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smithsonian contributions to botany • number 102

Smithsonian Institution

Scholarly Press

Smithsonian Institution

Scholarly Press

Andean Origin and Diversification 

of the Genus Perezia, 

an Ancient Lineage of Asteraceae

María José Apodaca, 

Jorge V. Crisci, and 

Liliana Katinas
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smithsonian contributions to botany • numb e r 1 0 2

Andean Origin and Diversification 

of the Genus Perezia, 

an Ancient Lineage of Asteraceae

María José Apodaca, 

Jorge V. Crisci, and 

Liliana Katinas

WASHINGTON D.C.

2015
ABSTRACT

Apodaca, María José, Jorge V. Crisci, and Liliana Katinas. Andean Origin and Diversification of the Genus Perezia, an 

Ancient Lineage of Asteraceae. Smithsonian Contributions to Botany, number 102, viii + 28 pages, 7 figures, 4 tables, 3 

appendixes, 2015.—Perezia is an Andean-centered genus and belongs to the early diverging lineages in the phylogenetic 

tree of the Asteraceae (Compositae). Previous studies in Perezia proposed several evolutionary lines and alternative areas 

of origin. A phylogenetic morphological analysis was performed to test these hypotheses and ancestral areas and dispersalvicariance analyses were applied. The results of the phylogenetic analysis support Perezia as a monophyletic taxon, including the recently excluded Perezia nutans and P. prenanthoides, and support most of the previously proposed evolutionary 

lines. The biogeographic results suggest the southern Andes as the probable ancestral area for Perezia, with multiple 

dispersals. Supported by geologic, paleoclimatology, and fossil evidence, it is inferred that the ancestor of Perezia may have 

inhabited the areas above the humid, temperate forests in the southern Andes during the Tertiary. KEY WORDS: Climatic changes, morphology, Mutisioideae, phylogenetic reconstruction, South America.

RESUMEN

Apodaca, María José, Jorge V. Crisci y Liliana Katinas. Origen andino y diversificación del género Perezia, un linaje temprano de Asteraceae. Smithsonian Contributions to Botany, número 102, viii + 28 páginas, 7 figuras, 4 tablas, 3 apéndices, 

2015.—Perezia tiene su mayor concentración en los Andes y pertenece a los linajes tempranos del árbol filogenético de 

Asteraceae (Compositae). En estudios previos en Perezia se propusieron varias líneas evolutivas para el género y áreas de 

origen alternativas. Se desarrolla aquí un análisis filogenético sobre la base de caracteres morfológicos para poner a prueba 

dichas hipótesis y se aplican los métodos biogeográficos de areas ancestrales y de dispersión-vicariancia. Los resultados del 

análisis filogenético muestran que Perezia es un taxón monofilético si incluye a las recientemente excluidas Perezia nutans

y P. prenanthoides, y sustentan a la mayoría de las líneas evolutivas previamente propuestas. Los resultados biogeográficos 

sugieren a los Andes del sur como probable área ancestral de Perezia, con múltiples dispersiones. Sobre la base de la evidencia geológica, paleoclimatológica, y fósil, se propone que el ancestro de Perezia podría haber habitado las áreas por encima 

de los bosques templados del sur de los Andes durante el Terciario. PALABRAS CLAVE: Cambios climáticos, morfología, 

Mutisioideae, reconstrucción filogenética, América del Sur.

Cover images, from left to right: Perezia multiflora subsp. multiflora (habit; photo by L. Katinas); Andes of southwestern 

Argentina (photo by M. Apodaca); Perezia recurvata (habit; photo by M. Bonifacino). 

Published by SMITHSONIAN INSTITUTION SCHOLARLY PRESS

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Library of Congress Cataloging-in-Publication Data

Apodaca, María José, author.

 Andean origin and diversification of the genus Perezia, an ancient lineage of Asteraceae / María José Apodaca, 

Jorge V. Crisci, and Liliana Katinas.

 pages cm. — (Smithsonian contributions to botany ; number 102)

 Includes bibliographical references.

1. Perezia—Andes—Phylogeny. 2. Phylogeography—Andes. I. Crisci, Jorge Víctor, author. II. Katinas, Liliana, author. 

III. Title. IV. Series: Smithsonian contributions to botany ; no. 102. 

 QK495.C74A66 2015

 583'.99—dc23

2015015635

ISSN: 1938-2812 (online); 0081-024X (print) 

Publication date (online): 29 July 2015 

c The paper used in this publication meets the minimum requirements of the American National Standard for Permanence 

of Paper for Printed Library Materials Z39.48–1992. 
Contents

FIGURES v

TABLES vii

INTRODUCTION 1

MATERIAL AND METHODS 3

Phylogenetic Analysis 3

Biogeographic Analysis 5

RESULTS 5

Phylogenetic Analysis 5

Biogeographic Analysis 11

DISCUSSION 11

Monophyly of Perezia and Evolutionary Lines 11

Historical Biogeography of Perezia 15

Integration of Morphology, Ecology, Geology, and the Fossil Evidence 17

ACKNOWLEDGMENTS 17

APPENDIX A: CHARACTERS AND CHARACTER STATES 19

APPENDIX B: DATA MATRIX 21

APPENDIX C: AREAS OF ENDEMISM 25

REFERENCES 27

Figures

1. Map of South America showing Brazilian and Patagonian subregions 2

2. Species representing the Perezia lineages 4

3. Areas of endemism used in the biogeographical analysis of Perezia 8

4. One of three trees obtained from the phylogenetic analysis of Perezia 9

5. Previous and current schemes of relationships among species groups 

of Perezia 10

6. Dispersal-vicariance analysis of Perezia 12

7. Simplified tree of Perezia with ancestral distributions and middle–late 

Miocene marine transgression 16

Tables

1. Species groups for Perezia proposed by Vuilleumier compared 

with species groups obtained from present analysis 6

2. Results of dispersal-vicariance analysis 13

3. Area gains and losses for species of Perezia 13

Appendix Table

B1. Data matrix for phylogenetic analysis 22

INTRODUCTION

Southern South America today has a high diversity of environments, biomes, and 

biotas probably as the result of the complex interactions through time of plants and 

animals with several geological forces, including the rising of the Andean Cordillera, 

sea-level changes, and glaciations (Ortiz-Jaureguizar and Cladera, 2006). The Andean 

Cordillera, a great series of mountain belts, sweeps up the west coast of South America 

from the southern tip of Chile and Argentina to Venezuela. The Andes are the world’s 

longest mountain range and boast the highest peaks in the world after the Himalayas; 

for instance Aconcagua in the Mendoza province of Argentina is 6,962 m high (22,841 

ft). The Andean Cordillera is a crucial barrier to atmospheric circulation in the southern 

hemisphere and has the highest plateau on Earth, the Altiplano-Puna at 3,000–4,000 m, 

formed at a noncollisional plate margin (Gregory-Wodzicki, 2000). 

It has been postulated that the Andes acted as a dispersal route for organisms and 

as a driver for rapid diversification via allopatric speciation and ecological displacement 

(Antonelli et al., 2009). This diversification was promoted by the emergence of heterogeneous ecological conditions in island-like habitats after successive Andean uplifts and 

Quaternary climate fluctuations facilitated geographical isolation (Ritz et al., 2007). 

As postulated by several authors, the Andes constitute the backbone of one of the 

two biogeographical regions of South America. South America was proposed as a subcontinent of hybrid origin that should be divided into two biogeographical areas: southern temperate and northern tropical areas (Humphries, 1981). The southern temperate 

region, the focus region of this study, is the area south of 30° south latitude in South 

America but also includes the Andean highlands north of this latitude. This area was 

named the Patagonian subregion by Kuschel (1969) and southern South America by 

Crisci et al. (1991) (Figure 1). An approximation of this area may be obtained by looking 

at the distribution of many individual taxa, such as Azara Ruiz et Pav. (Flacourtiaceae), 

Escallonia L.f. (Escalloniaceae), Mummucidae and Daesiidae (Solifugae), Tristiridae (Orthoptera), Pompilocalus Roig-Alsina (Hymenoptera), and genera of Coleoptera (Kuschel, 1969; Crisci et al., 1991). Many distributions of genera and species groups of the 

plant family Asteraceae are also congruent with this distributional pattern, for example, 

Lucilia Cass., Noticastrum DC., and members of the tribe Nassauvieae (Crisci, 1974), 

such as Leucheria Lag., Nassauvia Comm. ex Juss., Perezia Lag., and Trixis P. Browne. 

Perezia Lag. (Asteraceae, Nassauvieae), with 30 species of perennial herbs (Katinas, 2012), is distributed from Colombia to southern Chile and Argentina, including Islas Malvinas (Falkland Islands) (Figure 1). Its major concentration occurs in the 

Andean Origin and Diversification 

of the Genus Perezia, an Ancient Lineage 

of Asteraceae

María José Apodaca,* Jorge V. Crisci, and Liliana Katinas

División Plantas Vasculares, Museo de La Plata, 

Paseo del Bosque s/n, 1900 La Plata, Argentina.

* Correspondence: apodaca@fcnym.unlp.edu.ar 

Manuscript received 24 November 2014; accepted 11 February 2015.
2 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

FIGURE 1. Map of South America showing the two subregions, Brazilian and Patagonian, established by Kuschel 

(1969) on the basis of Coleoptera distributions. The distribution of the species of Perezia is shown in gray.
NUMBER 102 • 3

southern Andes and in Patagonia, with a few species in the area 

of southeastern Brazil, Paraguay, Uruguay, and northeastern 

Argentina. In addition, Perezia belongs to the basal grade in 

the phylogenetic tree of the family (Funk et al., 2009), making this an interesting genus to postulate hypotheses about the 

early Andean diversification among lineages in southern South 

America. 

The first revisionary work of Perezia was performed by 

Vuilleumier (1970), who established 30 species and proposed 

seven evolutionary lines of species groups based on morphological, anatomical, palynological, cytological, and chemical data 

(Figure 2). These evolutionary lines are (1) the Perezia coerulescens group, (2) the P. magellanica group, (3) the P. multiflora

group, (4) the P. prenanthoides group, (5) the P. pungens group, 

(6) the P. recurvata group, and (7) P. pilifera Less., which was not 

included in any of the groups (Table 1). Hypotheses on the origin 

and radiation of each one of these lineages were proposed by 

Vuilleumier (1970), and it was suggested that Perezia arose during the early middle Tertiary in open, warm forests that covered 

extratropical South America.

Based on 28 of the 30 species established by Vuilleumier 

(1970), a phylogenetic analysis to test these groups was developed by Simpson et al. (2009) using molecular sequence data of 

the nuclear rDNA internal transcribed spacer (ITS) sequences 

and the chloroplast intergenic spacers rpl32-ndhF and trnL 

(UAG)-rpl32. The authors noted the discrepancy between the 

phylogenies generated with the different markers, and the results 

of the combined analysis contained several polytomies within 

Perezia. Their combined phylogeny showed that the Braziliancentered P. multiflora group was the sister group of the remainder of the Perezia species. The P. multiflora and the P. recurvata

groups were the only species groups of Vuilleumier (1970) that 

were supported as monophyletic in the molecular analyses, with 

the P. recurvata group including additional species (P. linearis 

Less., P. pilifera, and P. viscosa Poepp. ex Less.) in one of the 

trees. Simpson et al.’s (2009) analysis, in contrast with previous 

hypotheses, suggested an eastern subtropical South American 

origin for the genus with a radiation into southwestern South 

America.

A more recent taxonomic revision of Perezia (Katinas, 

2012) led to drastic specific and generic redefinitions (Table 1). 

For example, the recognition of P. atacamensis (Phil.) Reiche, 

P. burkartii Cabrera, and P. capito (Phil.) Reiche was proposed; 

the inclusion of the new species P. catharinensis Cabrera, P. dentata (Cabrera) Katinas, P. eryngioides (Cabrera) Crisci, and P. 

volcanensis Cabrera, described or transferred from other genera after the first revision of the genus in 1970, was reported; 

and many species were synonymized with P. pungens (Humb. et 

Bonpl.) Less. and with P. pinnatifida (Humb. et Bonpl.) Wedd.

Perezia nutans Less. and P. prenanthoides Less., excluded from 

the genus in previous studies (Panero, 2007, based on unpublished data; Simpson et al., 2009), were tentatively placed in 

Perezia because no morphological gaps were found to warrant their segregation. These additions resulted in 30 species of 

Perezia being recognized, only 22 of which were included in the 

phylogenetic study of Simpson et al. (2009). Owing to the recent 

taxonomic changes that have occurred in Perezia, the limited 

sampling of previous studies, and the competing hypotheses resulting from the different molecular markers, the phylogenetic 

relationships within the genus needed to be investigated using a 

new set of data. 

In this study all the species of Perezia (according to the most 

recent revision of the genus, Katinas, 2012) were included, and 

a phylogenetic study was conducted using morphological and 

palynological characters. The results of this analysis were used 

to examine previous studies, focusing on the species groups established by Vuilleumier in 1970 because the results in that work 

are less ambiguous than those of Simpson et al. (2009). On the 

basis of the resulting phylogenies, we employed here the historical biogeographical approaches dispersal-vicariance analysis 

(Ronquist, 1997) and ancestral areas (Bremer, 1992) to seek the 

historical explanations that led to the origin and diversification 

history of Perezia in the Andes.

MATERIAL AND METHODS

Phylogenetic Analysis

For this study, the 30 species of Perezia sensu Katinas 

(2012) were used as terminal taxa. The morphological and 

palynological data of the species of Perezia were taken from 

previous studies (Crisci, 1974; Katinas, 2012), derived from the 

analysis of ~1,300 herbarium specimens, or gleaned from field 

studies. 

The apomorphic character state was identified by the 

outgroup comparison method (Watrous and Wheeler, 1981). 

Phylogenetic hypotheses proposed for the tribe Nassauvieae 

(Crisci, 1974; Katinas et al., 2008a; Luebert et al., 2009; 

Simpson et al., 2009) provided the basis for choosing Nassauvia

and Panphalea Lag. as appropriate outgroups for the 

phylogenetic analysis of Perezia. Data from 37 morphological 

and palynological characters were included (Appendix A). 

Multistate characters (e.g., 2, 3, 6) were treated as unordered 

(=nonadditive). Some character states were coded as “?” because 

they are inapplicable characters (e.g., characters of the pappus 

in Panphalea, which lacks a pappus, or characters of the cypsela 

hairs in taxa with glabrous cypselae) or because there are missing 

data, as for a few characters in P. volcanensis. Variable characters 

in some taxa (e.g., 5, 7, 9) were treated as polymorphic during 

the analysis. Appendix B contains the data matrix, which was 

analyzed with the Wagner maximum parsimony algorithm of 

PAUP* version 4.0a129 (Swofford, 1999) using the “heuristic 

search” option. The bootstrap method (Felsenstein, 1985) with 

100 replicates was employed to evaluate the reliability of the 

phylogenetic estimates. The program MacClade version 3.0 

(Maddison and Maddison, 1992) was used for examination of 

the character distribution.
4 • SMITHSONIAN CONTRIBUTIONS TO BOTANY
NUMBER 102 • 5

Biogeographic Analysis

Areas of Endemism: An area of endemism is 

defined here as an area of nonrandom distributional congruence 

among different taxa. It is identified by the congruent distributional boundaries of two or more species, where congruence 

does not demand complete agreement of those limits at all possible scales of mapping but relatively extensive sympatry is a 

prerequisite (Platnick, 1991). Areas of endemism used in this 

analysis (Figure 3) are defined by Cabrera and Willink (1980) 

and Sick (1969). The areas considered in this study are (A) Subantarctic, (B) northern Andean, (C) southern Andean, (D) Patagonia, (E) Puna, (F) Paranense, (G) Chacoan, (H) Pampean, and 

(I) Espinal. Islas Malvinas are here included in the Subantarctic 

(Appendix C).

Dispersal-Vicariance Analysis (DIVA):

Ancestral distributions were reconstructed using DIVA 1.1 (Ronquist, 1996) according to the dispersal-vicariance optimization 

method (Ronquist, 1997). Dispersal-vicariance analysis optimizes distributions for each node of the tree, allowing for vicariance events and minimizing the number of assumed dispersals 

and extinctions. The analysis assumed that the number of ancestral areas was unconstrained, favoring vicariance and allowing 

the ancestral distributions to contain the maximum number of 

areas (Crisci et al., 2003), which for this study was nine (as listed 

in “Areas of Endemism”). According to Ronquist (1996), the optimizations become less reliable as the root node is approached 

because it includes most or all of the areas occupied by the terminals. To address this shortcoming, the ancestral areas approach 

(Bremer, 1992), which determines the ancestral area of Perezia

under a different assumption, was also employed (assuming only 

dispersal and not dispersal and vicariance).

Ancestral Areas (AA): A taxon areas tree was 

constructed, and the ancestral areas method of Bremer (1992) 

was followed. This method is a cladistic procedure for approximating ancestral areas of an individual group from the topological information in its area tree. The areas are optimized on 

the tree, and the number of gains or presences (G) and losses or 

absences (L) for each individual area are computed. Finally, the 

G/L ratio for each geographic area was estimated to determine 

which individual area(s) had the highest G/L ratio(s) and, therefore, was a part of the hypothetical ancestral area (Crisci et al., 

2003). For a critique to this method see Ronquist (1994, 1995).

RESULTS

Phylogenetic Analysis

The phylogenetic analysis resulted in three equally parsimonious trees with a length of 144 steps, a consistency index of 

0.375, and a retention index of 0.600. The trees are similar and 

differ only in their placement of Perezia carthamoides (D. Don) 

Hook. et Arn., P. volcanensis, and P. pungens: (1) P. volcanensis

is sister group of P. pungens and together they form the sister 

group of P. carthamoides; (2) P. pungens is the sister group of 

P. carthamoides and both are the sister group of P. volcanensis; 

and (3) the three species form a trichotomy. We chose the first 

option (Figure 4) to show the character distribution. The lack of 

branch support in our analysis is coincident with the low support (50%–60%) or lack of support in many branches in the 

molecular analyses of Perezia (Simpson et al., 2009) based on 

the two different genes individually and in the combined tree. 

This could reflect high levels of homoplasy in the genus or very 

rapid evolution.

The species of Perezia form a monophyletic group with 

65% support, including P. nutans and P. prenanthoides, which 

have been excluded from Perezia in other analyses (Panero, 

2007; Simpson et al., 2009). Perezia is supported by the following unique combination of seven synapomorphies: presence of a 

scape, a one-seriate involucre with a length of 10–20 mm, outer 

involucral bracts with a ciliate margin, corollas white and colored, pollen grains with polar elevations, fruits that are densely 

pubescent, and a capillary pappus. Likely some of these character states may appear in other genera of Nassauvieae, but this 

combination of features is exclusive to Perezia.

Several monophyletic groups are recovered within Perezia. 

Unlike most vegetative characters, which are variable among 

species, the pubescence of the reproductive parts such as the receptacle and fruit (especially the amount and type of pubescence) 

are very reliable features that are often used to separate species. 

Figure 5 shows two diagrams comparing the evolutionary hypothesis of Vuilleumier (1970) (Figure 5A) with our phylogenetic 

results (Figure 5B). Below we list each of Vuilleumier’s (1970) six 

species groups (see also Table 1) and compare them with the tree 

obtained here. 

1. Perezia coerulescens species group (called by us P. pinnatifida species group): P. atacamensis, P. burkartii, P. ciliosa, 

FIGURE 2. (Opposite page) Species representing the Perezia lineages: (A) P. pinnatifida, of the P. coerulescens (=P. pinnatifida) species group; 

(B) P. magellanica of the P. magellanica species group; (C) P. multiflora, of the P. multiflora species group; (D) P. squarrosa, of the P. multiflora

species group; (E) P. prenanthoides, of the P. prenanthoides species group; (F) P. carthamoides, of the P. pungens species group; (G) P. recurvata, 

of the P. recurvata species group; and (H) P. pilifera. Photo credits: A, D, G: M. Bonifacino; B, H: Station Alpine Joseph Fourier (France) via 

Flickriver.com; C: L. Katinas; E: F. Vidoz (www.sib.gov.ar); F: M. Costea (Phytoimages).
6 

• SMITHSONIAN CONTRIBUTIONS TO BOTANY TABLE 1. Species groups proposed by Vuilleumier (1970) for the genus Perezia compared with the species groups obtained in the current analysis; morphological circum- scription and geographical distribution are included. Dashes represent species that lack autapomorphies in the phylogenetic trees. See the text for further explanations. Species groups proposed by Vuilleumier Species groups proposed by present analysis Perezia species group Species included Morphological circumscription Perezia species group Species included Morphological circumscription Distribution 1. P. coerulescens P. ciliosa P. coerulescens P. pinnatifida P. pygmaea Reduced stature, compact rosettes tightly appressed to the ground; heads hidden among the leaves 1. P. pinnatifida P. atacamensis P. burkartii P. ciliosa P. dentata P. pinnatifida Stem unbranched (scape); basal leaves with marginal cilia Altiplano of NW Argentina and N Chile to Peru 2. P. magellanica P. bellidifolia P. calophylla P. delicata P. fonkii P. lactucoides

P. lyrataP. magellanicaP. megalanthaP. pedicularidifoliaP. viscosa

Small, rosette plants; solitary capitula; fruits with long, dense hairs

2. Polyphyletic group: constituted by independent monophyletic groups and individual species

P. bellidifolia — Argentinian S Andes

P. calophylla Pappus white and 

colored

Argentinian S Andes

P. capitoP. megalantha

Involucre hemispherical; involucral bracts orbicular; scarce fruit pubescence

S Andean valleys of Chile and Argentina

P. delicata P. lactucoides P. magellanica

Involucral bracts without scarious margin

S Andes of Argentina and Chile, bogs, and Nothofagus forests

P. fonkii Long and filiform fruit 

pubescence

S Andes of Chile and Argentina, Nothofagusforests

P. lyrata — S Andes of Chile

P. pedicularidifoliaP. poeppigii

Fruit apex rostrate S Andes of Chile and 

Argentina, Nothofagusforests, and central valley between central Chilean Andes

P. spathulata — S Andes of Argentina 

and Chile, Nothofagusforests
NUMBER 102

• 

7

3. P. multiflora P. kingii

P. multifloraP. squarrosa

Silky, copper-colored fruit hairs; hemispherical involucre; reduced number of involucral bracts

3. P. multiflora P. catharinensis

P. eryngioidesP. kingiiP. multifloraP. squarrosa

Corymbose inflorescence; fruits with nonglandular hairs exclusively

Paraguay, Uruguay, SE Brazil, NE Argentina, one species extending to N Andes

4. P. prenanthoides P. nutans

P. prenanthoides

Large, foliaceous herbs; showy, open clusters of numerous magenta heads; broad, soft, basal leaves; fruits densely covered by amber-colored hairs

4. P. prenanthoides P. nutans

P. prenanthoides

Inflorescence paniculate; receptacle glabrous; fruits scarcely pubescent

S Andes of Argentina and Chile, Nothofagusforests

5. P. pungens P. carduncelloides

P. carthamoidesP. ciliaris

P. mandonii

P. pungensP. purpurataP. sublyrata

Large, caulescent, polycephalus plants

5. P. pungens P. carthamoides

P. pungensP. volcanensis

Leaves with marginal cilia; spherical involucre; fruits scarcely pubescent

Andes and Puna from central Argentina and N Chile to Colombia

6. P. recurvata P. linearis

P. poeppigiiP. recurvata

Special type of fruit hair; large, turbinate capitula; stiff, lanceolate involucral bracts

6. P. recurvata P. linearis

P. recurvata

Linear leaves, revolute or plicate; fruits scarcely pubescent

Central Chile, Nothofagus forests, Patagonia

Isolated species P. pilifera Not included in a 

group

P. pilifera Linear leaves with 

marginal spines; inflorescence shorter than the leaves; fruits with long and filiform, nonglandular hairs

Andes from central Argentina to the S, including Patagonia
8 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

FIGURE 3. Areas of endemism used in the biogeographical 

analysis of Perezia.
NUMBER 102

• 

9

FIGURE 4. One of the three trees obtained from the maximum parsimony analysis of Perezia; characters are superimposed onto the tree (see Appendix A). Black circles represent synapomorphies and white circles represent homoplasies (parallelisms and reversals). Numbers within circles above branches are bootstrap values (only values ≥ 50 are indicated).
1 0 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

FIGURE 5. Schematic comparison of the relationships among the species and species groups of Perezia as presented by Vuilleumier (1970) and 

based on our phylogenetic tree (shown in Figure 3): (A) hypothesis of Vuilleumier (1970); (B) hypothesis proposed here.
NUMBER 102 • 1 1

P. dentata, and P. pinnatifida. Two of the four species included 

in this group by Vuilleumier (1970), that is, P. coerulescens and 

P. pygmaea, are currently considered synonyms of P. pinnatifida. Perezia burkartii, established by Vuilleumier (1970) as a 

synonym of P. coerulescens Wedd., is now considered an independent species (Katinas, 2012), and this analysis supports it as 

the sister taxon of P. pinnatifida. Perezia ciliosa, placed by Vuilleumier (1970) in an intermediate position between this group 

and the P. pungens species group (Figure 5A), is included here in 

the P. coerulescens group together with P. dentata (previously a 

subspecies of P. ciliosa). Perezia atacamensis was established by 

Vuilleumier (1970) as a synonym of P. pungens. The phylogenetic analysis, however, shows that P. atacamensis belongs to the 

P. coerulescens species group. This group is supported here by 

the unbranched stems and the basal leaves with marginal cilia.

2. Perezia magellanica species group: P. bellidifolia (Phil.) 

Reiche, P. calophylla, P. capito, P. delicata Vuilleum., P. fonkii 

(Phil.) Reiche, P. lactucoides (Vahl) Less., P. lyrata (J. Rémy) 

Wedd., P. magellanica (L. f.) Lag., P. megalantha Speg., P. pedicularidifolia Less., P. poeppigii Less., and P. spathulata (Lag. ex 

D. Don) Hook. et Arn. This is the only group that is suggested 

as non-monophyletic in our analysis. Originally the group consisted of more or less the same species, but now it also includes 

P. capito (previously a synonym of P. lyrata) and a name change 

for P. viscosa Poepp. ex Less. (=P. spathulata). These species are 

arranged as follows in our tree: P. calophylla is sister taxon of the 

P. pinnatifida species group; the sister species P. pedicularidifolia

and P. poeppigii Less. form the sister group of the P. pungens

group and the P. multiflora group; and the remaining species 

form a grade in the tree following P. pilifera (D. Don) Hook. et 

Arn. and the P. recurvata species group.

3. Perezia multiflora species group: P. catharinensis, P. eryngioides, P. kingii Baker, P. multiflora (Humb. et Bonpl.) Less., 

and P. squarrosa. This monophyletic group originally included 

only P. kingii Baker, P. multiflora, and P. squarrosa. Perezia catharinensis and P. eryngioides were described after Vuilleumier`s 

(1970) revisionary study. This group is centered in Brazil and 

includes Eryngium-like (i.e., erect perennial herbs with long, narrow, spiny leaves and paniculate or corymbose inflorescences) 

species characterized by their corymbose inflorescences and the 

fruits covered exclusively by nonglandular hairs.

4. Perezia prenanthoides species group: P. nutans and P. prenanthoides. Our analysis supports this as a monophyletic group 

nested within Perezia. Vuilleumier (1970) placed this group in an 

independent, unrelated position in her evolutionary scheme of 

the genus (Figure 5A). The group is supported here by capitula 

arranged in panicles, a glabrous receptacle, and fruits with scarce 

pubescence.

5. Perezia pungens species group: P. carthamoides, P. pungens, and P. volcanensis. Originally this group included P. carthamoides, P. pungens, and many species (P. carduncelloides, P. 

ciliaris, P. mandonii, P. purpurata, and P. sublyrata) that were 

subsequently considered synonyms of P. pungens by Katinas 

(2012). The only difference in the results presented here is the 

addition to this monophyletic group of P. volcanensis, described 

after 1970. The group is supported by the presence of leaves with 

marginal cilia, a spherical involucre, and fruits that are scarcely 

pubescent.

6. Perezia recurvata species group: P. linearis and P. recurvata (Vahl) Less. Our analysis supports this group on the basis 

of the basal leaves, which are linear, revolute, or plicate, and 

cypselae that are densely pubescent. Perezia poeppigii, which 

was placed in an intermediate position by Vuilleumier (1970) 

between this group and the P. pungens species group (Figure 5A), 

appears in our analysis to be related to the P. magellanica species 

group.

Isolated species, Perezia pilifera: This species was not included in any group by Vuilleumier (1970) (Figure 5A). Our 

results place it as the sister group of the rest of the species of 

Perezia. It is thought to be morphologically close to the P. recurvata species group because all three species have characteristic 

linear leaves.

Biogeographic Analysis

Dispersal-Vicariance Analysis: The results 

of the DIVA analysis (Figure 6) show the Southern Andes (C) as 

the probable ancestral area for the extant species of the genus 

Perezia (node 19). The tree of Perezia shows 15 dispersal events 

and 5 vicariance events; these events are depicted in Table 2. 

There are multiple dispersals from the area of origin, the Southern Andes, to the Subantarctic (A) (e.g., nodes 11, 14, 15), which 

is the adjacent area at a lower altitude. The most frequent vicariance event shown in Table 2 occurs between the Southern Andes 

(C) and the Northern Andes (B) (nodes 4 and 6).

Ancestral Areas: In coincidence with DIVA, the 

application of Bremer’s method (1992) indicates that the Southern Andes (C) could be a part of the ancestral geographic range 

of Perezia, giving its relatively high G/L value of 4.00 and AA of 

1, which shows a marked departure compared with the G/L and 

AA values of the other areas (Table 3).

DISCUSSION

Monophyly of Perezia and Evolutionary Lines

The results of our phylogenetic analysis provide evidence 

supporting Perezia as a monophyletic genus. Different from other 

analyses (Panero, 2007, based on unpublished data; Simpson 

et al., 2009) that excluded P. nutans and P. prenanthoides, our 

analysis shows both species nested within the genus. It should be 

noted that in the chloroplast DNA and nuclear ITS trees obtained 

by Simpson et al. (2009) both species are well separated from 

Perezia and are the sister group of other genera (Calopappus

Meyen, Nassauvia, and Triptilion Ruiz et Pav.) with 91% support. However, in Simpson et al.’s (2009) Bayesian majority-rule 

tree based on the combined chloroplast DNA and nuclear ITS 
1 2 

• SMITHSONIAN CONTRIBUTIONS TO BOTANY

FIGURE 6. Phylogeny of Perezia, as shown in Figure 3, with areas optimized by dispersal-vicariance analysis (DIVA). Alternative equally optimal reconstructions are shown at 

the nodes. The areas used in this analysis are (A) Subantarctic; (B) Northern Andean; (C) Southern Andean; (D) Patagonia; (E) Puna; (F) Paranense; (G) Chacoan; (H) Pampean; and (I) Espinal. Numbers below nodes are events explained in Table 2. Black symbols represent nodes with many alternative optimal reconstructions.
NUMBER 102 • 1 3

data, this position of P. nutans and P. prenanthoides lacks support based on the maximum parsimony bootstrap value. In addition, Simpson et al. (2009) mentioned that the segregation of this 

group is justified, but their data (not shown) for several samples 

of both species suggest that only one species rather than two may 

be involved in the segregation. Furthermore, the morphological 

characters established by Panero (2007) for the segregation of 

Calorezia Panero from Perezia to support the molecular results 

do not really support such a distinction (for detailed descriptions 

and illustrations of Perezia, see Katinas, 2012). The following 

characters were established by Panero (2007): 

1. Apices of twin trichomes of cypsela are fused, tapered (versus divergent); nondivergent trichomes are found, for example, in P. eryngioides and P. megalantha. 

2. Glandular trichomes have two distinctive rows of cells of 

equivalent width and length and form a straight line between adjacent cells (versus staggered, forming a sinuous 

line); this is a very variable feature that may vary in the 

same individual and is found in many species of Perezia

(e.g., P. delicata and P. linearis). 

3. Capitula is sometimes nodding (versus never nodding); this 

feature may also be found in taxa outside this group, for 

example in P. lactucoides. 

4. Florets are pink-mauve or purple (versus blue, white, or yellow, rarely pink or purple); corolla color is highly variable in 

the genus, and different individuals of the same species may 

have different corolla colors, with pink corollas commonly 

found in many species of Perezia. 

5. Phyllaries are narrowly lanceolate (versus ovate) and usually without hyaline edges (versus with hyaline edges); phyllaries shape is also highly variable in the genus ranging from 

TABLE 2. Results obtained from the dispersal-vicariance analysis (DIVA) depicting the events of dispersal or vicariance at each node of 

the tree of Figure 6.

Node Dispersal events Vicariance events

1 Northern Andean to Puna

2 Northern Andean to Puna

3 Northern Andean to Puna

4 Southern Andean / Northern Andean

5 Northern Andean to Puna and Chacoan

6 Southern Andean / Northern Andean

7 Paranense to Chacoan and Pampean

8 Paranense / Pampean, Espinal

9 Northern Andean, Puna, and Chacoan to Paranense Paranense, Pampean, Espinal / Northern Andean, Puna, Chacoan

10 Southern Andean, Northern Andean / Puna, Paranense, Chacoan, Espinal

11 Southern Andean to Subantarctic

12 Southern Andean to Northern Andean, Puna, 

Paranense, Chacoan, and Espinal

13 Southern Andean to Northern Andean

14 Southern Andean to Subantarctic

15 Southern Andean to Subantarctic

16 Southern Andean to Subantarctic

17 Southern Andean and Subantarctic to Patagonia

18 Southern Andean to Subantarctic

19 Southern Andean to Subantarctic

TABLE 3. Gains and losses for the areas of species in the tree of 

Perezia. The most probable ancestral area (AA) for the group 

corresponds to the higher Gain/Loss (G/L) quotients, in this case 

the Southern Andean area (C).

Area of endemism Gain Loss G/L AA

Subantarctic (A) 6 9 0.66 0.165

Northern Andean (B) 3 14 0.21 0.052

Southern Andean (C) 12 3 4.00 1

Patagonia (D) 1 3 0.33 0.082

Puna (E) 5 16 0.3125 0.078

Paranense (F) 1 14 0.0714 0.017

Chacoan (G) 3 14 0.214 0.053

Pampean (H) 2 14 0.143 0.033

Espinal (I) 1 14 0.0714 0.018
1 4 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

linear to orbicular, and the same is true of the hyaline margins, which may vary in the same capitulum (i.e., phyllaries 

with and without hyaline edges).

Given all these uncertainties, we believe that a monophyletic Perezia, including P. nutans and P. prenanthoides and based 

on morphological data with 65% support, is valid. This monophyly is in line with the pollen ultrastructure, which shows no 

difference between these species and the remainder of the species of Perezia. Likewise, the morphological comparison among 

the species of Perezia and between Perezia and closely related 

genera also shows no characters that support the segregation of 

these two species from the genus (Katinas et al., 2008b; Katinas, 2012). Based on the morphological evidence the phylogeny 

matches the fossil record of the family (Barreda et al., 2010) and 

the biogeographical scenario proposed for early members of the 

family in southern South America (Katinas et al., 2013). It seems 

that the morphological phylogeny presented here is a better fit 

for what we know about Earth history.

In contrast with the molecular work (Simpson et al., 2009), 

our results provide evidence for the monophyly of most of the 

Perezia evolutionary lines proposed by Vuilleumier (1970). The 

only exception is the P. magellanica species group, which consists of two grades and one independent species, suggesting that 

it should not be considered a phylogenetic unit. Both grades include some monophyletic groups, such as those constituted by P. 

delicata–P. lactucoides–P. magellanica, P. capito–P. megalantha, 

and P. pedicularidifolia–P. poeppigii. The P. magellanica species group does not seem to have any morphological characters 

that allow a delimitation of this unit; instead, members share 

the lack of certain features that distinguish the other groups. 

The main characteristic of this group is its geographical distribution in the southern Andes. Simpson (1973) described this 

group as an exemplar case of speciation caused by the isolation 

provided by Pleistocene glaciations in contrast to the P. prenanthoides group, which followed phyletic evolution in old and 

stable habitats. Regarding the other species groups, only two 

have bootstrap values above 50%: the P. prenanthoides species 

group at 70%, and the P. recurvata species group at 65%. Other 

groups did not receive significant support, although they can be 

clearly recognized based on morphology. This is the case with 

the species of the Brazilian-centered P. multiflora species group 

with their eryngioid aspect, the northern Andean-centered P. 

pungens species group with their fruits scarcely pubescent, and 

the P. pinnatifida species groups with their short peduncles and 

amber-colored fruit pubescence. Molecular analyses (Simpson 

et al., 2009) support only the P. multiflora species group and 

the P. recurvata species group. The characters that support the 

species groups in our analysis (Figure 4) are, in general, different from those established by Vuilleumier (1970), who defined them on the basis of morphology, cytology, palynology, 

and chemistry but without a phylogenetic context (Table 1). 

This agreement between Vuilleumier’s (1970) and our results 

enhance the support of the species groups within Perezia. For 

example, Vuilleumier (1970) distinguished the P. multiflora

group by the hemispherical involucre with a reduced number 

of involucral bracts and the silky, copper-colored fruit hairs. In 

our tree this group is supported by the corymbose inflorescence 

and the absence of glandular hairs in the fruits. The only coincidence in the characters between Vuilleumier’s (1970) work and 

the results presented here is the type of inflorescence. In the P. 

prenanthoides species group as defined by Vuilleumier (1970), 

the inflorescence is a showy, open cluster of numerous heads. 

Here it is characterized as having a paniculate inflorescence. 

However, the remaining supporting characters in Vuilleumier’s 

treatment (1970; i.e., large, foliaceous herbs; broad, soft, basal 

leaves; fruits densely covered by amber-colored hairs) are different from those used in our analysis (i.e., glabrous receptacle, 

scarce pubescence in fruits). These differences are brought about 

by our distinction between synapomorphies and plesiomorphies 

in the phylogenetic analysis.

Another remarkable coincidence between our results and 

those of Vuilleumier (1970) is the position of P. pilifera, which 

appears not related to any species group. Vuilleumier (1970) 

considered that the distinctive morphology of this species (e.g., 

different type of pubescence found on the cypsela) made it difficult to determine its relationships. In the phylogeny (Figure 4), P. 

pilifera is the sister of the rest of the species of Perezia. Although 

P. pilifera is morphologically close to the P. recurvata species 

group, both having linear leaves that are exclusive to these taxa, 

the former species has several autapomorphies: leaves with marginal spines, short inflorescences, and long, nonglandular hairs 

in fruits. 

Although viewed as distinctive, Vuilleumier (1970) did 

not suggest that P. pilifera was an early diverging lineage in the 

genus, as occurs in our analysis, but instead suggested that the 

northern Andean-centered P. pungens group provided the stocks 

that gave rise to other evolutionary lines. The ancestor was thus 

hypothesized as a relatively large, leafy, perennial herb with a 

rhizomatous rootstock, a loose panicle of heads, and a likely 

chromosome number of 2n = 8. With regard to the possible early 

diverging members of the genus, the topology of the trees in the 

molecular analysis of Perezia by Simpson et al. (2009) differs 

significantly with Vuilleumier’s (1970) hypothesis and with our 

results. The chloroplast DNA, the nuclear ITS, and the combined 

trees show the Brazilian-centered P. multiflora species group as 

sister of the remaining species of the genus or in a basal polytomy. Simpson et al. (2009) supported the position of P. multiflora at the base of the tree by the low chromosome number of 

this and the other species of the P. multiflora group (2n = 8, 16; 

mistakenly registered as n = 16), which is similar to the chromosome number of the outgroup Panphalea with n = 8. The 

phylogeny presented here shows that the P. multiflora group is 

more highly nested in the tree and that P. pilifera is sister group 

to the remaining species. In addition, the chromosome counts of 

P. pilifera are the same as those of the P. multiflora group: 2n = 
NUMBER 102 • 1 5

16 (Crisci, 1974; Moore, 1981; Nordenstam, 1982). This could 

be interpreted as the repeated acquisition of polyploidy (2n = 

24 in most species groups). The subsequent loss of polyploidy 

in the P. multiflora group, with 2n = 16 (in P. multiflora; Diers, 

1961; Vuilleumier, 1970; and registers of n = 8, Huynh, 1965; 

Dillon, 1982; Spooner et al., 1995; Carr et al., 1999) and n = 4 

(in P. squarrosa subsp. cubataensis; Coleman, 1968), may have 

occurred by disploidy decreases (the change in the chromosomal 

base number through a rearrangement of chromatin and loss of 

centromeres without necessarily changing the amount of chromatin in the karyotype), which is common in Asteraceae (Semple 

and Watanabe, 2009).

Historical Biogeography of Perezia

Previous hypotheses about the probable place of origin of 

the ancestor of Perezia fall into two categories: (1) warm open 

forests of extratropical South America, such as the montane 

habitats of the central Andes (Vuilleumier, 1970), with elements 

that further colonized the southern areas (Simpson, 1973), or (2) 

eastern subtropical South America based on the basal position of 

the Brazilian-centered Perezia multiflora species group (Simpson 

et al., 2009). Our results are in disagreement with both hypotheses. The ancestral areas and dispersal-vicariance approaches applied here are in agreement and strongly support the southern 

Andes as the probable ancestral area for Perezia; this is also the 

area that holds the majority of species in the genus. This southern location is also congruent with the fossil record of the early 

diverging lineages of the family that includes Perezia. Several fossils of early branching lineages of Asteraceae have been found 

from the Paleogene in southwestern Argentina, the earliest from 

the middle Eocene (~50 MYA) (Barreda et al., 2010, 2012). The 

first and only records to date of fossil pollen of Nassauvieae are 

from the early Miocene (23–20 MYA) found in Argentina along 

eastern coast of Patagonia. By the late Miocene (11–9 MYA), 

fossil findings show an abundance of Nassauvieae taxa representing great morphological diversity (Katinas et al., 2007). This 

represents strong evidence supporting the southern origin hypothesis of the genus. 

Because the Andean orogeny influenced the continental biotas, it is important to note that it was not a continuous process. 

Orogeny in the Andean Cordillera was intermittent and episodic 

through Cenozoic times (Ramos, 1989), with uplift events in the 

southern Andes (Incaic and Quechua phases) from the Paleocene to the late Miocene (65–5 MYA), intercalated with a relatively quiescent period from the late Eocene to the late Oligocene 

(37–28 MYA) (Taylor, 1991). The late Oligocene–early Miocene 

interval was a transition time in the vegetation structure, from 

one dominated by tropical forests to one in which shrubby and 

herbaceous elements dominated. At this time members of the 

Asteraceae became increasingly important (Barreda and Palazzesi, 2007). This is the time of the first fossil records of Nassauvieae. During the middle and late Miocene three successive 

Atlantic marine transgressions, known as the Paranean Sea, were 

recorded in southern South America. Accordingly, during this 

time an open seaway, spreading over virtually all of eastern Argentina, western Uruguay, southern Paraguay, and southeastern 

Bolivia, separated terrestrial environments (Figure 7). This barrier surely affected the organism’s distribution, and it could be 

represented in our DIVA results as some of the vicariant events 

separating, for example, the southern and northern Andes from 

the Puna, Paranense, Chacoan, and Espinal areas. During the 

late Miocene–early Pliocene (11–3 MYA) this widespread surface flooding was succeeded by flat regions or plains reaching 

central and northern Argentina, Uruguay, and along the eastern 

slopes of the rising Andes north of Peru. The beginning of these 

new habitats is correlated with the Quechua phase of the Andean diastrophism when Patagonia and the Andean Cordillera 

were successively uplifted (14–10 MYA), progressively forming 

a major barrier to moisture-laden South Pacific winds. The resulting rain-shadow effect on the eastern Patagonian landscapes 

led to the first stages of the differentiation of the present biogeographic regions of southern South America, that is, the Subantarctic and Patagonia (Ortiz-Jaureguizar and Cladera, 2006). 

This differentiation is probably the time period when the ancestors of the extant species of Perezia adapted to the southern 

temperate forests and steppe environments, as shown by the high 

diversity in the Patagonian fossil pollen records of Nassauvieae 

during the late Miocene.

By the Pliocene (5.3–1.8 MYA), a new Andean diastrophic 

phase resulted in the elevation of the central cordillera of Argentina and Chile and the eastern orographic systems (e.g., Puna). 

During this epoch, the final uplift of the Puna had a dramatic 

effect on the biota, creating the very arid and extreme climatic 

conditions that are prevalent today. Our results are congruent 

with this sequence of events and support the hypothesis that the 

area of origin for Perezia is southern and not in younger northern habitats. 

Through the Pleistocene, glaciations were the main climatic factor that affected the Andes and, indeed, most of South 

America. The cyclical advance and retreat of glaciers produced 

a marked and concurrent expansion and retraction of arid (savanna and steppes) and humid (tropical and subtropical) biomes. 

During cold–dry glacial periods there was contraction of the 

areas occupied by subtropical and tropical biomes and expansion and interconnection of open habitats. Conversely, during 

warm–wet interglacial periods, open areas frequently retreated 

to high elevations and rainforest ecosystems expanded. These 

contraction–expansion periods may be the cause of the numerous dispersal events from the highlands of the southern Andes to 

the adjacent lower Subantarctic area, as showed by DIVA, possibly because the species did not completely adapt to the freezing 

temperatures. It is interesting to note that the biogeographical 

approach DIVA minimizes dispersal; despite this fact the results show many dispersal events in the biogeographic history 

of Perezia.
1 6 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

FIGURE 7. Simplified tree of Perezia showing the species groups of Perezia with their ancestral distributions according to DIVA superimposed 

onto a map of South America that shows the areas affected by the middle Miocene–late Miocene marine transgression (modified from OrtizJaureguizar and Cladera, 2006). Species groups are (1) P. pilifera; (2) P. recurvata species group; (3) P. magellanica species group; (4) P. prenanthoides species group; (5) P. magellanica species group; (6) P. multiflora species group; (7) P. pungens species group; (8) P. magellanica

species group; and (9) P. coerulescens (=P. pinnatifida) species group. Symbols represent the areas used in this analysis: Southern Andean (circle); 

Northern and Southern Andean, Puna, Paranense, Chacoan, and Espinal (rectangle); and Northern and Southern Andean (diamond).
NUMBER 102 • 1 7

Integration of Morphology, Ecology, 

Geology, and the Fossil Evidence

The current distribution of Perezia and many other plants 

and animals in the southern Andes is limited by the low temperatures and the winter snow (Cabrera, 1971). Thus, survival 

in freezing temperatures is key to the southern species. Sierra-Almeida and Cavieres (2010) studied several southern Andes plant 

species, including P. carthamoides, to analyze their freezing resistance. They found that these plants have a high ability to resist 

freezing temperatures during the growing season. A high proportion of the species, including P. carthamoides, lose part or all of 

their above-ground tissues before the onset of the less favorable 

winter conditions. This, suggests that they invest resources to 

protect the growth located below ground, accumulate reserves in 

below-ground tissues (a rhizome in the case of Perezia), or both 

instead of cold hardening the above-ground organs. In the past 

(late Oligocene–early Miocene) the southwestern area, hypothesized here as the ancestral area of Perezia, was characterized by 

the dominance of austral elements, indicating a humid, temperate forest (e.g., Nothofagaceae, Araucariaceae, Berberidaceae, 

and Winteraceae), probably with freezing temperatures in the 

higher elevations. Adaptation and speciation, and dispersal of 

early lineages of Perezia to adjacent areas, probably occurred 

under these harsh conditions.

It was suggested for Perezia (Simpson, 1973) and other 

taxa that many species were generated by splitting during the 

Pliocene and Pleistocene glaciations. The repetitious occurrence 

of the glacial cycles allowed opportunities for range expansion 

and subsequent isolation and speciation. This speciation model, 

linked to the Quaternary glaciations, has changed over the years 

in regards to the idea that the Tertiary and Quaternary events 

had different effects in the biotas. During the Tertiary there were 

long periods of uniform environmental conditions, sporadically 

interrupted by geologically short but highly disruptive periods 

of change. These changes drastically modified the taxonomic 

and ecological composition of the biotas by means of cladogenesis, extinction, and migration (Ortiz-Jaureguizar and Cladera, 

2006). The relationship between Andean orogeny and speciation 

has been supported by many workers through the analysis of 

different taxa (e.g., Gentry 1982; Hughes and Eastwood, 2006; 

Pirie et al. 2006). In contrast, the climatic changes during the 

Quaternary had larger amplitude and frequency and were responsible for chorological changes, expanding or contracting the 

distribution areas of taxa, communities, and biomes. Accordingly, we postulate that the main speciation events in Perezia

took place in the Tertiary, probably during the late Oligocene–

late Miocene time span (23–9 MYA), because fossil pollen of 

Nassauvieae was recovered from the Miocene. The Quaternary 

was probably a period of distributional changes in species of 

Perezia, mainly dispersal from the Southern Andes to the lower 

areas of the Subantarctic forest and from the Northern Andes 

down to the Puna, as suggested by DIVA. Marine introgressions 

in South America are hypothesized here as one of the main events 

responsible for the few vicariant events affecting the distribution 

of species of Perezia. 

Our results may have implications for better understanding 

the evolution and historical biogeography of other ancient lineages of Asteraceae, which are undoubtedly linked to the Andes, 

and to other lineages because, as mentioned in the introduction, 

the distribution of Perezia is part of a generalized distributional 

pattern shared by many other taxa.

ACKNOWLEDGMENTS

We acknowledge Jay Walker (Bebb Herbarium University 

of Oklahoma) for his critical reading of the manuscript; Vicki 

Funk (Department of Botany, Smithsonian Institution), the SISP 

editors, and anonymous reviewers for comments; Víctor H. Calvetti for drawing Figures 1 and 3–7; Julieta Tejeda for the design 

of Figure 2; Mauricio Bonifacino (Universidad de la República, 

Montevideo, Uruguay) for the use of his Perezia photographs for 

Figure 2A, D, and G and on the cover; F. Vidoz (Administración 

Parques Nacionales, Argentina) for use of the photo in Figure 

2E; Mihai Costea for use of the photo in Figure 2F, and Rolland 

Douzet from Station Alpine Joseph Fourier (France) for use of 

the photographs for Figure 2B and 2H. The study was financially 

supported by PIP 0729 from CONICET (Argentina) and PICT 

1683 from ANPCyT (Argentina). 

Appendix A: Characters and 

Character States

Below is the numbered list of characters and their numbered character states used in 

the phylogenetic analysis of Perezia (Asteraceae).

1. Life cycle: perennial (0); annual (1).

2. Underground organs: rhizome (0); exclusively roots (1); xylopodium (2).

3. Stem branching: at the base (0); at the apex (1); not branched or scape (2).

4. Leaves disposition: spread along the stem (0); in a basal rosette (1).

5. Upper leaves: numerous (0); few (1–3) to absent (1).

6. Blade shape of basal leaves: less than three times longer than wide (e.g., elliptic, 

lanceolate, obovate) (0); as long as wide (orbicular) (1); at least four times longer 

than wide (linear) (2).

7. Blade apex of basal leaves: acute (0); obtuse (1).

8. Basal leaves venation: pinnate (0); palmate (1).

9. Basal leaves marginal cilia: absent (0); present (1).

10. Leaves with marginal spines: absent (0); present (1).

11. Basal leaves transection: planate (0); revolute or plicate (1).

12. Basal leaves base: sessile (0); petiolate (1); petiole winged (pseudopetiole) (2).

13. Upper leaves shape: wide (0); linear (1).

14. Upper leaves base: sessile (0); clasping (1).

15. Type of inflorescence: clustered (0); lax (1).

16. Height of inflorescence: surpassing the basal leaves (0); shorter than the basal leaves (1).

17. Capitula disposition: glomerulose (0); paniculate (1); corymbose (2); solitary or 2–3 

capitula (3).

18. Number of capitula: 30–50 (0); 1–20 (1).

19. Involucre shape: cylindrical (0); campanulate (1); spherical (2).

20. Involucre length: 5–9 mm (0); 10–20 mm (1); 21–45 mm (2).

21. Receptacle surface: glabrous (0); pubescent (1).

22. Number of series of involucral bracts: 2 (0); 1 (1); 3–5 (2).

23. Scarious margin of involucral bracts: absent (0); present (1).

24. Shape of outer involucral bracts: linear (0); lanceolate to oblong (1); cordate to 

orbicular (2).
2 0 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

25. Margin of outer involucral bracts: entire (0); ciliate (1); 

spiny (2); pectinate (3).

26. Length of outer involucral bracts: shorter than the inner 

bracts (0); as long as or longer than the inner bracts (1).

27. Number of florets per capitulum: 5 (0); more than 5 (1).

28. Corolla color: white (0); colored (1); white and colored (2).

29. Pollen grains polar elevations: absent (0); present (1).

30. Pollen grains tectum: lacking ramifications (0); with 

ramifications (1).

31. Fruit apex: truncate (0); constricted or rostrate (1).

32. Fruit pubescence: absent (0); scarce (1); densely pubescent (2).

33. Type of fruit hairs: glandular hairs and nonglandular (0); 

only glandular hairs (1); only nonglandular hairs (2).

34. Nonglandular hairs shape: cylindrical or elliptical (0); very 

long and filiform (1).

35. Nonglandular hairs color: white to golden (0); reddish (1).

36. Type of pappus bristles: paleaceous (0); capillary (1); absent (2).

37. Color of pappus bristles: white (0); colored (1); white and 

colored (2).
Appendix B: Data Matrix
2 2 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

TABLE B1. The data matrix used in the phylogenetic analysis of Perezia. Character numbers and character states are defined in Appendix A. A question mark (?) indicates inapplicable or missing data. Variable characters in some taxa were treated as polymorphic for 

the analysis.

Species

Character state by character number 

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

Nassauvia magellanica 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 

Panphalea commersonii 0 2 1 1 1 1 1 1 0 0 0 1 1 0 1 0 2 

Panphalea heterophylla 1 1 1 1 1 1 01 1 0 0 0 1 0 1 1 0 2 

Panphalea smithii 0 0 1 1 1 2 0 0 0 0 1 1 1 0 1 0 3 

Perezia atacamensis 0 0 2 1 01 0 0 0 1 1 0 2 0 1 01 0 13 

Perezia bellidifolia 0 0 2 1 1 0 1 0 0 0 0 2 1 0 1 0 3 

Perezia burkartii 0 0 2 1 1 0 01 0 1 0 0 2 1 0 1 0 3 

Perezia calophylla 0 0 1 1 1 0 0 0 0 0 0 2 0 1 1 0 3 

Perezia capito 0 0 2 1 1 0 1 0 0 0 0 2 1 1 1 0 3 

Perezia carthamoides 0 0 1 1 01 0 0 0 1 1 0 2 0 1 1 0 3 

Perezia catharinensis 0 0 1 1 0 0 01 0 0 1 0 0 0 1 1 0 12 

Perezia ciliosa 0 0 2 1 1 0 0 0 1 0 0 2 1 1 1 0 3 

Perezia delicata 0 0 2 1 1 0 1 0 0 0 0 02 1 0 1 0 3 

Perezia dentata 0 0 2 1 0 0 0 0 1 0 0 02 1 1 1 0 3 

Perezia eryngioides 0 0 1 1 0 0 0 0 0 1 0 0 0 1 1 0 2 

Perezia fonkii 0 0 2 1 1 0 1 0 0 0 0 2 1 1 1 0 3 

Perezia kingii 0 1 1 1 0 0 1 0 0 1 0 2 0 1 01 0 2 

Perezia lactucoides 0 0 2 1 0 0 0 0 0 0 0 1 1 1 1 0 3 

Perezia linearis 0 1 2 1 1 2 0 0 1 0 1 0 1 0 1 0 3 

Perezia lyrata 0 0 2 1 1 0 1 0 0 0 0 2 1 0 1 0 3 

Perezia magellanica 0 0 2 1 1 0 1 0 0 0 0 2 1 1 ? 0 3 

Perezia megalantha 0 0 2 1 1 0 1 0 0 0 0 0 0 1 1 0 3 

Perezia multiflora 0 0 1 1 0 0 01 0 0 1 0 2 0 1 0 0 12 

Perezia nutans 0 0 1 1 1 0 1 0 0 1 0 2 0 1 1 0 1 

Perezia pedicularidifolia 0 0 2 1 1 0 0 0 0 0 0 2 0 1 1 0 3 

Perezia pilifera 0 0 2 1 1 2 0 0 0 1 0 0 1 0 1 1 3 

Perezia pinnatifida 0 0 2 1 1 0 1 0 1 0 0 2 1 1 1 1 3 

Perezia poeppigii 0 0 1 1 1 0 01 0 1 0 0 0 1 1 1 0 3 

Perezia prenanthoides 0 0 1 1 1 0 01 0 0 0 0 2 0 1 1 0 1 

Perezia pungens 0 0 1 1 01 0 01 0 01 01 0 12 01 1 01 0 23 

Perezia recurvata 0 0 2 1 01 2 0 0 0 01 1 0 1 0 1 0 3 

Perezia spathulata 0 0 1 1 1 0 1 0 0 0 0 2 0 1 1 0 23 

Perezia squarrosa 0 0 1 1 0 0 0 0 0 1 0 0 0 1 1 0 2 

Perezia volcanensis 0 0 1 1 0 0 01 0 1 1 0 2 0 1 1 0 3 
NUMBER 102 • 2 3

Character state by character number (Continued)

18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 ? ? ? 0 0

1 2 0 0 0 1 1 0 0 1 0 0 1 0 1 2 0 0 2 ?

1 2 0 0 1 1 1 0 ? 1 0 0 1 0 1 2 0 0 2 ?

1 2 0 0 0 1 1 0 0 1 0 0 1 0 1 2 0 0 2 ?

1 1 2 1 2 1 1 0 0 1 2 1 1 0 2 0 0 0 1 1

1 1 1 1 2 1 1 0 0 1 2 1 1 0 2 0 0 0 1 2

1 1 2 0 2 1 2 0 0 1 1 1 1 0 1 2 0 0 1 1

1 1 1 1 2 1 1 0 0 1 1 1 1 0 2 0 1 0 1 2

1 12 12 1 2 1 2 0 0 1 2 1 1 0 1 0 0 1 1 1

1 2 12 0 2 1 1 2 0 1 2 1 1 1 1 0 1 1 1 2

0 1 0 1 02 1 1 1 0 1 0 1 1 0 2 2 1 1 1 1

1 1 1 1 2 1 1 2 0 1 1 1 1 0 1 1 ? ? 1 1

1 12 1 1 2 0 1 0 0 1 1 1 1 0 1 0 0 0 1 1

1 1 1 1 2 1 1 0 0 1 1 1 1 0 2 0 1 0 1 1

0 1 1 1 02 1 1 2 0 1 0 1 1 0 2 2 1 1 1 1

1 1 12 1 2 1 1 0 0 1 1 1 1 0 2 0 1 1 1 1

01 1 0 1 0 1 1 2 1 1 2 1 1 0 2 2 1 1 1 0

1 1 1 1 2 0 1 1 0 1 2 1 1 0 2 0 0 0 1 1

1 1 12 1 2 1 1 1 0 1 2 1 1 0 1 0 0 1 1 2

1 12 1 1 2 1 1 0 0 1 2 1 1 0 2 0 0 1 1 1

1 1 01 1 2 0 1 1 0 1 2 1 1 0 2 0 0 0 1 2

1 2 12 01 2 1 2 1 01 1 2 1 1 0 1 0 0 1 1 1

01 1 1 1 2 1 1 2 0 1 2 1 1 0 2 2 0 1 1 1

1 01 1 0 2 0 1 0 0 1 1 1 1 1 1 0 0 1 1 1

1 1 1 1 2 1 1 3 01 1 1 1 1 1 1 0 0 1 1 1

1 0 1 0 02 1 1 2 0 1 2 1 1 0 2 2 1 0 1 2

1 01 12 0 2 1 1 0 0 1 2 1 1 01 1 0 0 0 1 1

1 01 12 1 2 1 1 2 0 1 1 1 1 1 2 0 0 1 1 1

1 1 01 0 2 1 1 0 0 1 1 1 1 0 1 0 0 1 1 1

1 12 12 1 2 1 1 02 0 1 2 1 1 0 1 0 0 0 1 1

1 1 1 1 2 1 1 2 0 1 2 1 1 0 1 0 0 0 1 1

1 1 12 1 2 1 1 02 0 1 1 1 1 0 2 0 0 1 1 1

1 2 0 1 02 0 1 0 0 1 2 1 1 0 2 0 1 1 1 1

1 2 1 ? 2 1 2 0 0 1 ? 1 1 0 1 ? ? ? 1 1

TABLE B1. (Extended)

Appendix C: 

Areas of Endemism

Described below are the areas of endemism used in the biogeographic analysis of 

the genus Perezia (Asteraceae) defined by Cabrera and Willink (1980), with the Andes 

delimited according to Sick (1969). The areas are listed in order from the temperate to 

the subtropical ones.

Subantarctic Province (A): The Subantarctic province consists of 

temperate forests that range up to 2,000 m in altitude and covers an area from 35°S latitude southward to Cape Horn in Chile, extending along the western side of the southern 

Andes and the Coastal Cordillera, including the Juan Fernandez Islands. In Argentina 

this province extends along the eastern side of the southern Andes from 38°S latitude to 

Islas Malvinas (Falkland Islands) and South Georgia Island. The climate is cold temperate, with abundant snow in the winter and frosts during almost the entire year. The predominant vegetation is the temperate mixed deciduous and evergreen forest, represented 

mainly by the genus Nothofagus (Nothofagaceae). The parasitic plant family Misodendraceae is endemic to this area—endemic genera of this family include Austrocedrus, Fitzroya, and Pilgerodendron (Cupressaceae) and Macrachaenium (Asteraceae). And several 

other endemic plant and animal species are present, such as Dromiciops australis and 

Rhyncholestes raphanurus (Marsupialia); Felis guigna (Carnivora); Pudu puda (Artiodactyla); and Irenomys australis, Akodon herschkovitzi (Rodentia).

Northern Andean (B): This area belongs to the Altoandean highlands 

with its typical dry and cold high-mountain climate. The main forms of precipitations in 

the Altoandean highlands are snow and hail, especially in the winter. The predominant 

vegetation type is the grassy and chamaephyte steppes, with plant adaptations to extreme 

climatic conditions. The Northern Andean section consists of the Andean highlands at 

3,000–4,500 m, reaching the permanent snow and extending from 27°–28°S latitude to 

the northern end of the Andes. This section with subtropical climate contrasts with the 

adjoining temperate southern section. The symmetry of the precipitation distribution, 

with heavy rainfalls on both sides of the northern range, gives way at approximately 4°S 

latitude to a dry west side, due to the influence of the Pacific anticyclones, and a humid 

eastern side, within the range of easterly air-streams (Sick, 1969). Endemic taxa include, 

for example, Hyppocamelus antisensis (Artiodactyla); Auliscomys boliviensis, Chinchilla 

brevicaudata, and Phyllotis magister (Rodentia); Felis jacobita (Carnivora); Lapageria 
2 6 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

rosea (Philesiaceae); Aciachne flagellifera and A. pulvinata (Poaceae); Aschersoniodoxa chimborazensis (Brassicaceae); Astragalus fabrisii (Fabaceae); and Leucheria pteropogon and Mutisia 

grandiflora (Asteraceae).

Southern Andean (C): This unit also belongs 

to the Altoandean highlands but ranges from 27°–28°S latitude 

to the southern end of the Andes, and altitude decreases from 

3,000 m to 500 m in the southern Argentinian province of Tierra 

del Fuego (at 54°S). The border between the Northern and the 

Southern Andean areas is a complex region that coincides with 

the boundaries among the Frontal Cordillera, the Cuyo Precordillera, the Principal Cordillera (Ramos et al., 2002), and 

the southern end of the Puna area. There is a transition from 

subtropical to temperate climate, with temperatures decreasing 

toward the south. The eastern and western slopes of the vast 

mountain range overall also differ in the amount of precipitation 

received but in a manner opposite to that in the northern Andes. 

The influence of the westerly winds can be traced, with cyclonic 

winter rain in association with summer dryness. Endemic taxa 

include, for example, Hyppocamelus bisulcus (Artiodactyla), Astragalus bellus (Fabaceae), and Nassauvia pinnigera, N. argentea, Leucheria eriocephala, L. nutans, and Mutisia linearifolia

(Asteraceae).

Patagonia (D): This area comprises the extraAndean semidesert area of Argentina and Chile from 37°S 

(Argentina) and 43°S (Chile) to Cape Horn at 56°S latitude. It includes the Pacific and Atlantic lowlands and coasts, the southern 

archipelagos, and the valleys, tablelands, and high plains extending between the Andes and the Atlantic and Pacific Oceans. This 

area is included in the circulation zone of the southern westerlies, 

reaching strong intensity in southern areas. In terms of vegetation 

it is a semiarid shrubby steppe with a predominance of cushion 

plant adaptation. There are many endemic genera, Ameghinoa, 

Pantacantha, Benthamiella, and Lepidophyllum (Asteraceae), 

and endemic species, such as Nassauvia axilaris, N. glomerulosa, 

and Chuquiraga avellanedae (Asteraceae); Retanilla patagonica

(Rhamnaceae); Festuca pallescens (Poaceae); and Akodon iniscatus, Notiomys edwardisii, Ctenomys colburni, C. haigi, and C. 

sericeus (Rodentia).

Puna (E): This area comprises the highland plateaus located in Peru, western Bolivia, northwestern Argentina, 

and northern Chile, basically between 15° and 30° S latitude and 

higher than 3,000 m altitude. It stretches for 1,800 km along the 

Central Andes and attains a width of 350–400 km. Climate is 

cold and dry, with summer rains. It is a semiarid shrubby steppe, 

with some areas of grassy steppe and open forests of Polylepis 

tomentella (Rosaceae). Endemic taxa include, for example, Nardophyllum armatum and Parastrephia lepidophylla (Asteraceae), 

Hoffmansegia minor (Fabaceae), Solanum acaule (Solanaceae), 

Chaetophractus nationi (Edentata), Vicugna vicugna (Artiodactyla), and Auliscomys sublimis and Phyllotis osgoodi (Rodentia).

Paranense (F): The Paranense area is a subtropical forest that ranges across southern Brazil (west of Serra do 

Mar), eastern Paraguay, and northeastern Argentina. The climate 

is warm and humid with precipitation during the entire year. 

There are different communities, such as forests of Araucaria 

angustifolia (Araucariaceae) and Euterpe edulis (Arecaceae) and 

grassy savannas. Endemic taxa include, for example, Nectandra 

lanceolata and Ocotea lancifolia (Lauraceae); Mikania summinima and Viguiera misioensis (Asteraceae); Dyckia mitis and D. 

niederleinii (Bromeliaceae), Monodelphis scalops (Marsupialia); 

and Thomasomys dorsalis, T. pictipes, Oryzomys buccinatus, 

Akodon nigrita, A. serrensis, Euryzygomatomys spinosus, and 

Kannabateomys amblyonyx (Rodentia).

Chacoan (G): The Chacoan area extends over 

southern and western Bolivia, western Paraguay, and northcentral Argentina. Its vegetation is a sclerophyllous, deciduous 

forest with tickets of savannas, grasslands, and shrubby steppes. 

There are forests of species of Schinopsis (Anacardiaceae), Prosopis (Fabaceae), and Aspidosperma quebracho-blanco (Apocynaceae). The climate is warm and dry, with more precipitation 

in the east. Endemic taxa include, for example, Alternanthera 

collina (Amaranthaceae), Aristolochia schulzii (Asclepiadaceae), 

Grindelia chacoensis and Hyaloseris andrade-limae (Asteraceae), 

Opuntia colubrina (Cactaceae), Marmosa formosa (Marsupialia), Vampyrops dorsalis (Chiroptera), and Oryzomys chacoensis, Pseudoryzomys wavrini, Andalgalomys pearsoni, Bibimys 

chacoensis, Ctenomys argentinus, and C. bonettoi (Rodentia).

Pampean (H): The Pampean area is a grassy 

steppe that extends between ~30° and 38°S latitude in southeastern Brazil, Uruguay, and east-central Argentina. This flat area 

is interrupted by the Tandilia and Ventania ranges (500 m and 

1,000 m high, respectively). Precipitation decreases from northeast to southwest and occurs throughout the year, with mild 

summer water deficits in the east and more severe winter dry 

periods in the west. Endemic taxa include, for example, Baccharis rufescens and Hieracium burkartii (Asteraceae), Rorippa 

ventanensis (Brassicaceae), Adesmia pampeana (Fabaceae), Bromus bonariensis (Poaceae), Eryngium cabrerae (Apiaceae), and 

Thomasomys oenax, Oryzomys delticola, Akodon kempi, Holochilus magnus, Ctenomys australis, C. minutus, C. pearsoni, C. 

porteousi, and C. talarum (Rodentia). 

Espinal (I): The Espinal area is a belt-shaped system of open xerophytic forests, with parklands, palm groves, 

bushy steppes, and savannas that surround the Pampean biogeographic province. The climate is warm and humid in the north 

and temperate semiarid in the west and south sections. The tree 

overstory has varying densities dominated by Prosopis and Acacia species (Fabaceae). Tree species richness declines southward, 

and plant species found in this area are generally found in other 

surrounding biogeographic provinces. Endemic taxa include, for 

example, Grindelia globularifolia and Hieracium caespitosa (Asteraceae); Adesmia lihuelensis and Prosopis caldenia (Fabaceae); 

Cereus argentinense and Gymnocalycium mesopotamicum

(Cactaceae); Oxypetalum fontellae (Asclepiadaceae); Croton 

laureltyanus (Euphorbiaceae); Ctenomys azarae and C. perrensis

(Rodentia); and Sturnella defilippii (Aves).
References

Antonelli, A., J. A. A. Nylander, C. Persson, and I. Sanmartín. 2009. Tracing the Impact of the Andean Uplift 

on Neotropical Plant Evolution. Proc. Natl. Acad. Sci. U.S.A. 106:9749−9754. http://dx.doi.org/10.1073

/pnas.0811421106.

Barreda,V., and L. Palazzesi. 2007. Patagonian Vegetation Turnovers during the Paleogene−Early Neogene: Origin 

of Arid-Adapted Floras. Bot. Rev. 73:31−50. http://dx.doi.org/10.1663/0006-8101(2007)73[31:PVTDTP]2

.0.CO;2..

Barreda, V. D., L. Palazzesi, L. Katinas, J. V. Crisci, M. C. Tellería, K. Bremer, M. G. Passalia, F. Bechis, and 

R. Corsolini. 2012. An Extinct Eocene Taxon of the Daisy Family (Asteraceae): Evolutionary, Ecological, 

and Biogeographical Implications. Ann. Bot. 109:127−134. http://dx.doi.org/10.1093/aob/mcr240.

Barreda, V., L. Palazzesi, M. C. Tellería, L. Katinas, J. V. Crisci, K. Bremer, M. G. Passalia, R. Corsolini, R. Rodríguez Brizuela, and F. Bechis. 2010. Eocene Patagonia Fossils of the Daisy Family. Science 329:1621. http://

dx.doi.org/10.1126/science.1193108.

Bremer, K. 1992. Ancestral Areas: A Cladistic Reinterpretation of the Center of Origin Concept. Syst. Biol.

41:795−803. http://dx.doi.org/10.1093/sysbio/41.4.436.

Cabrera, A. 1971. Fitogeografía de la República Argentina. Bol. Soc. Argent. Bot. 14:1−42.

Cabrera, A. L., and A. Willink. 1980. Biogeografía de América Latina. Serie de Biología, Monografía 13. Organización de los Estados Americanos, Washington, D.C.

Carr, G. D., R. M. King, A. M. Powell, and H. Robinson. 1999. Chromosome Numbers in Compositae. XVIII. 

Am. J. Bot. 86:1003−1013. http://dx.doi.org/10.2307/2656618.

Coleman, J. R. 1968. Chromosome Numbers in Some Brazilian Compositae. Rhodora 70:228−240.

Crisci, J. V. 1974. A Numerical-Taxonomic Study of the Subtribe Nassauviinae (Compositae, Mutisieae). J. Arnold 

Arbor. 55:568−610. 

Crisci, J. V., M. M. Cigliano, J. J. Morrone, and S. Roig-Juñent. 1991. Historical Biogeography of Southern South 

America. Syst. Zool. 40:152−171. http://dx.doi.org/10.2307/2992254.

Crisci, J. V., L. Katinas, and P. Posadas. 2003. Historical Biogeography: An Introduction. Harvard University 

Press, Boston, Mass.

Diers, L. 1961. Der Anteil an Polyploiden in den Vegetations gurteln der Westkordillere Perus. Österr. Bot. Z.

49:437−488.

Dillon, M. O. 1982. Additions to the Tribe Vernonieae (Compositae): I. Flora of Peru. Fieldiana, Bot. 11:1−7.

Felsenstein, J. 1985. Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution 39:783−791. 

http://dx.doi.org/10.2307/2408678.

Funk, V. A., A. Susanna, T. F. Stuessy, and H. Robinson. 2009. Classification of Compositae. In Systematics, Evolution, and Biogeography of the Compositae, V. A. Funk, A. Susanna, T. F. Stuessy, and R. Bayer, eds., pp. 

171–189. International Association for Plant Taxonomy, Vienna.

Gentry, A. H. 1982. Neotropical Floristic Diversity: Phytogeographical Connections between Central and South 

America, Pleistocene Climatic Fluctuations, or an Accident of the Andean Orogeny? Ann. Mo. Bot. Gard. 

69:557−593. http://dx.doi.org/10.2307/2399084.

Gregory-Wodzicki, K. M. 2000. Uplift of the Central and Northern Andes: A Review. Geological Society of America Bulletin 112:1091−1105. http://dx.doi.org/10.1130/0016-7606(2000)112<1091:UHOTCA>2.0.CO;2.

Hughes, C., and R. Eastwood. 2006. Island Radiation on a Continental Scale: Exceptional Rates of Plant Diversification after Uplift of the Andes. Proc. Natl. Acad. Sci. U.S.A. 103:10334−10339. http://dx.doi.org/10.1073/

pnas.0601928103.

Humphries, C. J. 1981. Biogeographical Methods and the Southern Beeches (Fagaceae: Nothofagus). In Advances 

in Cladistics: Proceedings of the First Meeting of the Willi Hennig Society, V. A. Funk and D. R. Brooks, eds., 

pp. 177−207. New York Botanical Garden, Bronx, N.Y.
2 8 • SMITHSONIAN CONTRIBUTIONS TO BOTANY

Huynh, K. L. 1965. Contribution a l’etude caryologique et embriologique des Phanerogames du Perou. Verh. Schweiz. naturforsch. Ges. 85:1−178.

Katinas, L. 2012. Revisión del género Perezia (Asteraceae). Bol. Soc. Argent. Bot. 

47:159−261.

Katinas, L., J. V. Crisci, P. Hoch, M. C. Tellería, and M. J. Apodaca. 2013. TransOceanic Dispersal and Evolution of Early Composites (Asteraceae). Perspect. 

Plant Ecol. Evol. Syst. 15:269−280. http://dx.doi.org/10.1016/j.ppees.2013

.07.003.

Katinas, L., J. V. Crisci, R. Schmidt Jabaily, C. Williams, J. Walker, B. Drew, J. M. 

Bonifacino, and K. J. Sytsma. 2008a. Evolution of Secondary Heads in Nassauviinae (Asteraceae, Mutisieae). Am. J. Bot. 95:229−240. http://dx.doi

.org/10.3732/ajb.95.2.229.

Katinas, L., J. V. Crisci, M. C. Tellería, V. Barreda, and L. Palazzesi. 2007. Early 

History of Asteraceae in Patagonia: Evidence from Fossil Pollen Grains. N. Z. 

J. Bot. 45:605−610. http://dx.doi.org/10.1080/00288250709509742.

Katinas L., J. Pruski, G. Sancho, and M. C. Tellería. 2008b. The subfamily Mutisioideae (Asteraceae). Bot. Rev. 74:469−716. http://dx.doi.org/10.1007

/s12229-008-9016-6.

Kuschel, G. 1969. Biogeography and Ecology of South American Coleoptera. In 

Volume 2: Biogeography and Ecology in South America, E. J. Fittkau, J. Illies, H. Klinge, G. H. Schwabe, and H. Sioli, eds., pp. 709−722. Dr. W. Junk 

NV, The Hague. 

Luebert, F., J. Wen, and M. O. Dillon. 2009. Systematic Placement and Biogeographical Relationships of the Monotypic Genera Gypothamnium and Oxyphyllum (Asteraceae: Mutisioideae) from the Atacama Desert. Bot. J. Linn. 

Soc. 159:32–51. http://dx.doi.org/10.1111/j.1095-8339.2008.00926.x.

Maddison, W. P., and D. R. Maddison. 1992. MacClade: Interactive Analysis of 

Phylogeny and Character Evolution, Version 3.0. Sinauer Associates, Sunderland, Mass. 

Moore, D. 1981. Chromosome Numbers of Fuegian Angiosperms. Bol. Soc. Broteriana 53:995−1012.

Nordenstam, B. 1982. Chromosome Studies in the Southern African Flora. S. Afr. 

J. Bot. 48:277−278.

Ortiz-Jaureguizar, E., and G. A. Cladera. 2006. Paleoenvironmental Evolution of 

Southern South America during the Cenozoic. J. Arid Environ. 66:498−532. 

http://dx.doi.org/10.1016/j.jaridenv.2006.01.007.

Panero, J. L. 2007. Calorezia, a New Genus of Tribe Nassauvieae (Asteraceae, 

Mutisioideae). Phytologia 89:198−201.

Pirie, M. D., L. W. Chatrou, J. B. Mols, R. H. J. Erkens, and J. Oosterhof. 2006. 

‘Andean-Centred’ Genera in the Short-Branch Clade of Annonaceae: Testing 

Biogeographical Hypotheses using Phylogeny Reconstruction and Molecular 

Dating. J. Biogeogr. 33:31−46. http://dx.doi.org/10.1111/j.1365-2699.2005

.01388.x.

Platnick, N. I. 1991. On Areas of Endemism. Aust. Syst. Bot. 4:11−12.

Ramos, V. A. 1989. The Birth of Southern South America. Am. Sci. 77:444−450.

Ramos, V. A., E. O. Cristallini, and D. J. Pérez. 2002. The Pampean Flat-Slab of the 

Central Andes. J. South Am. Earth Sci. 15:59−78. http://dx.doi.org/10.1016

/S0895-9811(02)00006-8.

Ritz, C. M., L. Martins, R. Mecklenburg, V. Goremykin, and F. H. Hellwig. 2007. 

The Molecular Phylogeny of Rebutia (Cactaceae) and Its Allies Demonstrates 

the Influence of Paleogeography on the Evolution of South American Cacti. 

Am. J. Bot. 94:1321−1332. http://dx.doi.org/10.3732/ajb.94.8.1321.

Ronquist, F. 1994. Ancestral Areas and Parsimony. Syst. Biol. 43:267−274. http://

dx.doi.org/10.1093/sysbio/43.2.267.

———. 1995. Ancestral Areas Revisited. Syst. Biol. 44:572−575. http://dx.doi.org

/10.1093/sysbio/44.4.572.

———. 1996. DIVA, Version 1.1. Computer program and manual available by 

anonymous FTP from Uppsala University (ftp.uu.se or ftp.systbot.uu.se).

———. 1997. Dispersal-Vicariance Analysis: A New Approach to the Quantification 

of Historical Biogeography. Syst. Biol. 46:195–203. http://dx.doi.org/10.1093

/sysbio/46.1.195.

Semple, J. C., and K. Watanabe. 2009. A Review of Chromosome Numbers in 

Asteraceae with Hypotheses on Chromosomal Base Number Evolution. In 

Systematics, Evolution, and Biogeography of the Compositae, V. A. Funk, 

A. Susanna, T. F. Stuessy, and R. Bayer, eds. pp. 61–72. International Association for Plant Taxonomy, Vienna.

Sick, W. D. 1969. Geographical Substance. In Volume 2: Biogeography and Ecology in South America, E. J. Fittkau, J. Illies, H. Klinge, G. H. Schwabe, and 

H. Sioli, eds., pp. 449−474. Dr. W. Junk NV, The Hague. 

Sierra-Almeida, A., and L. A. Cavieres. 2010. Summer Freezing Resistance Decreased in High-Elevation Plants Exposed to Experimental Warming in the 

Central Chilean Andes. Oecologia 163:267−276. http://dx.doi.org/10.1007

/s00442-010-1592-6.

Simpson, B. B. 1973. Contrasting Modes of Evolution in Two Groups of Perezia

(Mutisieae: Compositae) of Southern South America. Taxon 22:525−536. 

http://dx.doi.org/10.2307/1218627.

Simpson, B. B., M. T. K. Arroyo, S. Sipe, M. Dias de Moraes, and J. McDill. 

2009. Phylogeny and Evolution of Perezia (Asteraceae: Mutisieae: Nassauviinae). J. Syst. Evol. 47:431−443. http://dx.doi.org/10.1111/j.1759

-6831.2009.00039.x.

Spooner, D. M., D. C. de Jong, B. Y. Sun, T. F. Stuessy, K. M. Gengler, G. L., 

Nesom, and P. E. Berry. 1995. Chromosome Counts of Compositae from 

Ecuador and Venezuela. Ann. Mo. Bot. Gard. 82:596−602. http://dx.doi

.org/10.2307/2399840.

Swofford, D. I. 1999. PAUP*. Phylogenetic Analysis Using Parsimony (* and other 

methods), Version 4. Sinauer Associates, Sunderland, Mass. 

Taylor, D. W. 1991. Paleobiogeographic Relationships of Andean Angiosperms 

of Cretaceous to Pliocene Age. Palaeogeogr. Palaeoclimatol. Palaeoecol. 

88:69−84. http://dx.doi.org/10.1016/0031-0182(91)90015-J.

Vuilleumier, B. S. 1970. The Systematics and Evolution of Perezia Section Perezia

(Compositae). Contrib. Gray Herb. Harvard Univ. 199:1–163. 

Watrous, L. E., and Q. D. Wheeler. 1981. The Out-Group Comparison Method 

for Character Analysis. Syst. Zool. 30:1−11. http://dx.doi.org/10.2307

/2992297.
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