are given in Brooks and Wiley 

(1986, chapter 3; 1988). An accumulation of such effects could 

produce phenotypic differences among species that are quite 

marked. 

Two major approaches to examining the question of 

magnitudes of phenotypic change during phylogenesis have 

been tried. The first involves proposing archetype ancestral 

phenotypes and the second involves comparing sister lineages 

in phylogenies. We will consider the second approach here. 

Systematists have recognized for a long time that sister species 

are not equally dissimilar to the ancestor. Hennig (1966) called 

this the “deviation rule”: for any pair of descendant species, 

one will always resemble the ancestor more than the other. 

Traditional explanations for such states have stressed (1) 

differential adaptation under different selection regimes, and 

(2) founder effects. That is, dissimilar states are the result of 

different speciation modes. With the recent advent of interest 

in developmental constraints, we must now consider an 

additional possible contributing factor. The genetic and 

ontogenetic changes characteristic of a descendant population 

alone may even be sufficient to explain the perceived 

magnitude of phenotypic change in some cases. 

One major class of developmental constraints that has 

received recent attention is heterochrony. This is a general term 

denoting changes in timing of events during ontogeny. There 

are two reasons heterochrony is attractive to evolutionary 

biologists. The first is that genetic changes early in ontogeny 

could have major phenotypic effects. This means that 

significant morphological differences could be achieved 

through relatively small genetic changes, and such genetic 

changes could be subject to effective selection (i.e., they could 

be relatively free of pleiotmpic effects). Accepting this premise 

provides one way of reducing the concept of developmental 

constraints to standard microevolutionary processes and 

explanations. This also provides a mechanism whereby 

punctuated equilibrium could be explained as a wholly 

neo-Darwinian phenomenon (for recent attempts to provide 

such an explanatory reduction, see Charlesworth, Lande, and 

Slatkin, 1982; Stebbins and Ayala, 1984). 

The second reason heterochrony is attractive to evolutionary 

biologists is that amplification of small differences in initial 

conditions producing markedly different endpoints is highly 

characteristic of nonequilibrium thermodynamic systems operating under a variety of kinetic constraints (Brooks and Wiley, 

1986, 1988). If such processes characterize part of the 

production of phenotypic diversity in biology, evolution of 

such phenotypes would follow a “line of least resistence” 

determined by kinetic constraints, initial conditions (including 

phylogenetic history), and possible selective constraints. 

Robust evolutionary explanations would require partitioning 

out the relative contributions of each of these classes of causal 

agents rather than reducing phenotypic order to a single causal 

agent, such as selection or chemical kinetics. 

We use the general description of classes of heterwhronic 

changes proposed by Alberch et al. (1979). Their model 

assumes that an ancestral sequence can be construed as a 

trajectory characterized by a positive rate, “k.” The trajectory 

has a direction in time determined by a starting point, a, and 

endpoint, p, and a degree of complexity (usually construed as 

size and/or shape change), y. The trajectory has a positive slope 

appearing on a plane whose x-axis is time, with a and p 

indicated, and whose y-axis is complexity, denoted by values 

of ‘y. Thus, the trajectory is characterized by time-dependent 

(irreversible) increases in complexity, denoted by the rate “k.” 

Using this framework, heterochrony can be divided into two 

major classes, peramorphosis and paedomorphosis. Peramorphosis occurs when k increases, or when developmental timing 

(the difference between a and p) lengthens for a given y 

paedomorphosis occurs when k decreases, or when developmental timing shortens for a given y. There are three types of 

peramorphosis. If k increases, the process is termed acceleration; a portion of development has occurred more rapidly than 

in the ancestral condition. If a is displaced to the left, the 

length of time of development is increased by starting earlier; 

this is termed predisplucement. If p is displaced right, the 

length of time of development is lengthened by continuing 

longer; this is termed hypermorphosis. Also, there are three 

complementary types of paedomorphosis. If k decreases, the 

process is neoteny: a portion of ontogeny has proceeded slower 

than in the ancestral condition. Displacement of a to the right 

initiates a portion of ontogeny later than in the ancestral 

condition; this is termed postdisplacement. Finally, progenesis 
10 SMITHSOMAN CONTRIBUTIONS TO BOTANY 

PERAMORPHOSIS 

01 P ff- P 

faster rate starts sooner 

ff -P 

stops later 

22 AC C E L E R AT I 0 N PREDISPLACEMENT HY PERMORPHOSIS 

PAEDOMORPHOSIS 

Y 

D- 1~~ , liLOOOOOOO 00°0 00°0 00°0 

0°‘ OOeO 

ff P 

slower rate 

-ff P 

starts later 

01 Pstops sooner 

23 NEOTENY POSTDISPLACE MENT PROGENESIS 

FIGUW 22-23.-Examples of the six categories of heterochronic changes. 22, The three types of changes 

representing peramorphosis, in that the descendant’s morphology is more developed than that of the ancestor. 

23, The three types of changes representing paedomorphosis, in that the descendant’s morphology is less 

developed than that of the ancestor. Alternations in the mte of developnent (k), its time (t) of initiation (a), or 

its time of cessation (p) can produce changes in the morphology (13 of the descendant (D), as compared to that 

of its ancestor (A). Dotted lines indicate ancestral “developmental trajectoy”; solid lines indicate heterochrdc 

derived trajeaories. (Modified from O’Grady, 1987.9. b.) 

occurs when j3 is displaced left, terminating development 

earlier than in the ancestral condition. Figures 22 and 23 

summarize these classes of effects. 

Fink (1982) pointed out that Alberch et al. (1979) did not 

indicate how one might estimate the ancestral condition from 

which all assessments of heterochrony in evolution might be 

made. Fink further suggested that the outgroup criterion from 

phylogenetic systematics might provide an appropriate estimate of ancestral conditions in many cases, and provided 

examples of distributions of ontogenetic data on phylogenetic 

trees that correspond to the six forms of heterochrony listed 

above. Figure 24 shows a generalized view of the phylogenybased observations that could lead to explanations of various 

forms of heterochrony in the evolution of characters. 

O’Grady (1987) used phylogenetic systematics and laboratory manipulations of development to apply Fink’s (1982) 

formalism. The organisms used represent a monophyletic 

group of digeneans (parasitic flukes) in the genus Glypthelm’ns, 

inhabiting frogs and toads; Figure 25 is the phylogenetic tree 

for this group. One species, G. intestinalis, differs markedly 

from its sister species, G. shastai, and the rest of the members 

of its clade, by having an unusually attenuated hindbody (the 

portion of the body posterior to the ventral sucker, Figure 26). 

By raising G. intestinalis and one of its close relatives, G. 

quieta, under the same laboratory conditions, O’Grady was 

able to compare plesiomorphic and apomorphic developmental 

trajectories for the hindbody (Figure 27). According to the six 

categories established by Alberch et al. (Figure 24), the 

hindbody of G. intestinalis evolved by acceleration, a form of 

peramorphosis. O’Grady (1987) was able to confirm this 

through laboratory manipulations (raising G. intestinalis in an 

abnormal host, which retarded development) and produced 

specimens of G. intestinalis exhibiting the plesiomorphic 

hindbody condition. This amounts to experimentally produced 
NUMBER 73 11 

A B C D 

x-P-P-c x-P-P-c x-P-P-c 4f 

- 

x-P-c-c acceleration 

X- P- P-C- D hypermorphosis 

P-P-c predisplacement 

X-P-P-P-C neoteny 

x-P-P progenesis 

x-x-P-P postdisplacement - 

24 

FIGURE 24.4eneralized view of phylogeny-based observations indicating 

evolution by means of six different modes of heterochrony. A, B, C exhibit 

plesiomo@uc developmental trajectory beginning with initial state x 

developing into state p. fhhing with state c * = possible apomorphic 

conditions in D resulting from six different modes of hetemhronic changes 

in evolution. 

25 / 

FIGURE Z.--Phylogenetic tree of a monophyletic group within the digmetic 

trematode genus Cfypthefmins (parasitic flukes). This was the only tree 

produced. 

houw 

26 

26.-Venual 

w 

view of two species of Glypthefmins. Left, G. shastai, 

which has the plesiomorphic condition. Right, G. intestinalis, with a long hind 

body, which is the apomorphic condition. Scale bar = 1 mm. 

neoteny, the form of paedomorphosis that is coupled with 

acceleration. Phylogenetic systematics allowed O’Grady to 

determine the plesiomorphic condition of the group. Likewise, 

Mooi (1987) used a phylogeny to determine plesiomorphic 

conditions in sand dollars and thereby identify progenesis and 

neoteny. 

A recurring theme in comparative biology is the question 

of the relationship between the genotype and the phenotype. 

One way to approach this problem is to compare cladograms 

constructed from genotypic data (e.g., macromolecular, nucleic 

acid sequence) with those produced from phenotypic data (e.g., 
12 

0.8 -. 

0.7 -. -I 

i- 

\ 

-I 

I 

m 

m 

0.6 -I 

0.5 -I 

SMITHSONIANCONTRIBUTIONS TO BOTANY 

:/ in,qu 

@testinah 

shastqi 

fU 

gl&g 

californiensis 

1 I I I 1 + I -------- I 

META 1 4 8 12 

27 MA1 

FIGURE 27.-Plesimorphic and apomorphic developnental trajectories for the hindbody of two parasitic flukes. 

Values for the mean ratio (with means) of hindbody length to total body length (HBIJl’BL) in specimens of the 

two species at metacercariae (META) and at 1,4,8, and 12 months after infection (MAI) in Ram pretiosa, for 

Haplometrana intestinalis (in), and in Rana pipiem, for Glypthelmim guieta (qu). The values for mature adults 

of other species of Glypthelm’ns, of unknown ages. are given at 12 + MAI. (Redrawn from O’Grady, 1987a. b.) 

morphology, karyology). Hillis and Davis (1986) presented a 

summary phylogeny for North American ranid frogs based on 

information taken from allozyme, immunological distance, 

morphology, and rDNA data (see also Hillis, Frost, and Wright, 

1983). Figures 28-31 are cladograms based on each type of 

data; Figure 32 is the summary tree. For these data, both Adams 

consensus and mapping methods yield Figure 32. Strict 

consensus analysis finds only two identical components in all 

four trees: (1) the clade containing “tarahumme group” and 

“palmipes group,” and (2) the clade formed by the “montezumae group,” “areolata group,” “pipiens group,” and 

“berlandieri group.” These two components indicate instances 

in which evolutionary change occurred in all four data sets on 

the same internode. Figure 32 has 19 branches, 10 of which 

are characterized by phenotypic as well as some form of 

genotypic change. All morphological changes are correlated 

with some genotypic change but not all genotypic change is 

accompanied by phenotypic change. None of the four data sets 

conflicts with any of the others (except for a minor ambiguity 

in the immunological distance data), but neither does any of 

them alone produce the summary tree (Figure 32). Therefore, 

for the data examined, there is evidence of correlated genotypic 

and phenotypic change, and some evidence of genotypic 

change without phenotypic change. 

HYBRIDIZATION 

In an evolutionary sense, hybrids are organisms descended 

from parents with different lineages. As such, they fall outside 

of our normal idea of “inherited traits” in that characters from 

different lineages show up in the same individual. This 

movement of characters increases the “evolutionary noise” and 

makes the determination of phylogenies more difficult. There 

are three classes of hybrids. One can use the term hybrid to 

refer to offspring of parents from different demes or 

populations of the same species, but this is usually an 

accounting device used in studies of gene flow and need have 

no macroevolutionary connotations. There are two classes of 

interspecific hybrids-those that must be continually produced 

by interspecific matings and those that can persist on their 

own. Funk (198 1,1985) summarized various genetic combinations characteristic of hybrids. In some cases, the hybrid 

population consists of F1 generation organisms that are either 

infertile or which produce F2 offspring that are developmentally deficient. Such “hybrid swarms” must be replenished 

continually by reproduction between the two parental species. 

These populations are “evolutionary noise.” 

In the second class of interspecific hybrids, some hybrids 

are capable of reproducing and persisting on their own. 

However, this ability to persist does not guarantee that they 
NUMBER 73 

will continue as independent evolutionary lineages. If the 

reproductive compatibility that allowed the parents to produce 

the hybrid in the first place does not disappear in the hybrid, 

it is possible that one or both of the parental species will 

assimilate the hybrid. Depending on how long the hybrid 

population persisted prior to such assimilation, one could 

construe this as a “reductive speciation event.” If the hybrids 

are capable both of persisting on their own and of withstanding 

assimilation by either parent, they will be capable of persisting 

as distinct evolutionary species. 

There are three phenotypic and ecological outcomes of 

speciation by hybridization. In the first case, the hybrids can 

segregate strongly with one parent (have most of the 

characteristics of one parent). When this happens, the hybrids 

are subject to the same selection regime as the parent. Since 

the parent species is already surviving in the environment, it 

is likely that the hybrids will survive as well. It is also possible, 

under such conditions, that interspecific competition will 

occur, since new genetic information has been added to the 

biota without enlarging the resource base used. In the second 

case, the hybrids may represent a mix of parental attributes, 

some of which may be intermediate in nature. Such hybrids are 

capable of surviving in a wider range of habitats than either 

parent, and should thus have a relatively good chance of 

survival. Although subject to a wider range of selection 

pressures, the flexibility of such hybrids should reduce the 

intensity of competition with either parent. Finally, the hybrids 

could represent a unique phenotypic and ecological system. 

In this case, survival should be more problematical, because 

the new combination must correspond to one allowed by the 

resource base available. However, such hybrids, if they survive, 

should face no competition from either parent. Thus, there are 

three pathways of survival open to species of hybrid origin. 

Each implies slightly different microevdutionary scenarios 

that can conceivably be tested, if one knows who the parental 

species were and the degree of phenotypic similarity between 

hybrids and parents. These can be assessed using phylogenetic 

systematic analysis. 

Over the years various methods have been suggested for 

identifying hybrids. Most involve the recognition of some 

intermediate character or combination of characters. However, 

recent publications using phylogenetic systematics (Humphries, 1983; Funk, 1985). show that hybrids can have characters 

of one parent, of both parents, or of neither parent. 

It has been noted in the literature (Funk, 1985) that there is 

no reason to expect apomorphies from both parents to be 

expressed in the hybrid. Indeed, for this to be true, apomorphies 

would always have to be dominant over the corresponding 

plesiomorphy. For the sake of discussion, we will use a simple 

Mendelian example. If the apomorphy must be in the 

homozygous condition to be expressed, then all apomorphies 

not present in both of the parents will be in the heterozygous 

condition in the F1 and will not be expressed. In diploid 

hybrids the F2 would have a 1:2:1 and so on. Thus, some 

members of a hybrid would have apomorphies of the parents 

13 

and some would not. Indeed, any one organism would have 

the possibility of having any combination of the apomorphies 

of either parent. This condition is actually a good indication 

at the data gathering stage that the taxon under consideration 

is a diploid hybrid. Usually polyploid hybrids have the 

complete genome of both parents and so have the possibility 

of having all of the apomorphies of both parents. They usually 

express only a portion of the apomorphies possible to them 

because they inherit the genomes of both parents and so almost 

all characters are in the heterozygous condition. Hence, while 

they do not display all of the possible apomorphies, the ones 

they do express are usually more consistent from one individual 

to another than in diploid hybrids. 

As well as displaying a bewilderingly inconsistent array of 

apomorphies, diploid hybrids tend to exhibit quantitative 

characters that are intermediate between the two parents. 

Because of these traits diploid hybrids are sometimes easier 

to identify at the data gathering stage than are polyploid 

hybrids. But whether diploid or polyploid hybrids exist in a 

data set, phylogenetic systematics can be useful in generating 

hypotheses of hybridization, which can then be investigated 

using independent data such as pollen fertility, karyotyping, 

or geographic distribution. Crossing experiments are useful in 

“recreating the hybrid” and for demonstrating that the putative 

parents are indeed capable of producing viable offspring. 

However, crossing data cannot be used to determine closeness 

of relationship (Rosen, 1975). 

Funk (1985) presented many examples using cladograms to 

aid in the search for species of possible hybrid origin. A portion 

of one of those examples, a clade from the Enceliu study, can 

be used to demonstrate the various techniques. The clade has 

ten taxa and 12 characters (Table 6). The PAW computer 

program for phylogenetic analysis, written by David Swofford 

(Swofford and Maddison, 1987), produced 27 equally parsimonious cladograms, 15 of which were topologically different. 

Nearly all of the various branching patterns found in those 

cladograms can be represented in two cladograms (Figures 33 

and 34). A strict consensus analysis produced Figure 35 and 

an Adams consensus tree is identical to Figure 34. Figure 36 

is a summary diagram showing the various positions possible 

for these three taxa in all 27 cladograms. Figures 35 and 36 

indicate that taxa ASP, CAL, and CAN are located in more 

than one place on the cladograms. In addition, LAC and CAN 

have characters that are intermediate in nature, and FAR is 

characterized by three reversals (Figures 33 and 34). Based 

on the cladograms there are five ma that should be 

investigated as possible hybrids: ASP, CAL, CAN, FAR, and 

LAC. After examining the distribution and life history of these 

five taxa, three are supported as hybrids (ASP, CAN, and 

LAC). Examining the results of a phylogenetic analysis-both 

from the standpoint of character distribution and consensus 

tree construction-provides a method for indicating possible 

hybrids and their parents. Once a hypothesis of hybridization 

has been identified, it can be “tested” by information not used 

in the analysis. Some of the most useful types of information 
14 SMITHSONIANCONTRIBUTIONS TO BOTANY 

28 I 29 tD 

30 t' 31 I 

FIGURES 28-3 1.-Four cladograms for tar groups of North American ranid frogs, each produced using a different 

type of data. 28, Allozmne data. 29, DNA data. 30. Immunological distance data. 31, Morphological data. A = 

apomorphic allouxne character. D = apomorphic DNA character, I = immunological distance data, and M = 

apomorphic morphological character. AU taxon names follow the order found in Figure 32. 
NUMBER 73 15 

FIGURE 324ummary cladogram for 10 groups of North American ranid frogs (Figures 28-3 1). A = apanorphic 

allomme character, D = apanorphic DNA character, I = immunological distance data, and M = apanorphic 

morphological character. (Redrawn from Hillis and Davis, 1986.) 

are distribution, karyology, greenhouse hybridization studies, 

allozyme studies, pollen fertility, life history, and phenology 

studies. 

BIOGEOGRAPHY 

With the advent of theories of an evolving geosphere, 

especially of plate tectonics and continental drift, biogeographic distributions have become an important source of 

information about the ages of evolutionary lineages, complementing data from paleontology and molecular biology. 

Paradoxically, this new knowledge has also led to controversy 

about evolutionary explanations for geographic distributions 

of related species. 

The general microevolutionary processes deter mining geographic distributions are reproduction and dispersal. At any 

point in time a species’ distribution depends on the vagility of 

its members. In the absence of constraints on range expansion, 

we would expect all species distributions to expand over time. 

That is, if a species originates as a small peripheral population, 

there should be a direct correlation between the age of the 

species and the area it occupies. Because abiotic (temperature, 

rain fall, etc.) and biotic (reproduction and vagility) factors 

exist, such “age and area” estimates have been criticized and 

rejected by most biogeographers. In fact, most species exist in 

relatively small ranges, while a few notable exceptions are 

widespread. 

One common geographic distribution pattern is one in which 

the members of a given clade are allopatric or parapatric, and 

in which closest relatives occupy adjacent areas. If this pattern 

is the result of persistent microevolutionary processes, then 

dispersal into new areas accounts not only for the range 

occupied by the clade, but also for the particular pattern of 

occurrence of distinct species within the clade. The conven- 
16 SMITHSONIANCONTRIBUTIONS W BOTANY 

LAC VEN PAL CAN RAD FAR PHE CAL SC ASP 

LAC VEN PAL CAN RAD FAR PHE CAL SC ASP 

LAC VEN ASP CAL PAL CAN RAD FAR PHE SC 

LAC VEN ASP CAL PAL CAN RAD FAR PHE CAL SC ASP 

35 36 'i; 

FmUW 33-36.-Cladograms for a monophyletic group within the genus Enccliu. 33 and 34. Two dadograms 

that maximize the differences found in the 15 equally parsimonious cladograms. 35, Strict 43nsensus tm for 

Figures 33 and 34 (Adams consensus tree same as Figure 34). 36, Tree illustrating various positions for the four 

taxa that are found in more than one place on the 15 possible cladogms; dotted lines indicating multiple 

placement of terminal taxa. Taxon names are found in Table 6. * = intermediate characters. 

tional explanation is that as an ancestral species disperses, it particular area. 

encounters new selection pressures and, in adapting to these An alternative explanation is that new species arise within 

pressures, it evolves into various descendant species, each the range of older species, and push them, or are pushed, into 

characteristic of the particular environment found in a marginal habitats (see various papers in Nelson and Rosen, 
NUMBER 73 17 

TABLE 6.-Data matrix for one clade of Encelia (Compositae). ASP = E. 

aspergoh (S.F. Blake) Clark & Kyhas, CAL = E. cdifornica Nud, CAN = 

E. canescens Cavdes, FAR = E. farinosa Gray var. farinosa, LAC = E. 

laciniata Vasey, PAL = E. palmeri Vasey & Rose, PHE = E. farinara var. 

phenicodonta I.M. Johnson, RAD = E. radianr Brandegm, SC = undescribed 

taxon. VEN = E. ventorwn Brandegee. * = character of intermediate nature. 

(See Figures 33-36.) 

Characters 

Taxa 

ANC 

ASP 

CAL 

CAN 

FAR 

LAC 

PAL 

PH E 

RAD 

sc 

VEN 

- 

12 3 5 7 8 9 10 1213 1416 ~~ ~ ~~ 

0 0 0 1 0 0 0 0 0 0 0 0 

110101100000 

110101001000 

1 1 1 1 1 1 0 0 10 1*0 

0001 2000 1020 

11 11 0 1 0 1* 0 1 0 0 

11 1111001000 

11 112000 1020 

11 1120000000 

010100001001 

11 11 01 0201 01 

1981). Such “forced dispersal” results in the occurrence of 

relatively primitive members of a clade in marginal habitats. 

Regardless of the particular scenario one adopts, previous 

explanations have relied on discerning the center of origin of 

a group to provide an explanation of the biogeographic history. 

That is, find the center of origin and connect the distributions 

of the members of a given group-this is the dispersal route. 

Darwin and Wallace seemed to view speciation as a sympatric 

phenomenon and yet viewed dispersal as evolutionarily 

important as well. Mayr (1942, 1963) forged a synthesis of 

speciation and biogeography by proposing that most speciation 

events took place in peripheral habitats occupied by small 

populations established by chance dispersal over geographic 

barriers. 

So long as geographic stasis is assumed, there appears to 

be a smooth reduction from macroevolutionary geographic 

patterns to microevolutionary ones. However, the advent of 

acceptable theories of mobile geology forces evolutionary 

biologists to consider a second possible interpretation for 

macroevolutionary biogeographic patterns. That is, despite the 

ongoing process of dispersal in all lineages in all generations, 

it is possible that some descendant species occur where they 

do and are distinct from the other members of their clade 

because the changing geography isolated them. In this case, 

dispersal explains how the ancestral population got into the 

area where the descendant occurs, but geological changes 

explain why the descendant population became isolated and 

subsequently speciated. Speciation could occur as a result of 

the isolation without directional selection from new environmental conditions. This is a possibility that cannot be deduced 

directly from microevolutionary processes in biology, although 

it is certainly not inconsistent with any of them. In addition, 

if we are to allow the possibility of geological changes causing 

the isolation that led to speciation for one group, it is 

conceivable that a single geological episode could set the stage 

for speciation in a large number of co-occurring ancestral 

species. Thus, mobile geology inserts a macroevolutionary 

process into evolutionary theory. We now have more possible 

explanations, and the possibility that what explains one set of 

distributions may or may not explain another. 

One assumes that a biogeographic pattern common to more 

than one group requires an explanation involving a process 

that can affect many lineages in a similar fashion. If the 

biogeographic pattern is a historical one, the general explanation should also be historical. The greatest constraint on this 

kind of research is a paucity of well-documented phylogenies. 

This has led some scientists to accuse systematists of culling 

their data, using only those few out of many phylogenies that 

showed the general patterns (Simberloff, Heck, McCoy, and 

Connor, 1981). These objections do not deny the reality of the 

patterns. They attempt to persuade other scientists that, 

although the patterns are real, given millions of phylogenies 

showing independent dispersal on a finite planet, some will 

be correlated by chance alone. Endler (1977) went even further, 

suggesting that the general patterns represent only common 

adaptive pathways by independent lineages. The conservative 

nature of ecological diversification in phylogeny contradicts 

this possibility. 

Biogeographic studies using phylogenetic systematics have 

changed during the past twenty years. Hennig (1966) and 

Brundin (1966) plotted cladograms on distribution maps and 

produced explanations invoking dispersal routes (in “Speciation,” below, we will see that for certain modes of speciation, 

that is exactly what they represent). Following these publications, studies have concentrated on looking for associations 

between distributions and major tectonic changes. In many 

cases, the biogeographic analysis implied ages of origin and 

years of persistence in excess of fossil findings or of theoretical 

expectations. Paleontologists and traditionally minded ecologists and population biologists objected. This led to comparing 

the phylogenies of different groups of organisms having similar 

distributions (Croizat, Nelson, and Rosen, 1974; Rosen, 1975). 

This involved constructing ureu cladogrm-cladograms of 

ma (Figure 37) with their distributions in place of taxon names 

(Figure 38). 

The null hypothesis in biogeography is that biogeographic 

patterns among clades or species should be due entirely to 

chance, that there is no pattern, and there should be no 

necessary underlying reason for distributional correlations, and 

the area of disjunction of the ancestral species cannot be 

determined by inspecting the ranges of its descendants. 

Therefore it is important to show first, which clades have 

unique distribution patterns and which have patterns exhibited 

by other clades. Initially studies concentrated on developing 

ways to highlight the redundant distributions. Cladograms for 

different groups of organisms were compared, and those 

species in each tree showing nonredundant distributions were 
18 SMITHSONIANCONTRIBUTIONS TO BOTANY 

sp.0 sp b sp.c sp. d sp. e area A area B area C area D area E 

37 / 38 / 

ROUW 37-38.-The area cladogram. 37, For species a-e. 38, For letters A-E, indicating distribution and 

replacing the names of terminal taxa. 

deleted, producing “reduced cladograms” showing those parts 

of the phylogenies of different groups that appeared to be the 

same (Rosen, 1975). This attempt to pinpoint the redundancies 

more closely unfortunately also fueled the suspicions of 

selective data culling raised by some ecologists. More recently, 

consensus tree methods have been employed in which the 

nonredundant portions of phylogenies are reduced to unresolved 

polytomies on consensus trees of the various areas involved 

in the study (Nelson and Platnick, 1981; Humphries and 

Parenti, 1986). 

Another method of analysis involves treating cladograms 

as if they were multicharacter transformation series of the areas 

in which their members occur (Brooks, 1981). The assumption 

is that geographic distributions play a role in phylogenesis, and 

so any cladogram can be mapped onto a pattern of areas 

through time. Those portions of different clades that act as 

synapomorphies on a tree of areas have common evolutionary 

histories with respect to that pattern of areas. Those that show 

autapomorphic or homoplasious distributions on the tree of 

areas have unique histories, with autapomorphies indicating 

vicariant or peripheral isolates, allopatric speciation, or 

sympatric speciation, and homplasies indicating secondary 

dispersal subsequent to speciation, or sympatric speciation. 

All the above methods have some utility. Strict (Nelson) 

consensus trees are useful when looking for replicated areas 

of cladograms, and Adams consensus trees can be applied to 

questions of maximum resolution. Mapping gives a summary 

of all of the data. We will look at two different sets of data (fish 

and birds) to illustrate their utility. 

Possibly the most analyzed biogeographic data are Rosen’s 

on two genera of Central American fishes, Heteran&ia and 

Xiphophorus (Rosen, 1978, 1979). Figures 39 and 40 are the 

area cladograms for the clades of these genera found in Central 

America. The Adams consensus tree for the two area 

cladograms can be illustrated by either Figure 41 or by Figure 

42, in which we have used the methods developed to recognize 

hybrids (see “Hybridization,” above) and have removed area 

11 and placed it above the area cladogram. From studying 

Figure 42 and comparing it to Figures 39 and 40 it is obvious 

that the areas that are changing position are areas 6,3, and 9. 

These areas may have been affected by dispersal. 

The bird data of Cracraft (1982) can also be analyzed by 

this method. Figures 43 (Wedgebills and Birds-of-Paradise 

have identical area cladograms) and 44 (Wrens) combine to 

form Figure 45 and this ACT combines with a third genus 

(Finches, Figure 46) to form the ACT in Figure 47. If one is 

willing to assume a hybrid origin for area 3 (dispersal act), 

Figure 48 is the best estimate of the relationships using Adams 

consensus. 

The method developed by Rosen (1975) and Nelson and 

Plamick (1981) is similar to strict consensus or Nelson 

component analysis (see “Consensus Analysis,” above). It asks 

the question, “Given all of the area cladograms under 

consideration, what patterns of relationship are found in all of 

them?” It seeks to find redundant patterns because these are 

the patterns that provide the strongest evidence for vicariance. 

Areas that are not found on all of the area cladograms or that 

are in conflict are removed to produce a reduced area 

cladogram (for a justification of this procedure see Nelson and 

Plamick, 1981). Because the method for reducing Rosen’s two 

area cladograms to the redundant areas has been published 

several times (Rosen, 1978,1979; Nelson and Platnick, 1981; 

Humphries and Parenti, 1986) we will not repeat it in its 

entirety here. Instead we will give the fiial reduction with 

Figure 49 (reduced area cladogram for Heterandria) and Figure 

50 (reduced area cladogram for Xiphophorus) simplified to 

produce the summary reduced area cladogram shown in Figure 

51, which gives the area relationships that are agreed on in 

both area cladograms. Figure 51 gives us the area relationships 

that may be a result of geographic separation by vicariance 

followed by speciation. Cracraft’s bird data do not lend 

themselves to this type of analysis because some of the area 

cladograms are mutually exclusive. 

The third way of looking at nonidentical area cladograms is 
NUMBER 73 

6 I 9 4.5 II 10 7 8 I1 2,3 

19 

I I I I 3 4.5.6 II 9,lO 8 II 2 

39 / 

I6 3 94,511 10 7 8 2 

42 / 

41 / 

is c tac Rosa. 39, Area cladogram for He!er&ia. 40, Area 

cladogram for Xiphphorw. 41, Adams consensus tree. 42, Tree with area 11 treated as a hybrid area (dispenal 

act). Terminal taxa are geographic ams that reflect distribution of species. 

via mapping. Each tree can be coded as a multistate character 

(see “Character Coding,” above) and the resulting diagram is 

a summary of all of the data. It differs from the two methods 

described above in that it gives weight to the number of times 

a pattern is repeated. For instance if five area cladograms imply 

that a and b are more closely related to each other than either 

was to c and one area cladogram implies that b and c were 

more closely related to each other than either was to a, mapping 

analysis will link a and b together, suggesting that the single 

instance of close relation between b and c was due to dispersal. 

In both forms of consensus analysis, the result would be a 

trichotomy for a, b, and c. 

The procedure for coding the fiih data is explained by 

examining Figures 52 and 53 in conjunction with Table 7 for 
20 SMITHSOMAN CONTRIBUTIONS TO BOTANY 

6 3a I 2 4 5 3 

4.5 3 

Y 

4 5 3 I2 6 30 

4 5 1,2 3 4 5 3 I2 6 3a 4 5 3 I2 6 30 

46 47 I 48 I 

FIGURES 43-48.-Area dadograms --r several groups c birds from Australia. 43, Area cladogram of 

Wedgebills; Birds-of-Paradise have an identical area dadogram. 44, Area cladogram of Wrens. 45, Adams 

consensus tree for Figures 43 and 44.46, Area cladogram of Finches. 47, Adams consensus tree for Figures 45 

and 46. 48, Consensus tree treating area 3 as a hybird area (dispersal event). Terminal taxa are geographic am 

that reflect distribution of species. (Data from Cracraft, 1982.) 

49 / 50 / 

FIOURES 49-51.-Area dadograms for Heterandria and Xiphophoncr. 49, Hererandria. 50, Xiphophorus. 51, 

Summary diagram. Terminal taxa are geographic areas that reflect distribution of species; circled numben 

indicate areas that, once removed, yield a reduced area dadogram. (Figures 49 and 50 redrawn from Rosen, 1978.) 
NUMBER 73 21 

FTOuREs 52-53.Ueterandria and Xiphophorus cladograms with areas of occurrence listed above taxa and 

nodes labeled for ABC. Circled numbers refer to geographic areas representing species distribution. (See Table 

7.) 

TABLE 7.-ABC matrix for the Xiphophorus and Heterandria data of Rosen (1979). “9” indicates the taxon is 

absent from the area. (See Figures 52 and 53.) 

Areas I 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 

ANC 

ONE 

TWO 

THREE 

FOUR 

FIVE 

SIX 

SEVEN 

EIGHT 

NINE 

TEN 

00000000000100000000000000000001 

01000000000001111110000000001111 

00001111111100000000000111110101 

00000001111111100001000000010101 

00010000000111100000100000110101 

00010000000111100000100000110101 

10000000000000100000100000110101 

00000100011111199999999999999999 

00000010111111100000001011110101 

00100000000011100000010001110101 

00001000001111100000010001110~01 

- 

the ABC and Figures 54 and 55 in conjunction with Table 8 

for the NLC. The data were run using PAUP and the results 

using the two data matrices were the same. There are 10 equally 

parsimonious area cladograms (Figures 56-65), four of which 

(Figures 51,53,55, and 57) simply change the position of area 

3. Close examination of the remaining six area cladograms 

shows where the taxa that were eliminated from the strict 

consensus may belong. Area 6 is either at the second node from 

the bottom or it is sister to the clade of 5 plus 4. Area 3 is 

either sister to 2 or sister to the clade of 2 plus 8. The most 

variable groupings are for 9 and 10, principally 9. Area 9 is 

found both below and above the clade of 4 plus 5. It is sister 

to 10 or sister to the clade of 4 plus 5. Areas 9 and 10 together 

can be above or below the clade of 4 plus 5 or sister to it. 

Species associated with the areas that are unstable on the 

various area cladograms are prime candidates for hypotheses 

of dispersal. If we look at the distribution of characters 

(species) on the area cladograms we find that most are 

consistent but that several can be interpreted as either parallel 

evolution or loss. As suggested in “Comparative Methods,” 

above, we can intrepret the parallel evolution as a result of 

dispersal and the loss as a result of extinction of the species 

in that area. With some, both hypotheses are equally likely. 

For example, Heterundriu bimuculutu, “character 8,” can be 

either independently gained in both area 2 and area 3 or it could 

have become extinct in area 8 (Figures 64 and 65). From such 

data, hypotheses of historical episodes of vicariance and 

dispersal can be generated. 

The bird data were also coded using both ABC (Figures 

66-69 and Table 9) and NLC (Figures 70-73 and Table 10). 
22 

Areas 

ANCE 

ONE 

SMITHSONIANCONTRIBUTIONS TO BOTANY 

codes nodes because each node is counted as a character. 

Phylogeneticists have used three methods in biogeographic 

analysis and each method is designed to ask a different 

o 1 o o o o o 2 1 2 1 2 o o o o 2 question. Strict (Nelson) consensus analysis asks which 

lo l1 l2 l3 l4 l5 l6 l7 

54 

TWO 

THREE 

FOUR 

FIVE 

SIX 

SEVEN 

EIGHT 

NINE 

TEN 

00000008000000007 

00000008000010003 

00010004000001004 

00010004000001004 

10000001000001004 

00000106999999999 

00000017000000016 

00100003000000105 

00001005000000105 

Figure 74 (constructed using NLC data matrix, Table 10) is the 

most parsimonious arrangement of the data for both ABC and 

NLC. It appears from the distribution of the data that areas 6 

and 3a grouped together because they are missing 17(1) and 

17(2) and that there is a link between area 3 and the clade of 

areas 1 and 2 because of the parallel occurance of 17(3). One 

explanation for this area cladogram (Figure 74) is that there 

was a historical colonization (dispersal) event into area 3 by 

an ancestral species denoted by 17(3) and that some species 

have become extinct in areas 6 and 3a (perhaps due to a 

common event). 

There is one facet of “mapping” that must be kept in mind 

when a taxon is found in more than one area, the procedure is 

to score it as primitively present for both areas. This method 

called “inclusive ORing” (implicit in Brooks, 1981, and 

explicit in Cressy et al., 1983hwhere presence in an area 

always has precedence over absence-will bias the outcome 

in some cases (O’Grady and Deets, 1987). For instance, if one 

portions of different cladograms exhibit identical distribution 

patterns. Adams consensus analysis asks which portions of 

phylogenies for different groups are consistent with a single 

geographic distribution pattern. Finally, mapping methods give 

a summary of all of the data with possible placements for the 

taxa that do not conform to a general pattern. 

Biogeography has microevolutionary as well as macroevolutionary components. On microevolutionary scales, the phenomena of interest involve the local and regional movements 

of individual species. Even multispecies associations are 

considered to result from independent movements of the 

component species (MacArthur and Wilson, 1967). Macroevolutionary phenomena (historical biogeography) involve regional and global patterns of occurrence of different species. 

Associations of multiple species showing a single pattern are 

assumed to share common histories with respect to their 

geographic distributions. Wiley (1988) has recently stressed 

that historical biogeography encompasses two major research 

questions. First, do different clades exhibit speciation patterns 

that covary with respect to the same geographical distributions? 

And second, do the phylogenies of clades correspond to the 

geological history of the areas in which endemic species occur? 

If the answer to the second question is “yes,” the answer to the 

first is also “yes.” This does not necessarily mean that the 

converse is true. The relationship between geography and 

phylogeny is one of speciation events. 
NUMBER 73 23 

3 3 

2 2 

3 3 

60 61 

2 

3\ 

2 2 

2 

3\ 

FIGURES 5645.-Ten equally parsimonious area cladograms produced by “mapping” of distribution data of 

Heterandria and Xiphophorus phylogenies together as characters of their areas of occurrence. = indicates a 

possible dispersal event; x indicates a possible extinction event. Terminal taxa are geographic am. Figures 57, 

59.61, and 63 differ from Figures 56,58.60. and 62. respectively, only in the placanent of area 3. 
24 SMITHSONIANCONTRIBUTIONS TO BOTANY 

TABLE 9.-ABC matrix of Cracraft’s bird data (1986). “9” indicates the taxon is absent from the area. (See 

Figures 66-69.) 

Areas 

Codes 

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Z7 28 29 30 

ANCE 

ONE 

TWO 

THREE 

THREA 

FOUR 

FIVE 

SIX 

000000100000010000100000000001 

000101100010119999900000010111 

000011100001119999900000010111 

999999999999990001101100001111 

011000101100019999999999999999 

999999999999991010100010100011 

999999999999990110100001100011 

101000110100019999999999999999 

Frourn 66-69.-Australian bird cladograms with areas of occurrence listed above taxa snd nodes labeled for 

ABC. 66. Wedgebills. 67, Birds-of-Paradise, 68, Wrens. 69, Finches. Terminal taxa are species. and numbers 

inside circles represent geographic are89 that correspond to the species distribution. (See Table 9.) 

I 2 34 5 6 78 9 10 I1 12 13 14 15 16 17 

FIOURES 70-73.-Australian bird dadograms with are89 of occurrence listed above tax8 and nodes labeled for 

NLC. 70. Wedgebills. 71. Birds-of-Paradise. 72, Wrens. 73, Finchs. Terminal taxa are species, and numbers 

inside circles correspond to the geographic areas of those species distribution. (See Table 10.) 
NUMBER 73 

Areas 

25 

codes 

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 

TABLE 10.-NLC matrix of Cracraft’s bird data (1986). “9” indicates that the 

taxon is absent from the area. (See Figures 70-74.) 

ANCE 

ONE 

TWO 

THREE 

THREA 

FOUR 

FIVE 

SIX 

I 

00010001100000001 

00120012999000013 

00030003999000013 

99999999101110004 

11011101999999999 

99999999300201102 

99999999210200202 

20012001999999999 

SPECIATION 

Speciation is a term that denotes the formation or emergence 

of new evolutionary lineages from ancestral species. Wiley 

(1981) suggested that speciation can be studied as patterns 

and/or as mechanisms (e.g., genetic). These correspond to 

“extrinsic factors” (conditions under which speciation is 

initiated) and “intrinsic factors” (genetic, reproductive, behavioral, and ecological attributes that characterize and maintain 

the descendant species as distinct lineages), respectively. We 

will discuss the use of cladograms to study extrinsic factors in 

speciation and how these studies can help establish more 

meaningful research programs for studying the intrinsic factors. 

There are (at least) two common uses of the concept species, 

evolutionary and taxonomic. An evolutionary species is a 

single lineage that maintains its identity from other such 

lineages and which has its own evolutionary tendencies and 

historical fate (adapted from Wiley, 1981; Wiley and Mayden, 

1988). A tamnom’c species is usually a group of pheneticly 

distinct individuals but, actually, it can be anything a 

taxonomist says it is. In some cases a taxonomic species may 

correspond to an evolutionary species but in other cases the 

taxonomic species may over- or underestimate the number of 

evolutionary species. For instance, some taxonomic species 

contain cryptic species or semispecies and so underestimate 

the number of evolutionary species. For our purposes the term 

species is used to mean evolutionary species. 

In all populations there are two processes occurring 

simultaneously. One is identified with variation and local 

differentiation in response to selection, which tend to disrupt 

species identity. The other consists of historical constraints and 

gene flow among demes, which tend to keep the species 

together. Members of one species with strong historical 

constraints may not change even if separated from the 

remainder of the individuals of that species, while members 

of another species with weak historical constraints may change 

even when they are sympatric with other members of the 

species, and in the absence of environmental change. 

Biogeography is intertwined with the use of phylogenetic 

systematics in the study of speciation-the study of one is 

4 5 3 I 2 6 3a 

\ 

\ / 

From 74.-Area cladogram for Australian bird data produced by mapping 

using NLC. = indicates possible dispersal event; x indicates a possible 

extinction event. Terminal taxa are geogra@c areas. (See Table 10.) 

necessary to the other. Even with sympatric and parapatric 

speciation it is necessary to document the fact that they are 

sister species. Of primary importance is the recognition that 

where species occur today may or may not correspond to where 

they occurred at the time of speciation. Only by reconstructing 

the phylogeny can we begin to study modes of speciation. 

There are different modes of speciation, each of which involves 

a combination of extrinsic and intrinsic factors. In some cases, 

speciation can be explained by reference to differences in 

intrinsic factors among sister species alone (e.g., sympatric 

speciation). In other cases the extrinsic factors play a major 

role. Extrinsic factors pertinent to speciation are manifested 

by different biogeographic patterns. A combination of phylogenetic and biogeographic analysis can help distinguish 

different modes of speciation in different groups. A consideration of sympatric, allopatric, and parapatric speciation and their 

biogeographic patterns follows, based on the discussion by 

Wiley (1981). 

SYMPATRIC SPEcIAnoN.-Sympatric speciation occurs when 

species arise with no geographic segregation of populations. 

It can happen by hybridization, ecological partitioning, or 

some mode of producing asexual or sexually isolated 

populations, such as apomixis. Species that are sympatric today 

may not have been so when speciation occurred, and unless 

two sympatric species are sister taxa there is no evidence that 

sympatric speciation has ocurred. A phylogeny is necessary to 

determine whether or not any sympatric species are sister ma. 

If so, sympatric speciation is a possibility. 

ALLOPATRIC SPECIATION, MODEL 1.-Model I is called 

vicariant speciation or geographic speciation and results from 
26 SMlTHSONIANCONTRIBUTIONS TO BOTANY 

Jaua Yaw Chimanta Roraimo 

I+ 

Duido * -- 

R. Ventuari 

Upper R. Orinoco R. Cauca 

R. Casiquiare 

75 I 

FIGURE 75.4ladogram of the teplis of Venezuela that have records of members of the flowering plant family 

Compositae, tribe Mutisieae. Labeled nodes refer to rivers that separate groups of tepuis. The groups of tepuis 

are named using the best known of the group. such as the Duida group, which refers to Duida, Marahuaca, and 

Huadramaceri. 

the physical separation of two relatively large populations of 

a single ancestral species and the attainment of lineage 

independence by each of these large populations. This will be 

reflected in biogeography in three ways: (1) the range of the 

ancestral species may be estimated by adding the ranges of the 

daughter species, (2) the geographic point of disjunction 

corresponds to the boundary between disjunct or contiguous 

daughter species, and (3) many clades inhabiting the same 

geographic area should show the same phylogenetic and 

biogeographic patterns. 

An example of Model I is a group of plants found in the 

tepuis of the Guayana Highlands of the Venezuelan department 

of Bolivar and the Federal Territory Amazonas and adjoining 

areas. The tepuis are mountains that are part of the Guayana 

Shield, which was overlain by the Roraima Formation. This 

formation probably consisted of an extensive plateau that 

originally covered more than 2,000,000 square kilometers and 

that has since eroded away to leave these isolated, highly 

dissected, table mountains (= “tepui,” singular). The tepuis 

often rise abruptly from the surrounding savanna or rainforest, 

and often have vertical cliffs exceeding 1000 meters and 

sometimes reaching 2OOO meters. Ecologically, the tepuis are 

very different from the hot tropical lowlands below, with 

summit climates that range fmm harsh and barren to cool and 

constantly moist. It has been estimated that there are 

approximatley 2000 species of plants found on the summits 

with a 60?6-95% endemicity level (Maguire, 1970; Steyermark, 1986) for the larger tepuis. 

The Mutisieae (one tribe in the flowering plant family 

Compositae) has a high level of endemism on the tepuis. There 

are 13 genera containing 63 species (according to Steyermark, 

pers. comm., 1987), most of which are found only on or near 

the tepui summits. Figure 75 is a branching diagram 

constructed for all of the tepuis that have records of members 

of the Compositae growing on their summits. The positioning 

of the tepuis on this cladogram was based on the distance 

among the tepuis and the number and size of river systems 

separating them. Based on the assumption that all of the tepuis 

had a common origin and that the amount of time they have 

been isolated is reflected in the distance that separates them, 

we can use this branching diagram as an area cladogram. For 

the sake of this discussion we will refer to this area cladogram 
NUMBER 73 27 

FIGURE 76.-Cladogram of the flowering plant genus Slewpadus (Asteraceae: Mutisieae) superimposed on the 

tepui cladogram (Figure 75). ’Ihe tepui cladogram is represented by solid lines and the taxon cladogram by 

dashed lines with the elevations of the terminal taxa in place of their names. ?he position of one species of 

SIenopdus is uncertain and this is indicated with a dotted line. 

as a “tepui cladogram.” Following the completion of the tepui 

cladogram, the cladogram for each monophyletic group of 

plants (usually a genus) was constructed using characters based 

on morphology and anatomy. Each genus cladogram was then 

compared with the tepui cladogram. One makes the assumption 

that if vicariance followed by allopatric speciation explains the 

occurrence of the endemic species in these summit tepui 

groups, then the cladograms of the monophyletic groups should 

not conflict, or should be consistent, with the tepui cladogram. 

The example from that ongoing study (Funk, in prep) which 

best exemplifies Model I is given here. 

The cladogram for the genus Stempadus, which has species 

on eleven of the tepuis, is compared with the tepui cladogram 

in Figure 76. Optimization of the taxon cladogram shows that 

the ancestral species were distributed at high elevation. Even 

without mapping or consensus analysis, we think it is evident 

that the majority of speciation appears to support an 

interpretation of vicariance followed by allopatric speciation. 

However, several areas on Figure 76 suggest other explanations. On Duida there are three species: the one found at 2000 

meters is sister to two species found further down the slopes 

at 900 and 700 meters. On Sipapo there are two species that 

are most closely related, one at 1500 meters and one lower in 

elevation at 500 meters, and on Neblina there are sister species 

with elevations of 1700 and lo00 meters. These patterns are 

better explained by dispersal from the summits to lower 

elevations followed by allopatric speciation (see discussion 

under “Model II”). There is one species that cannot be placed 

at this point: it is found in the lowland areas around Roriama 

and Chimanta. All six genera examined so far show similar 

results. Although the species of the monophyletic groups 

studied are not found on all of the same tepuis, the cladograms 

of the groups do not conflict with the tepui cladogram. In 

addition, occasionally there appears to have been speciation 

resulting from dispersal into lower elevations or even, in one 

case, into the Venezuelan Andes. This is not unusual. A recent 

article by Huber (1988) pints out that the tepuis were exposed 

to the same climatic changes as the Andes and that some groups 

do not have strong evidence of vicariance speciation. 

ALLOPATRIC SPECIATION, MODEL 11.-Model 11, or peripheral isolation, supposes that a new species arises on the 

boundary of a larger central population. The parental species, 

which is primitive in morphology, must occupy the ancestral 

range. The isolate, exhibiting more derived morphology, 
28 SMITHSOMANCONTRIBUTIONIONS TO BOTANY 

Cacosmia 

hiero rugo had 

Y 

77 

FIGURE 77.-Cladogram and distribution of the species of the flowering plant genus Cacosmia (Compositae: 

Liabeae). hiem = C. hieronym' H. Robinson, mgo = C. rugmu HBK, had = C. harlingii Nordenstam. 

occupies a new area peripheral to the ancestor. Other clades 

will not necessarily be expected to show similar biogeographic 

patterns because peripheral isolation is expected to occur in 

different ways in different species. However, under certain 

circumstances, such as dispersal and speciation along an island 

chain, there will be repeating patterns following Hennig's 

Progression Rule (e.g., Brundin, 1966). 

Hart (1985a, b) studied distribution patterns among species 

of Lepechinia sect. Parvflorae (Lamiaceae), a group of mid-to 

Upper Andean WdY Plats. The Glade Comprises both 

Widespread ad ldY endemic Species. In all cases the 

endemic species are more recently evolved (located further 

Austroliabum 

Chi Mic poly cand erem 

Mic-Microliabum 

Chi-Chionopappus 

78 

FIGURE 78.-Cladogram and distribution of the species of the flowering plant genera Micrdiubwn and 

Awfroliabwn (Compositae: Liabeae). 'he sister group is Chionopllpppw. ply = A. polymnioides (R.E. Fries) 

H. Robinson and BretteIl. cand = A. cundidwn Grisebach) H. Robinson and Brettell, eran = A. eremophilwn 

Cabrent 
NUMBER 73 29 

along on the cladogram) than their widespread relatives. Hart 

was able to associate this pattern of apparent peripheral 

isolation speciation with climatic fluctuations in the inhabited 

areas during the Pleistocene. Data from the Compositae tribe 

Liabeae show similar results. Eight genera endemic to the 

Andes have been analyzed (Funk, in prep) and two of the 

simpler cladograms (Figures 77 and 78) show what we consider 

to be the classic pattern of speciation by peripheral isolation. 

The pattern is usually identified by a clade with most species 

in an unresolved polytomy with one member a wide ranging 

species without autapomorphies. The remainder of the species 

are isolated endemics with autapomorphies. In Cacosmia the 

three species are in a trichotomy with one, C. rugosa, being 

widespread and without apomorphies and the C. hurlingii and 

C. hieronymi having restricted distributions and autapomorphies (Figure 77). Figure 78 is a cladogram for two genera, 

Austroliabum and the monotypic Microliabum, treated here as 

one group with four species (Chionopappus is the outgroup). 

Of the four species, one, A. polymnioides is widespread, lower 

in elevation and has no autapomorphies. The other three species 

are more restricted in distribution, higher in elevation, and 

have autapomorphies. Two of the species are more closely 

related to one another than they are to any of the other species. 

None of the cladograms constructed for this study have 

repeating patterns. 

Other studies illustrating peripheral isolation are Lynch 

(1982), who provides complementary data involving toads 

(genus Cerutophrys) in eastern South America and Wiley 

(1981), who suggests that a number of the uniquely distributed 

species of Heterandria and Xiphophorus (discussed in 

“Biogeography,” above) represent the products of speciation 

by peripheral isolation. 

when two populations of an ancestral species differentiate 

despite the fact that they maintain a small area of overlap 

throughout the speciation process. This will produce sister 

species that initially have parapatric distributions. Other clades 

are not expected to have the same pattern, so we do not expect 

to find repeating biogeographic patterns. 

There is also the possibility that two populations of an 

ancestral species, having been separated, may differentiate to 

a degree allopatrically and then continue to develop lineage 

independence during a subsequent period of parapatry. This 

mode of speciation (“alloparapatric speciation”) shares the 

biogeographic statements of Models I and I1 depending on the 

size of the isolated populations. 

In using phylogenetic systematics to study speciation, 

repeating patterns are found in allopatric Models I and 11, 

vicariance, and the progression rule, while in all other modes 

of speciation the phylogenetic pattern should be individualized 

for each clade. 

PARAPATRIC sPECIATION.-parapatriC Speciation WCUrS 

HISTORICAL ECOLOGY 

Historical ecology is the name of a research program in 

evolutionary ecology that uses phylogenetic trees to produce 

direct estimates of the origin and persistence of various aspects 

of ecological associations and diversity. It builds on phylogenetic studies of biogeography and speciation in an attempt 

to provide evolutionary explanations that take many different 

causal agents into account. The name was first proposed by 

Brooks (1985) because many evolutionary ecologists had 

objected to extending the term evolutionary ecology to studies 

involving phylogenetic trees. This pinpoints a problem to 

which we alluded in the introduction. One’s choice of 

analytical methods depends on whether or not one allows for 

the possibility of among-species processes in explaining 

among-species patterns. Evolutionary ecology has developed 

as a discipline concerned with explanations based entirely in 

microevolutionary processes. If a unified view of evolutionary 

processes becomes widely accepted, the dichotomy between 

macroevolution and microevolution will largely disappear, and 

historical ecology will become that part of evolutionary 

ecology dealing with among-species phenomena. 

Ricklefs (1987) referred to the “eclipse of history” in 

community ecology as having a profound negative influence 

on the field. He expressed hope that incorporation of historical 

(systematic and biogeographical) information, along with new 

methods of documenting statistical patterns, might “bring to 

ecology some of the resurgence enjoyed recently in the fields 

of systematics and biogeography” (Ricklefs, 1987:171). We 

think this is a readily achievable goal. 

Ecological associations do not evolve in the same sense that 

we think species evolve: rather, they are “assembled.” 

However, some of the “assembly rules” may be evolutionary. 

For instance, ecological associations (1) are spatially localized, 

although their boundaries are often fuzzy, (2) are comprised 

of particular species, although the species need not be endemic 

to the association, and (3) are characterized by particular 

ecological interactions among the member species. Each of 

these three aspects of ecological associations may have 

historical components; we have already examined this possibility with respect to geographic distributions. In this section, 

we will consider the question of macroevolutionary patterns 

and evolutionary processes with respect to species cooccurrence (coevolution) and to the evolutionary diversification of ecological and behavioral traits. 

COEVOLUTION.-The critical question asked in macroevolutionary studies of biogeographic patterns is “Why do these 

species share the same real estate?” This does not presuppose 

that those species actually have anything to do with each other 

ecologically. However, in any ecosystem some species do 

interact, and in a variety of ways. In some cases the interactions 

are very general (zebras will eat a variety of plants, and lions 

will eat a variety of mammals). In other cases the interactions 
30 SMFHSONIANCONTRIBUTNS M BOTANY 

are very specific and predictable, such as those of pollinators 

and plants, or of hosts and parasites. The proximal explanations 

for such regular associations is that one or more of any set of 

interacting species has very specific ecological life history 

traits that constrain the kinds of interactions possible. 

The area of evolutionary ecology that deals with species 

having specific ecological relationships is coevolution (Futuyma and Slatkin, 1983). Like other areas of biology, 

coevolution has been construed in two different ways: one a 

within-species view, and the other an among-species view. The 

microevolutionary view stresses generation-length ecological 

phenomena that characterize and maintain such relationships. 

The macroevolutionary view attempts to estimate the conditions under which such relationships were established, and how 

long they have persisted. Phylogenetic analysis can aid studies 

of this macroevolutionary perspective that provides the 

historical context for ongoing coevolutionary dynamics. 

There are two major inquiries to be addressed in a study of 

coevolution: (1) why do the species co-occur and (2) why do 

they interact the way they do? The microevolutionary 

explanations for co-occurrence of individuals of different 

species is parallel to the microevolutionary explanations for 

biogeographic co-occurrence. Dispersal of offspring forms the 

basis for the establishment of new associations characteristic 

of each generation. This form of dispersal is sometimes called 

host-switching. The diagnostic units of such associations are 

symbiotic species, just as the diagnostic units of geographic 

assemblages are sympatric species. The microevolutionary 

explanation for the traits that characterize particular associations is called reciprocal adaptive response (see Futuyma and 

Slatkin, 1983). It can often, but certainly not always, be shown 

that each species in an association constrains and is constrained 

by the other(s). 

The macroevolutionary perspective begins by asking how 

long ecological associates have been associated. There can be 

either a historical or a nonhistorical answer in each case. The 

historical answer is that the ancestors of each species were 

themselves associated, the nonhistorical answer is that the 

symbionts differentiated evolutionarily in association with 

other species, and subsequently became associated by hostswitching or colonization. The nonhistorical answer is thus a 

direct expansion of microevolutionary processes to explain 

macroevolutionary patterns. The historical explanation is 

analogous to historical explanations of biogeographic cooccurrence. And, just as the historical analysis of biogeographic panerns does not presuppose any particular ecological 

interactions, the analysis of coevolutionary patterns does not 

presuppose any particular reciprocal adaptive response. The 

development of phylogenetic protocols for examining coevolution has shown some degree of coevolution with the protocols 

for examining biogeography. In the late 1960s and 1970s some 

ecologists suggested that, in accordance with the MacArthurWilson model of island biogeography, “hosts” should be 

considered as “islands” and parasites or other symbionts as 

“colonizers.” Beginning in the late 1970s phylogenies of 

symbionts and their hosts were compared qualitatively with a 

view more towards long-term association than short-term 

colonization, just as comparisons of phylogenies for sympatric 

taxa were examined more with respect to patterns of continental 

drift than to dispersal on fixed geographical configurations 

(see references in Brooks, 1988). 

First, we consider a hypothetical example: given a group of 

host species-Family X (five species), and their parasites, 

genus Z (four species>-one constructs a cladogram for each 

group (Figures 79 and 80). Then the host cladogram is used 

as a base and the parasite found in each species is written in 

above the host species (Figure 81). Now a transformation series 

can be constructed for the parasites based on the host 

cladogram. The ancestor to host species D and E is postulated 

to have been inhabited by the ancestor of parasite species d; 

the ancestor of host species CDE is postulated to have been 

inhabited by the ancestor of parasite species cd; the ancestor 

of host species BCDE is postulated to have been inhabited by 

the ancestor of parasite species bcd, and the ancestor of host 

species ABCD must have been infected by the ancestor of 

parasite species abcd. The transformation series for this is 

abcd-bcd-cd (Figure 82). 

Next one examines the parasite cladogram (Figure 83; 

constructed using parasite characters) and forms another 

transformation series. According to the parasite cladogram, c 

and d shared an ancestor exclusive of the other parasite taxa; 

bcd shared an ancestor exclusive of the other parasite ma, and 

abcd shared an ancestor exclusive of the other parasite ma 

This yields a transformation series of abcd-bcd<d (Figure 

84). The transformation series constructed from the host 

cladogram and the one constructed from the parasite cladogram 

are congruent and this gives complete support to the hypothesis 

of mutual descent. 

The historical interaction of ecological associates has been 

likened to that of species and the areas that they inhabit, i.e., 

historical biogeography. In the case of parasites and their hosts 

one can view the host as a geographic area and the parasites 

as the biota in that area. The organisms in that area can either 

evolve with the area in response to some isolating event 

(vicariance) or they can disperse into new areas (dispersal) just 

as ecological associates can be assembled as the result either 

of mutual descent or of transfer from one ecological associate 

to another. Because of this similarity we can use all of the 

methods applied under “Biogeography,” above, to handle 

problems such as missing data, widespread ma, and congruence determination for Studies in CoeVOhtiOn. 

Comparing the phylogenies of ecological associates is the 

most commonly used method of assessing the extent to which 

mutual descent accounts for the history of groups of organisms. 

For example, phylogenies have been constructed for a group 

of figs (Ficus) and the wasps (Aguunidae) that inhabit their 

fruits (Ramirez, 1974% b). When the two phylogenies are 

superimposed (Figure 85). the matching patterns indicate 

mutual descent. Note that the two cladograms are not identical, 

but are congruent (except for Area A, Figure 85). For instance, 
NUMBER 73 

A C D E a b C d 

31 

a b C d 

79 / 

FIGURES 79-8O.-Host/parasite cladograms. 79, Phylogeny of host 80, 

Phylogeny of parasite. 

cd 

there are several instances in which the same species of wasps 

is found in sister taxa of figs and one place (Area A, Figure 

85) in which the same species of wasp is found in two figs 

that are not sister ma. Area A (Figure 85) may be the result 

of host transfer. 

A second example of comparing phylogenies (Brooks and 

Glen, 1982; h4itter and Brooks, 1983) involves primates and a 

group of pinworms that parasitize them (Enterobius; Figure 

(a, b.c.d 1 

81 / 

cd 

t 

bcd 

t 82 abcd 

FIGURES 81432.-Parasite distribution and transformation series. 81. Parasite 

distribution mapped onto host cladogram. 82, Transformation series for parasite 

based on host cladcgram. Upper case letters represent host species and lower 

case letters represent parasite species. 

t 

bcd 

t 84 abcd 

FIGURES 83-84.-Parasite phylogeny and corresponding tramsfonnation series. 

83, Parasite phylogeny. 84, Transformation series for parasite based on parasite 

phylogeny. Lower case letters represent parasite species. 

86). There is not complete congruence between the host and 

parasite cladograms, but there is, however, an overall similarity 

in the basic branching sequence. The indication is that mutual 

descent has played a role in establishing the general pattern 

but that host transfer (ecological associate transfer) has also 

taken place. This second example, in which both types of 

historical interaction appear to have had an effect, is more 

common, with complete congruence between the phylogenies 

of both ecological associates being rare. It seems logical that 

both mutual descent and host transfer have played important 

roles in establishing present day ecological interactions. 

In another example, Hafner and Nadler (1988) compared 

branching patterns based on allozyme data of a group of 

rodents and their ectoparasites. The authors found a “high 

degree of concordance” in the diagrams, which they suggest 

is the result of cospeciation. 

In an attempt to provide better estimates of which 

associations have historical bases and which do not, Brooks 

(1981) proposed that “hosts” could be used as ma and 

“parasite” or “symbiont” phylogenies could be used as 

complex multistate characters of the hosts. If a host-group 

phylogeny is available, the symbiont phylogenies could be 

mapped onto the host phylogeny and an estimate made of 

which associations have historical bases and which do not. For 

example, Figure 87 depicts the relative phylogenetic relationships of four groups of vertebrates, and Figure 88 is a 

cladogram of four genera of closely related digenetic 

trematodes. Following the method of Brooks (1981), the 

parasite cladogram can be considered a character-state tree, or 
32 SMFHSONIANCONTRIBUTIONS TO BOTANY 

c 

FIGURE 85.4dognuns for figs (dotted lines) and fig wasp (solid lines) superimposed. hter A marks the 

Occurrence of the same species of wasp in two figs that are not sister ma. (Redrawn from Ramirez, 1974.) 

Enterobius species Primate hosts 

lemuris. ............... .Lemur 

inalisi ......... Colobus sp. 'a' 

zw Presbvtis entellus 

IonaisDiculum .P. obscura 

..... 

.... 

presbvtis.. ........ --\ .f'. ghayrei 

p. CreDuscuIus 

-- P. cristata 

pesteri ........ Colobus sp. 'a' 

colobus ............ _C. us 

brevicauda. ............ .mo 

bipaDiliatUS.. .. .CercoDithecus 

vermicularis.. ......... .Homo 

anthropopitheci ......... .Pan 

I a roux i. .............. ' bucklevi .Ponpo / 86 .............. 

FIGURE 86.-Primate and pinworm phylogenies. (Redrawn and modified from Miner and Brooks, 1983.) 
NUMBER 73 33 

FIGURES 87-89.-Host parasite cladograms. 87, Phylogeny for four groups of vertebrates. 88, Phylogeny for 

four groups of digenetic trematodes. 89, Host relationships based on ABC mapping of Figures 87 and 88. (See 

Table 11.) 

TABLE 11.-ABC matrix for the parasite phylogeny. (See Figures 87-89.) 

Taxa AB CD E F G 

10 0 0 1 1 1 

01 0 0 1 1 1 

00 I 0 0 1 1 

00 0 1 0 0 1 

00 0 0 1 1 1 

00 0 0 0 1 1 

00 0 0 0 0 1 

I 2 3 4 5 6 

transformation series, of the host group, and can be converted 

into a matrix of binary codes (Table ll), out of which a 

cladogram of host relationships can be constructed (Figure 

89). Points of agreement between host phylogeny and 

parasite-based host relationships support association by descent; points of disagreement represent episodes of colonization. Note the parallels between the documentation of historical 

and nonhistorical associations between species and the 

documentation of historical and nonhistorical geographic 

distributions. In the absence of a host phylogeny, the 

12 13 14 15 

FIGURES 90-92.-ABC for primate parasites. 90, Portion of the cladogram for Enterobius. 91, Portion of the 

cladogram for Oesophugostomwn (Conobebcria). 92, Host phylogeny that results from mapping Figures 90 and 

91 with respect to inhabited hosts. * = characters eppearing more than once on the diagram (host-switching). 
34 SMITHSOMANCONTRIBUTIONS TO BOTANY 

Taxa 

cladograms of more than one symbiont group could be used 

as characters, with hosts as taxa to provide a summary 

cladogram. In such cases, symbionts that act like homologies 

on the resultant tree indicate coevolutionary relationships and 

those that act like homoplasies indicate colonization events. 

Figures 90 and 91 depict portions of the phylogenetic trees 

for Enterobius (pinworms) and Oesophagostomum (Conobeberia) (hookworms) species inhabiting hominoid primates. 

Each cladogram is labeled according to its binary coding. 

Figure 92 shows the host cladogram that results from mapping 

the two trees together with respect to inhabited hosts. Note 

that two host transfers, one between Hylobates and Homo and 

one between Hylobates and Pongo, are postulated to have 

occurred. Thus, although neither parasite group shows strict 

mutual descent (i.e., Homo and its pinworm have different 

sister groups), the host tree based on these parasite data 

corresponds to the general pattern of primate phylogeny 

(Spuhler, 1988). For a more extensive analysis of parasite data 

pertaining to hominoid phylogeny, see Glen and Brooks 

(1985a, b). 

Coevolution encompasses more than just mutual association; 

it also embodies concepts of mutual modification, or “reciprocal adaptation” between the members of any ecological 

association. “Hosts” evolve defense traits against attack by 

predators or parasites, which themselves evolve “counterdefense” traits. One theory is that many secondary plant 

products such as terpenes and flavonoids evolved as “defense” 

traits against insect predation. However, the compounds may 

be historical in nature-they may have coevolved with the 

plants. The only way to distinguish between these two 

alternatives is to employ a phylogeny. Sesquiterpene lactone 

data are available for 20 of the 30 taxa of the genus Montanoa 

(Seaman et al., in prep.; Table 12). The data can be handled 

in two ways. Using the method described by Seaman and Funk 

(1983) one can produce a phylogenetic tree for the group based 

on the biosynthetic pathways for various sesquiterpene lactones 

(Figure 93); each branching point in the phylogeny represents 

the origin of a possible “defense” trait. Comparing this 

chemical phylogeny with the cladogram produced from 

morphological data we find that there is little obvious 

concordance. Alternatively, the chemical characters can be 

mapped onto the morphology cladogram in order to judge their 

consistancy with the phylogenetic hypothesis. Using the 

resulting cladogram of Montanoa (Figure 94) we can observe 

how well the possibility of a historical origin is supported by 

the data. Five of the chemical characters (A3, A5, A7, B1, B5) 

Characters 

A2 A3 A4 AS A1 B1 B2 B3 BS UMB 

TABLE 12.-Data matrix for sesquiterpene lactones of 20 taxa of Montunoa. 

The 0 condition is regarded as plesiomorphic. The A and B in the characters 

do not indicate homology, A refers to skeletal changes and B to substitutional 

changes. The UMB is a regulatory change. (See Figures 93 and 94.) 

OG 

RE 

FU 

MO 

GU 

XA 

TO 

RO 

QU 

ov 

HI 

HE 

AT 

PT 

KA 

AR 

LE 

GA 

IM 

BI 

SP 

0000000000 

1000000101 

0010001000 

1000000101 

1000000101 

0010001000 

0010001000 

0010001000 

0000010010 

0000010010 

1001000101 

0001000001 

1000000101 

1000000101 

1000000101 

0010001001 

1000000101 

0100000001 

0000000001 

0000100000 

0000100000 

oriented introductions of hydroxyl groups at C-6). The 

presence of the UMB pathway in Montanoa is unique in the 

Compositae family. Previously it had been reported only from 

members of the Umbelliferae family. There are two ways to 

interpret this character on the Montanoa morphology cladogram. For one, the UMB is a synapomorphy of the entire genus 

followed by five random losses. The second alternative, which 

is one step shorter, has it gained twice and lost three times 

(Figure 94). The possibility that this unusual pathway occured 

more than once is considered “not very likely” by the chemists 

involved in the study (Seaman et al., in prep.). Also, one 

wide-ranging COM species had two populations in Central 

America with UMB, which would seem to favor UMB being 

considered a synapomorphy for the entire genus. Regardless 

of which interpretation one accepts, the conclusion is that 

morphology-based phylogeny, combined with the data we 

have available, indicates that the presence of sesquiterpene 

lactones in Montanoa are consistant with a historical 

are completely consistent. Indeed, these characters resolve two 

trichotomies, provide an autapomorphy, and support the RGURE~ 93-94.--Cladogram of the members of the taxa of the genus 

sesauitetuene lactone data. 94. Cladoeram based on momholoev onto which 

monophyly Of a group’ The remaining five characters show Monunw using sesquiterpene lactone data, 93, Cla&g- based on either homoplay Or loss* Characters A2 and B3 vary together 1‘ . “I 

as did A4 and B3. These four can be explained by a simple 

gain-loss phenomonon. 

the sesquiterpene lactone data has be& mapped. Solid lines indicate taxa for 

which there are chemical data and dashed lines indicate taxa for which there 
\ 

UMBICOM ...... 0 

A2,B3 ...... A 

A4,02 ...... 

0 

\ 

WWC OM.... 0 

A482 .... m 

A283 .... A 

indicate8 reversal. 

i 

94 
36 SMlTHSONIANCONTRIBUTIONS TO BOTANY 

explanation only 37% or 38% of the time. So, in the majority 

of instances coevolution is not an acceptable explanation for 

the presence of specific sesquiterpene lactones. A study is now 

underway to investigate the possibility that, at least in parts of 

the cladogram, there may be a correlation between the 

chemistry, habitat, elevations, and other factors. 

If phylogenetic trees for the other ecological associates, such 

as insect predators on plants, are mapped onto the “host” 

phylogeny, one could discern if the evolution of the “defense” 

traits coincided with any changes in association by descent or 

by colonization (the insect predators must belong to a clade). 

Furthermore, if there are postulated “counter-defense” traits 

that have evolved, mapping phylogenies together could show 

whether “defense” traits and “counter-defense” traits have 

evolved together or independently. 

Phylogenetic systematics provides a way of differentiating 

between historically constrained characters and those independently acquired. 

ECOLOGICAL AND BEHAVIORAL DIVERSIFICATION.4althe 

(1985) (see also Eldredge, 1985; Brooks and Wiley, 1988) has 

suggested that evolution results from the interaction of two 

biological hierarchies, each having its own characteristics in 

addition to the properties that emerge from the interactions. 

On the one hand, the ecological hierarchy is an economic 

system, manifested by patterns of energy flow in ecosystems. 

It is also the hierarchy of classes, such as trophic levels or 

herbivore-crop interactions. From the perspective of the 

ecological hierarchy the particular identities of the species 

involved does not matter. Any herbivore and any plant species 

will suffice to produce a herbivore-crop interaction. On the 

other hand, the genealogical hierarchy is an information-flow 

system, manifested by genealogical relationships and the 

phylogenetic hierarchy. It is the hierarchy of indviduals. From 

this perspective, it does not matter what functional properties 

a given species possesses just so long as the members of the 

species can find sufficient resources to survive and reproduce. 

Evolution does not make complete sense without taking 

both hierarchies into account. It takes energy to make and to 

maintain organisms, but each organism uses energy only in 

particular forms as determined by properties inherited from its 

parents. 

If we adopt the two-hierarchy model as a working 

world-view, it is appropriate to ask questions about the 

genealogical context of ecological and behavioral traits or, to 

phrase it in an equivalent way, about the ecological context of 

genealogy. Are there macroevolutionary patterns indicating the 

way in which the two hierarchies have interacted in the past 

to produce the diversity we see today? There are a number of 

research programs amenable to this kind of analysis. The 

ecological life history and behavioral traits exhibited by species 

can be construed as “solutions” (or “strategies”) to the problem 

of survival in the environment at hand. Using this reasoning, 

we would expect the different species in a clade that occupy 

similar habitats to show similar convergent ecological and 

behavioral traits. A phylogenetic tree can be used as a template 

for comparisons to ask whether or not ecological and 

behavioral similarities among members of a clade are due to 

convergence or to inheritance from a common ancestor. 

If there are phylogenetic constraints on ecological and 

behavioral diversification, closely related species may have the 

same ecological or behavioral traits regardless of the environment in which they find themselves. In addition, contemporaneous species may show ecological and behavioral traits that 

evolved in environments different from the ones in which they 

find themselves today. Two or more members of a clade may 

occur in different habitats and yet share common ecological 

life history traits. Alternatively, two or more members of a 

clade may occur in similar habitats and yet exhibit divergent 

ecological and behavioral traits. In these cases we recognize 

that there can be a degree of independence between the 

products of the genealogical hierarchy and the constraints of 

the environment. This is theoretically important if one assumes 

that phylogenetic change is driven by environmental changes 

that force ecological and behavioral changes, that in turn lead 

to morphological changes (e.g., see Mayr, 1963; Futuyma, 

1979). Ecological and behavioral traits showing phylogenetic 

constraints lead us to think that ecological and behavioral 

change can be viewed as conservative elements in evolution, 

rather than as driving forces of it. And this begs the question 

of-just what is the driving force of evolution if it is not 

ecological change. 

Among-species questions in this regard can be investigated 

by considering just how closely phylogenesis in any clade is 

associated with changes in ecological or behavioral characteristics relevant to speciation. How closely does ecological and 

behavioral evolution match phylogenetic patterns? Can one 

obtain a robust cladogram by analyzing ecological and 

behavioral traits alone? Do such cladograms agree with 

phylogenies derived from morphological and biochemical 

data? How often do adaptive changes in structure and in 

function actually appear on the same branch of the phylogenetic tree? Are there ecological and behavioral traits that 

characterize species-rich clades? These questions can be 

examined by looking at individual cladograms. 

By comparing the historical context of ecological and 

behavioral traits for several clades represented in ecological 

associations, it is possible to ask questions about the evolution 

of ecosystem structure. This is an important interface between 

the two hierarchies, because the range of energy-flow pathways 

in ecosystems is determined by the attributes of the component 

species; particular environmental effects at any time determine 

what subset of that range will actually be operating. Persistent 

ancestral ecological and behavioral traits represent instances 

in which the genealogical hierarchy has constrained the 

ecological hierarchy, and adaptive changes represent instances 

of the genealogical hierarchy responding to effects of the 

ecological hierarchy. Phylogenetic constraints will limit the 

way in which a species could adapt to changes in selection 

pressures (the “selection arena” again). 

If a number of coevolving clades show ecological shifts at 
NUMBER 73 37 

the same points in history, it would be possible to find evidence 

of ecological reorganization and ask if it appeared to be 

episodic or stochastic. Such questions have been approached 

by Erwin (1985) for neontological data and by Boucot (1978, 

1982, 1983) for paleontological data. For the latter, one might 

also want to see if such Occurrences are correlated with episodic 

mass extinctions. If there are periodic mass extinctions, one 

would expect to find subsequent ecological reorganization. 

Boucot (1983) has suggested that such patterns occur in the 

fossil record, and ate a major source of “punctuated” change 

in community structure. 

Ross (1972a, b), who can be regarded as the modern father 

of historical ecology, suggested that for a variety of insect 

groups, ecological diversification is consistent with phylogenetic relationships but that it occurs infrequently. He 

suggested that approximately one in thirty speciation events 

is correlated with some form of ecological diversification. 

Recently, a number of studies have been conducted to 

investigate just how consistent ecology and phylogeny really 

are. Andersen (1982) examined the Gerromorpha, a group of 

semiaquatic hemipteran insects. He demonstrated that ecological correlates of speciation could often be used as diagnostic 

traits at what he considered to be the generic level. This also 

indicates a high degree of phylogenetic concordance and 

conservatism in the evolution of ecological diversity. Roskam 

(1985) demonstrated parallel evolution of gall-inducers from 

mycetophages in sister taxa of a group of dipteran insects 

(Figure 95). Erwin (1985) proposed that a major part of the 

evolution of diversity in carabid beetle communities results 

from the irregular evolution of novel ecological traits in 

particular species, with subsequent geographic spread and 

speciation (through peripheral isolation) distributing carabids 

with new ecological traits in new communities. Erwin termed 

these periodic episodes of ecological diversification “taxon 

pulses.” These neontological findings complement the paleontological findings of Boucot (1983) by indicating the 

conservative nature of ecological evolution. All of these studies 

show the utility of using phylogenies to study ecology. 

Wanntorp (1983) examined the evolution of leaf retention 

and of deciduousness in oaks and beeches. Otto and Nilsson 

(1981, 1982) had proposed that leaf retention evolved from 

deciduousness as an adaptation to close the nutrient cycles of 

forest ecosystems over winter. Wanntorp demonstrated that 

leaf retention is the plesiomorphic condition in this group of 

trees, and that deciduousness was actually the trait that evolved 

secondarily. This renders the adaptive senario untenable, and 

leads to questions about the evolution of deciduousness rather 

than about the evolution of leaf retention. 

Several recent studies attest to an interest in phylogenetic 

constraints on reproductive modes or “strategies.” Duellman 

(1985) found 29 reproductive modes among anuran amphibians 

(frogs and toads). He concluded that, although many reproductive modes have evolved independently in different clades, 

shared derived modes can be identified and can be shown to 

be congruent with the phylogenetic relationships of the 

95 1 

FrOUW 95.4esults of a study on gall-inducing diptera showing parallel 

evolution of gall-inducers from mycetophages. (Redrawn and modified from 

Roskam, 1985.) 

members of the groups. Hart (1985b), in a study of dioecism 

in Lepechinia sect. Parviforue, and Cox (in press), in a study 

of the Pandanaceae, also found a high degree of phylogenetic 

concordance and conservatism in the evolution of breeding 

systems in plants. Brooks, O’Grady, and Glen (1985) 

demonstrated phylogenetic congruence and conservation in the 

evolution of life cycles for digenetic trematodes. 

Pearson et al. (1988) and Mooi et al. (in press) have used a 

branching diagram to examine the occurrance of benzaldehyde 

in tiger beetles. Both studies found that benzaldehyde does not 

correlate with ecology. In addition, Mooi et al. concluded that 

the presence of benzaldehyde is plesiomorphic for tiger beetles 

and that it is the “loss” of the production of the compound that 

has evolutionary significance. The point is not that everything 

is the result of phylogenetic constraints, but that the only way 

to distinguish among those that are the product of phylogenetic 

constraints and those that are not is to employ phylogenetic 

systematics. 

Although many ecologists are beginning to recognize the 

significance of phylogenetic constraints, some comparative 

ethologists have expressed reservations about the existence or 

importance of phylogenetic constraints on behavior (Thornhill 

and Alcock, 1983; Vehrenkamp and Bradbury, 1984; Yokel, 

1986). Others, such as Clutton-Brock and Harvey (1984) have 

doubted the utility of phylogenetic systematics (sensu Hennig 
38 SMITHSONIANCONTRIBUTIONS M BOTANY 

17-24 96 

FIGURE 96.-W&-building behavior and morphology in araneoid spiders. 

* = morphological apanorphies; other characters refer to cunponents of 

web-making behavior. (Redrawn and modified fmn Coddington, 1986.) 

1966) for documenting such constraints. Both of these attitudes 

are currently being questioned. We have already mentioned 

Dobson’s (1985) study of the run-jump behavior in Richardson’s 

ground squirrels and in prairie dogs. In a more comprehensive 

study, Coddington (1986) showed that it was possible to 

reconstruct the phylogeny of a group of spiders using a suite 

of characters derived from web-making behavior and morphology (Figure 96). His sutdy has altered the basic premise of the 

phylogeny of araneoid spiders. McLennan et al. (1988) 

produced a phylogenetic tree for stickleback fishes (Gasterosteidae) using only behavioral characters (Figure 97) and found 

it to be consistent with phylogenies derived from morphology 

and karyology; in fact, the tree based on behavioral characters 

showed only three instances of homoplasy. They also showed 

how the tree could be used to assess relative contributions of 

inter-sexual selection, intra-sexual selection, and natural 

selection in true evolutionary diversification of certain 

behaviors (Figures 98-100). There appear to be macroevolutionary components in behavior, and when present these can 

be documented using phylogenetic systematics. 

It seems that there are methodological resources available 

to explore a wide range of questions about phylogenetic 

constraints on the evolution of ecology and behavior. It also 

seems that the possibilities remain virtually unexplored. The 

few studies that have been done have found less adaptive 

change than necessary if we are to explain phylogenesis 

primarily in those terms (see Figure 101; also Brooks, 1985; 

Brooks and Wiley, 1986, 1988; Brooks, O’Grady, and Glen, 

1985). These preliminary data indicate that we may have 

FIGURE 97.-Cladogram of gastemsteid fishes based on fish behavioral data. *** = nversds, numbers in 

parentheses indicate a character in a multichamcter transformation series. (Redrawn from Mchan, Brooks, 

and McPhail, 1988.) 
NUMBER 73 

0- 

39 

I 

0 ei SDinachia Aprltas ; 

I 

98 

I 1 t 

0 0 

E. gculratus G. whratlandi Culaea/Punaitius 

0 

Punait iua 

- 

0 I 

I I I 

2 3 4 

MALE NUPTIAL COLOURATION STATES 

0 I 2 3 4 

99 MALE NUPTIAL COLOURATION STATES 

0 

Qlaea/Punaitius 

I I I I I 

0 I 2 3 4 

100 MALE NUPTIAL COLOURATION STATES 

FIOURBS 9&100.-F'lots of behavior during the phylogenesis among gastaollteid fishes. 98, Changes in 

male-male agressive behavior (intra-sexual selection). 99, Changes in courtship behavior (inter-sexual selection). 

100, Changep in parental care behavior (natural selection). Taxa to the right of the dotted lines exhibit full-body 

coloration in males during the breeding cycle. The diversification of male coloration is weakly correlated with 

natural selection, and strongly correlated with inter-sexual selection. (From Mchan. Bds. and McPhail, 

1988.) 
40 SMITHSOMANCONTRIBUTIONS TO BOTANY 

101 

overestimated the 

FIGURE 101.-Phylogenetic tree for families of digmetic trematodes. Solid circles represent nontenninal 

branches diagnosed by any of six categories of ecological change; slash marks indicate terminal branches 

diagnosed by any of six categories of ecological changes: changes in production of colonizing larvae; changes 

in first intermediate host type; changes in behavior of colonizing larvae; changes in second intermediate host 

type; changes in vertebrate host type; and changes in site of infectim in vertebrate host Over 609b of the branches 

on the tree are characterized by ecological conservatism. (Redrawn and modified from Brooks, O’Grady, and 

Glenn, 1985.) 

evidence supporting adaptively driven 

evolution. Whether or not adaptive changes have taken place, 

phylogenetic systematics offer us a method for studying it. If 

it can be shown that adaptive change is not involved, then 

evolutionary explanations must begin to include additional 

factors. 

One of those additional factors is developmental constraints. 

Brooks, O’Grady, and Glen (1985) examined the phylogenetic 

relationships of all digenetic trematodes at the familial level. 

Previous efforts to study the phylogeny of these parasitic 

worms concentrated on data from a larval stage (the cercuriu) 

that develops in mollusks and spends some time swimming 

freely before infecting a host, or from the adult stage that 

resides in a vertebrate, generally in the intestine. Some workers 

felt that the cercarial stage would be less “adaptively plastic” 

and would therefore provide better estimates of phylogeny; 

others felt that the adult stage would be less plastic. Both sides 

of the argument agreed that different phylogenetic relationships 

would be supported by each data set. Because each stage 

develops in a different environment, it was felt that each would 

be subjected to different selective pressures. Brooks, O’Grady, 

and Glen showed that when the data were analyzed phylogenetically, both cercarial and adult characters agreed on the 

same phylogeny, and that neither developmental stage showed 

more plasticity than the other. The cercarial and adult data 

resolved approximately 75% of the familial relationships, and 

more than 50% of all branches were diagnosed by both 

cercarial and adult changes (the c.i. for a cladograrn with all 

characters is 74%). This indicates strong phylogenetic components of developmental constraints (Figure 101). Presumably 

cercarial and adult stages are as well adapted as possible, in a 

microevolutionary sense, given the macroevolutionary constraints provided by their developmental programs. 

The Compositae genus Monfunoa Cervantes offers an 

additional example of how one can study adaptation (Funk, 

1982). Montanou has 30 ma, 25 of which are shrubs or vines 

and five of which are trees of approximately 30 meters in 

height The trees all have daisy-like flowers, grow in cloud 

forests in higher elevations than the rest of the ma, and three 

that have been examined chromosomally are high-level 

polyploids (Funk and Raven, 1980; Funk, 1982). One species 

grows in each of the folowing areas: Guerrero, Mexico; 

Chiapas, Mexico, and northern Guatemala, Costa Ria; 

Venezuela and Colombia; and the Santa Marta Mountains, 

Colombia. All five species have a number of similar 

morphological and anatomical characters that allow them to 
NUMBER 73 41 

* 0 

R E LI AN ST FU M G T 

** 0 

Q J AG 0 F H HE AT P K LE L GA B I S 

102 I 

FIOURE l(n.-Cladognun of Montana showing conservative nature of the evolution of habitat. * = species 

that are polyploid trees; remaining species are diploid shrubs. (Redrawn and modified from Funk, 1982.) 

survive in cloud forests. None of the trees has been found at 

lower elevations. They are members of four different clades 

in the genus (Figure 102, the two taxa from South America are 

sister ma), their sister species being shrubs living allopatrically at lower elevations. One could speculate that in these 

four clades natural selection has “selected” those characters 

that allow these species to be better adapted to cloud forest 

environments. However, an understanding of developmental 

constraints leads us to a more interesting conclusion. Among 

composites, it is not uncommon for polyploids to be larger 

than diploids; prehaps, being tr’ees rather than shrubs may be 

simply a developmental consequence of high ploidy level. 

Composites, especially woody polyploids, conduct water less 

efficiently than some other plants, so it is likely that tree forms 

of composites can survive only in habitats, like cloud forests, 

where they are continuously moist. Conversely, greenhouse 

experiments (Funk, pen. observ.) indicate that the shrub-like 

species of Montanoa cannot survive under conditions of high 

moisture. Hence, the developmental constraints on size, 

moisture requirements, and moisture tolerance indicate that 

polyploids of Montunou prduced too far from a cloud forest 

to disperse into high moisture mnes for germination will have 

difficulty surviving. Likewise, diploid seeds that disperse into 

a cloud forest will have difficulty surviving. The evolution of 

tree-like species of Montanoa four times indicates a certain 

degree of developmental plasticity in polyploid production 

(something common among composites in general), while the 

strict habitat segregation (altitudinal and moisture-level) 

between trees and shrubs in the genus indicates developmental 

constraints rather than any possible competitive interactions 

as the originator of the characteristics. 

These examples are not meant to indicate that all characters 
42 SMITHSONAN CONTRIBUTIONS TO BOTANY 

are the result of developmental constraints. Rather, they 

emphasize that the use of phylogenetic systematics can enhance 

and direct studies in ecology and behavior. 

Concluding Statement 

As stated at the outset, a major reason for pursuing 

macroevolutionary research is to try to determine if there are 

any macroevolutionary processes. Thus far, there appear to be 

two classes of them: (1) those affecting many lineages 

simultaneously and in the same way, and (2) those affecting 

particular lineages but operating on time scales longer than 

those appropriate for microevolutionary processes (i.e,, longer 

than the duration of my one smcies). SO their evolutiom 

events are those due to the effects of isolation by mobile 

geological elements. Cracraft (1982,1985b) has suggested that 

the extent to which speciation events are tied to geologically 

mediated isolation is the extent to which geological evolution 

will act as a rate-limiting factor, a macroevolutionary 

constraint, on evolution. Likewise, the extent to which 

extinctions in different groups are correlated and are due to 

terrestrial or extraterrestrial perturbations of a periodic nature 

is the extent to which those perturbations affect the rate of 

extinction. 

MaCroevolutioW Processes affecting Particular lineages 

comprise phylogenetic constraints. Phylogenetic constraints 

Can be seen both in stuctd and in functional diversification. ,. 

effects are not apparent in the record of each speciation event. 

None of these processes is a sufficient explanation for 

evolutionary diversification, nor can they be deduced from 

microevolutionary considerations. For these reasons, we 

eschew any attempts to reduce evolutionary explanations to 

either macro- or microevolutionary processes. We opt for a 

hierarchy of causal agents, each operating on a different time 

scale and each contributing something to the evolved diversity 

we study. 

Macroevolutionary processes affecting many lineages simultaneously are responsible for at least some correlated speciation 

events and for correlated extinctions. The correlated speciation 

They affect evolution in two ways. First, they limit the extent 

to which, and the manner in which, species can adapt to 

different selection regimes. Second, the constrained portions 

act as conservative “filters” on changing portions, eliminating 

variants that might be seen as functional individual units but 

which do not integrate with the whole organism well enough 

to allow viability. In both senses, they establish the arena, or 

context, of evolutionary change. Changes in the genealogical 

hierarchy are slow; changes in the ecological hierarchy are fast. 

The interplay of the two hierarchies produces a strong 

self-organizing and adaptive evolutionary imperative in biological systems. 
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