# Parallel Ecological Speciation in Plants?

Authors: Katherine L. Ostevik; Brook T. Moyers; Gregory L. Owens; Loren H. Rieseberg
Journal: International Journal of Ecology
 (2012)

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## Abstract

Populations that have independently evolved reproductive isolation from their ancestors while remaining reproductively cohesive have undergone parallel speciation. A specific type of parallel speciation, known as parallel ecological speciation, is one of several forms of evidence for ecology's role in speciation. In this paper we search the literature for candidate examples of parallel ecological speciation in plants. We use four explicit criteria (independence, isolation, compatibility, and selection) to judge the strength of evidence for each potential case. We find that evidence for parallel ecological speciation in plants is unexpectedly scarce, especially relative to the many well-characterized systems in animals. This does not imply that ecological speciation is uncommon in plants. It only implies that evidence from parallel ecological speciation is rare. Potential explanations for the lack of convincing examples include a lack of rigorous testing and the possibility that plants are less prone to parallel ecological speciation than animals.


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## Body

## 1. Introduction

The past two decades have witnessed a dramatic shift in studies of speciation from an emphasis on stochastic and other nonecological processes to a focus on ecological mechanisms of speciation. Indeed, the proverbial pendulum has swung so far toward ecology that some authors have argued that essentially all plausible types of speciation involve ecological processes [1]. Despite the pervasive role of natural selection in evolution, evidence that ecologically based divergent natural selection is the primary cause of reproductive isolation (ecological speciation sensu Schluter, 2001 [2]) is often weak or incomplete in case studies [3].To more critically evaluate the importance of ecological speciation in nature, several authors have suggested methods for reliably inferring ecological speciation [2–5]. These include (1) direct measurements of divergent ecological selection on parental genotypes (e.g., immigrant inviability) or hybrids (i.e., extrinsic postzygotic isolation) in the different environments; (2) natural selection studies showing that phenotypic differences underlying premating reproductive barriers are a consequence of divergent ecological selection; (3) molecular marker studies of selection against immigrants (i.e., isolation by adaptation); (4) molecular evolutionary studies linking intrinsic genetic incompatibilities with divergent ecological selection; and (5) tests of parallel ecological speciation, which is the process in which related lineages independently evolve similar traits that confer shared reproductive isolation from their ancestral populations [6].In plants, widespread application of the first two methods listed above points to an important role for ecology in speciation. For example, there is a long tradition of reciprocal transplant studies since early in the 20th century, and there is abundant evidence of immigrant inviability among recently diverged populations or species [7, 8]. Because habitats often are spatially segregated, divergent habitat adaptation results in ecogeographic isolation, which is considered by many botanists to be the most important reproductive barrier in plants [1, 9]. Likewise, studies that examine the relative importance of different components of reproductive isolation in plants indicate that ecologically based reproductive barriers often play a key role in the early stages of plant speciation [8]. However, evidence of extrinsic postzygotic isolation in plants is surprisingly weak, possibly because of heterosis [8, 10]. Also, few studies have explicitly tested for isolation by adaptation in plants [1] or for ecological causes of hybrid incompatibilities (reviewed in [11]). The evidence for parallel ecological speciation is perhaps least clear because while “recurrent” formation of plant species and races is thought to be common [12], the evidence underlying these apparent examples has not been examined systematically.On the other hand, parallel speciation is regularly cited as evidence for ecological speciation in animals (e.g., [6, 13–22]), and the evidence for many individual cases of parallel ecological speciation is strong. For example, the threespine stickleback has undergone several well-documented parallel transitions between environments. The most well-known case is likely the independent origin of “benthic” and “limnetic” ecotypes in at least five British Columbian lakes [23, 24]. Another well-studied system is the marine snail Littorina saxatilis, which has repeatedly evolved pairs of ecotypes on the rocky coasts of Northwestern Europe [25]. Numerous other strong candidates for parallel ecological speciation are found in animals, including but not limited to lake whitefish [26], cave fish [27], walking sticks [20], scincid lizards [21], lamprey [28], electric fish [29], horseshoe bats [30], and possibly even in the genetic model organism Drosophila melanogaster [31], though not all of these examples are fully validated with the criteria described below.Here we use explicit criteria to evaluate the strength of evidence for parallel ecological speciation in plants. We evaluate plant systems using criteria that are more often used to evaluate animal systems because comparable evaluations across taxa are important for determining general patterns of speciation. We find that evidence for parallel ecological speciation in plants is surprisingly rare in comparison to animals and provide potential explanations for this finding.


## 2. Studying Parallel Ecological Speciation

Parallel speciation is the process in which related lineages independently evolve similar traits that confer shared reproductive isolation from their ancestral populations [6]. It is good evidence that selection drove the evolution of reproductive isolation, as it is unlikely that the same barriers would arise independently by chance [6]. Schluter and Nagel [6] listed three criteria for parallel speciation: (1) related lineages that make up the new descendent populations are phylogenetically independent; (2) descendent populations are reproductively isolated from ancestral populations; (3) independently derived descendent populations are not reproductively isolated from each other. They add that an adaptive mechanism must be identified to show that natural selection drove the evolution of reproductive isolation [6]. Together, these four conditions are the evidence necessary to demonstrate the process we refer to as parallel ecological speciation. We choose to use the term “parallel” over the alternative term “convergent” because of the initial similarity of the independent lineages [32–34] and because this vocabulary is consistent with the original description of the process [6].If we apply these criteria to well-known examples of parallel or “recurrent” speciation in plants [12], it is clear that botanists and zoologists are mainly studying different things. For example, many auto- and allopolyploid species have multiple independent origins (reviewed in [35]), in which independently derived polyploid lineages are reproductively isolated from their common ancestor but not from one another. Additionally, a high proportion of homoploid hybrid species studied arose in parallel [36]. Although there is evidence that natural selection is important in polyploid and hybrid speciation [10, 37, 38], the genomic changes that accompany polyploidization and hybridization reduce our ability to show that parallel ecological selection was the primary driver of reproductive isolation. This differentiates parallel polyploid and hybrid speciation from parallel ecological speciation described above and represented in the animal cases listed previously.In cases of parallel ecological speciation, the independent descendent populations are found in a new environment where they experience new and shared ecological selection that causes speciation. However, not all cases in which multiple transitions to a new environment are associated with repeated speciation events represent true parallel ecological speciation. Several possible patterns exist and are shown in Figure1. In parallel ecological speciation, ancestral and descendent groups each represent single compatible groups (Figure 1(a)). However, one can also envision several other patterns, in which either the ancestral or descendent groups (or both) represent multiple compatibility groups (Figures 1(b)–1(d)).An illustration of several patterns in which multiple independent transitions to a new environment are coupled with speciation. The yellow and green boxes represent two different environments, the arrows represent multiple independent transitions between the environments, and the closed shapes represent reproductively compatible groups. Only panel (a) represents parallel ecological speciation, the process we are interested in.
(a)(b)(c)(d)The pattern in which the descendent groups are incompatible with one another (Figure1(b)) can be caused by mutation-order speciation in which the same selective pressure leads to different genetic changes in the multiple populations [4]. The isolation between ancestral groups could also be the result of drift. The third pattern (Figure 1(c)) has been called “replicated ecological speciation” [39] and is made up of multiple distinct speciation events. Studying similarities and differences between these replicate speciation events can help identify general patterns of speciation [39]. Finally, the last pattern (Figure 1(d)) is to our knowledge novel, and we do not know of any empirical examples.In this survey, however, we are only interested in parallel ecological speciation (Figure1(a)), which tells us something more specific than other patterns. In particular, parallel ecological speciation indicates that all of the new barriers present are predominantly if not entirely due to natural selection, whereas in the other cases, other forces may have been at play along with natural selection. For example, if the descendent populations are reproductively isolated from one another (Figures 1(b) and 1(c)), it is plausible that changes, driven by processes other than ecological adaptation, caused the isolation between descendent populations as well as the isolation across habitats. This means that testing the compatibility of descendent populations is essential for documenting parallel ecological speciation. However, this test is not necessary for demonstrating all forms of evidence for ecological speciation.When studying parallel ecological speciation, it is also useful to recognize that evidence of parallelism may or may not extend across multiple levels of biological organization. Although the individuals of the descendent species must have the same isolating trait, this common trait is not necessarily governed by the same mutation, gene, or even pathway in the different replicates. Even when the same mutations are responsible for parallel transitions in a given isolating trait, these mutations can be either the result of recurrentde novo mutation or standing variation. While independent genetic changes simplify the task of reconstructing population and trait histories, parallel changes from standing genetic variation can be useful for pinpointing regions of the genome responsible for ecological selection and reproductive isolation [40].


## 3. Literature Survey

For this survey, we searched the scientific literature for evidence of parallel ecological speciation in plants. We used combinations of the words “parallel”, “recurrent”, “multiple”, “convergent” and “speciation”, “evolution”, “origins”, “reproductive barriers/isolation” as well as “paraphyly” as search terms in Web of Science and Google Scholar. We also examined all papers citing candidate examples and searched for additional papers about the candidate species. Levin [12] reviewed a number of potential cases of parallel ecological speciation in plants. Although his paper was not strictly about parallel ecological speciation, we consider all of his ecological examples in our table in order to revisit their validity and discuss new evidence for each case. We used explicit criteria to determine the strength of evidence for parallel ecological speciation. Specifically, we judged the strength of evidence for each of the aforementioned four criteria: independence, isolation, compatibility, and selection. To merit inclusion, we required that each newly identified case has at minimum weak direct evidence for repeated adaptation to similar environments (independence) or multiple origins of an isolating trait (isolation) and indirect evidence for the other condition. Evidence that an example failed to meet any of the four criteria resulted in its exclusion. As a result, several promising systems were not included in our table or appendix (e.g., Frankenia ericifolia [41] and Heteropappus hispidus ssp. Leptocladus [42]). This was because Frankenia ericifolia has only indirect evidence of both independence and isolation and Heteropappus hispidus ssp. Leptocladus has no evidence of isolating traits. Lastly, we evaluated a few of the frequently cited examples of parallel ecological speciation in animals for comparison. The list of animal examples is not exhaustive and does not necessarily include all of the best cases.The following sections discuss each criterion and the types and strengths of evidence we considered.


### 3.1. Independence

Parallel speciation requires that replicate lineages be phylogenetically independent, so that the “shared traits responsible for reproductive isolation evolved separately” [6]. Estimating phylogenetic independence can be difficult for recently diverged taxa because of inadequate resolution, hybridization and introgression, and deep coalescence. These issues are exacerbated when phylogenies are based on a small number of loci or if the loci employed have little phylogenetic information content (e.g., isozymes). Additionally, it is not strictly necessary for populations to be phylogenetically independent for reproductive barriers to evolve separately, if different genes, mutations, or genetic pathways are exploited by selection in populations that remain connected by gene flow.Therefore, in this survey, strong evidence for independent evolution includes: (1) phylogenetic analyses supporting independence with multiple, phylogenetically informative loci or (2) direct evidence that a shared isolating trait has evolved independently (e.g., the trait is a result of different mutations in different populations). Phylogenetic analyses with a single locus, or with loci having little information content, are deemed weak direct evidence. Note that we consider genetic information from completely linked markers (e.g., multiple genes sequenced from the chloroplast genome) as information from one locus. Finally, indirect evidence for independence could include the improbability of long-distance colonization or gene flow between geographically separated but ecologically similar habitats, or phenotypes that are similar but not identical suggesting different genetic bases.


### 3.2. Isolation

As with any test of incipient or recent speciation, reproductive isolation must have evolved between descendent and ancestral populations, though not necessarily to completion. For strong evidence of isolation, we require experimental evidence for strong reproductive barriers that are genetically based, such as substantial differences in flowering time or pollination syndrome in a common garden and/or F1 hybrid inviability or sterility. Experimentally demonstrated weak but statistically significant reproductive barriers between diverging populations (including selection against immigrants and hybrids), or genetic divergence between locally diverging populations despite the opportunity for gene flow, are considered weak evidence for isolation. We view systems with apparent immigrant or hybrid inviability (e.g., serpentine adaptation), long-term persistence of divergent populations in sympatry, or strong divergence in mating system as indirect evidence that barriers likely exist. Although we would not consider isolation that has no genetic basis as evidence for parallel ecological speciation, we acknowledge that phenotypic plasticity can facilitate or impede the evolution of reproductive barriers and is an important consideration for studies of ecological speciation [43] (e.g., [44]). Furthermore, because explicitly testing that isolation is genetically based was rare in our candidate studies, we only required the genetic basis of isolation to be confirmed for cases to have strong direct evidence.


### 3.3. Compatibility

As we briefly discuss above, the lack of reproductive barriers between descendent populations is a key criterion distinguishing true parallel ecological speciation from other forms of replicated ecological speciation (Figure1). For strong evidence of reproductive compatibility we require that descendent populations show little or no barriers to reproduction when experimentally crossed and minimal ecological divergence as demonstrated by reciprocal transplant or manipulative ecological experiments. If only one of these two components of compatibility were demonstrated, we consider the evidence to be weak. We also consider substantial genetic analysis showing little genetic differentiation at neutral markers between the descendent populations to be weak direct evidence for compatibility, although this might weaken the case for the criterion of independence. Lastly, if the evolution of environmental specificity or mating system is such that descendant populations are indistinguishable in these parallel traits and have no other phenotypic differences, we consider this indirect evidence for compatibility.It is difficult to ascertain the strength of evidence for isolation and compatibility when multiple independent origins of self-fertilization (autogamy) have occurred. This is because replicate populations of selfers are likely to be as strongly isolated from one another as they are from the ancestral outcrossing populations. For this reason, replicated selfing lineages were excluded from consideration unless accompanied by the evolution of other reproductive barriers.


### 3.4. Selection

Without evidence of selection, parallel speciation cases can tell us nothing about ecology’s role in speciation. Because of this, we searched for evidence of the adaptive mechanism(s) underlying parallel isolation. For strong evidence, we include reciprocal transplants showing strong local adaptation, manipulative experiments relating adaptive traits to extrinsic fitness, and/or signatures of selective sweeps at loci underlying putatively adaptive traits. Similarly, reciprocal transplants showing weak local adaptation, manipulative experiments showing a weak relationship between traits and extrinsic fitness, or common garden experiments comparing QST to FST are deemed weak evidence. Finally, we consider correlations between novel traits and environments or habitats to be indirect evidence for the role of selection.


## 3.1. Independence

Parallel speciation requires that replicate lineages be phylogenetically independent, so that the “shared traits responsible for reproductive isolation evolved separately” [6]. Estimating phylogenetic independence can be difficult for recently diverged taxa because of inadequate resolution, hybridization and introgression, and deep coalescence. These issues are exacerbated when phylogenies are based on a small number of loci or if the loci employed have little phylogenetic information content (e.g., isozymes). Additionally, it is not strictly necessary for populations to be phylogenetically independent for reproductive barriers to evolve separately, if different genes, mutations, or genetic pathways are exploited by selection in populations that remain connected by gene flow.Therefore, in this survey, strong evidence for independent evolution includes: (1) phylogenetic analyses supporting independence with multiple, phylogenetically informative loci or (2) direct evidence that a shared isolating trait has evolved independently (e.g., the trait is a result of different mutations in different populations). Phylogenetic analyses with a single locus, or with loci having little information content, are deemed weak direct evidence. Note that we consider genetic information from completely linked markers (e.g., multiple genes sequenced from the chloroplast genome) as information from one locus. Finally, indirect evidence for independence could include the improbability of long-distance colonization or gene flow between geographically separated but ecologically similar habitats, or phenotypes that are similar but not identical suggesting different genetic bases.


## 3.2. Isolation

As with any test of incipient or recent speciation, reproductive isolation must have evolved between descendent and ancestral populations, though not necessarily to completion. For strong evidence of isolation, we require experimental evidence for strong reproductive barriers that are genetically based, such as substantial differences in flowering time or pollination syndrome in a common garden and/or F1 hybrid inviability or sterility. Experimentally demonstrated weak but statistically significant reproductive barriers between diverging populations (including selection against immigrants and hybrids), or genetic divergence between locally diverging populations despite the opportunity for gene flow, are considered weak evidence for isolation. We view systems with apparent immigrant or hybrid inviability (e.g., serpentine adaptation), long-term persistence of divergent populations in sympatry, or strong divergence in mating system as indirect evidence that barriers likely exist. Although we would not consider isolation that has no genetic basis as evidence for parallel ecological speciation, we acknowledge that phenotypic plasticity can facilitate or impede the evolution of reproductive barriers and is an important consideration for studies of ecological speciation [43] (e.g., [44]). Furthermore, because explicitly testing that isolation is genetically based was rare in our candidate studies, we only required the genetic basis of isolation to be confirmed for cases to have strong direct evidence.


## 3.3. Compatibility

As we briefly discuss above, the lack of reproductive barriers between descendent populations is a key criterion distinguishing true parallel ecological speciation from other forms of replicated ecological speciation (Figure1). For strong evidence of reproductive compatibility we require that descendent populations show little or no barriers to reproduction when experimentally crossed and minimal ecological divergence as demonstrated by reciprocal transplant or manipulative ecological experiments. If only one of these two components of compatibility were demonstrated, we consider the evidence to be weak. We also consider substantial genetic analysis showing little genetic differentiation at neutral markers between the descendent populations to be weak direct evidence for compatibility, although this might weaken the case for the criterion of independence. Lastly, if the evolution of environmental specificity or mating system is such that descendant populations are indistinguishable in these parallel traits and have no other phenotypic differences, we consider this indirect evidence for compatibility.It is difficult to ascertain the strength of evidence for isolation and compatibility when multiple independent origins of self-fertilization (autogamy) have occurred. This is because replicate populations of selfers are likely to be as strongly isolated from one another as they are from the ancestral outcrossing populations. For this reason, replicated selfing lineages were excluded from consideration unless accompanied by the evolution of other reproductive barriers.


## 3.4. Selection

Without evidence of selection, parallel speciation cases can tell us nothing about ecology’s role in speciation. Because of this, we searched for evidence of the adaptive mechanism(s) underlying parallel isolation. For strong evidence, we include reciprocal transplants showing strong local adaptation, manipulative experiments relating adaptive traits to extrinsic fitness, and/or signatures of selective sweeps at loci underlying putatively adaptive traits. Similarly, reciprocal transplants showing weak local adaptation, manipulative experiments showing a weak relationship between traits and extrinsic fitness, or common garden experiments comparing QST to FST are deemed weak evidence. Finally, we consider correlations between novel traits and environments or habitats to be indirect evidence for the role of selection.


## 4. Results of the Survey

The most striking result of this survey is that very few plant cases have strong evidence for two or more criteria of parallel ecological speciation, and most have only weak or indirect evidence for any of the criteria (Table1; Appendix A). Only 3 of the 15 examples discussed by Levin [12] meet our minimum requirements for inclusion in the table. We did identify 8 new candidate systems. These were Cerastium alpinum, Eucalyptus globulus, Geonoma macrostachys, Hemerocallis citrina var. vespertina, Lasthenia californica, Petunia axillaris, Schizanthus grahamii,andStreptanthus glandulosus. Some of the new candidate systems are quite promising, but none have strong evidence for all criteria. These cases and a review of Levin’s [12] examples are summarized in Table 1 and Appendix A. The animal cases used as a comparison are summarized in Table 2 and Appendix B. Although few of the animal cases have strong evidence for all the criteria either, these well-studied animal systems are more strongly supported than the plant examples.Table 1
Candidate examples of parallel ecological speciation in plants showing the strength of evidence for each case. The details of each example can be found in AppendixA. The strength of evidence for each case was coded as follows: ***: strong direct evidence, **: weak direct evidence, *: indirect evidence, —: no evidence, †: evidence against, and NA: no data.
SpeciesMin. number of originsIndependenceIsolationCompatibilitySelectionMajor parallel trait(s)ReferencesAlopecurus myosuroidesLXMany**NANA***Herbicide tolerance[45–51]Agrostis capillariesLXMany*****Edaphic tolerance[52–54]Agrostis stoloniferaLXNANA****Edaphic tolerance[55–57]Agrostis tenuisLNA***NA**Edaphic tolerance[58, 59]Armeria maritimaLXNA***†**Edaphic tolerance[60–63]Chaenactis spp.LX2***†***Flower colour[64, 65]Cerastium alpinum2***NA***Edaphic tolerance[66]Chenopodium albumLXNA*NANA*Herbicide Tolerance[67–70]Crepis tectorumLX2**NANA**Leaf morphology[71, 72]Deschampsia caespitosaL2*****Edaphic tolerance[73, 74]Eucalyptus globulus3*******Dwarfed morphology[75]Geonoma macrostachys3******Habitat type; reproductive strategy[76–78]Hemerocallis citrina var. vespertina3****NANocturnal flowering[79]Hieracium umbellatumLXNA****Habitat type (dunes)[80]Lasthenia californica2*********Edaphic tolerance[81–87]Microseris lanceolataL2*******Habitat type (elevation)[88–90]Petunia axillaris6******—Flower colour[91, 92]Plantago maritimaLX2*NANANASpike morphology[93]Poa annuaLXNA*—**Herbicide tolerance[94, 95]Schizanthus grahamii2****NA*Pollination syndrome, self-compatibility[96]Silene dioicaLXNA**NANA—Edaphic tolerance[97, 98]Silene vulgarisLX2**NA***Edaphic tolerance[99–102]Streptanthus glandulosusMany******Edaphic tolerance[103–107]L: Levin example.X: Example that would not have been included in this table had they not been reviewed in Levin [12].Table 2
Examples of parallel ecological speciation in animals showing the strength of evidence for each case. This list is not exhaustive and instead is a selection of well-studied cases serving as a comparison to the plant examples. The strength of evidence for each case was coded as follows: ***: strong direct evidence, **: weak direct evidence, *: indirect evidence, —: no evidence, †: evidence against, and NA: no data.
SpeciesMin. number of originsIndependenceIsolationCompatibilitySelectionMajor parallel trait(s)ReferencesAstyanax cave fishes2**********Pigmentation, eye functionality[27]Coregonus clupeaformis6*********Body size and shape, foraging niche[13, 108–115]Coregonus lavaretus3********Body size and shape, foraging niche[14, 115–117]Gasterosteus aculeatus benthic/limnetic5*********Body size and shape, foraging niche[3, 15, 16, 23, 24, 118–122]Gasterosteus aculeatus lake/stream6********Body size and shape, foraging niche[3, 23, 123–130]Gasterosteus aculeatus anadromous/stream residentmany**********Body size and shape, life history[3, 17, 23, 131–133]Littorina saxatilis-Galician Spain3**********Shell size and shape, microhabitat adaptation[18, 19, 134–141]Timema cristinaeNA*********Color pattern, host plant adaptation[20, 142–144]Many of the putative plant cases lack evidence of compatibility among independent parallel populations. In fact, none of the examples have strong evidence for compatibility. This is unfortunate given the effectiveness of this criterion for demonstrating that ecological selection was the main cause of reproductive isolation in these systems—the primary reason for studying parallel ecological speciation in the first place. Hopefully, future studies in these systems will test for evidence of compatibility between suspected examples of parallel species. On the other hand, the criterion with the most evidence is the independent evolution of lineages that appear to be diverging in parallel. This is unsurprising given the widespread application of molecular phylogenetic methods in plants.One of the best candidates of parallel ecological speciation in plants to date isEucalyptus globulus [75] (Appendix A). In this case, three populations of E. globulus that inhabit granite headlands have a dwarfed morphology. Data from several nuclear and chloroplast markers show that each of the dwarfed populations is more closely related to its nearest tall population than to other dwarfed populations. Furthermore, there are two lines of evidence for isolation. First, the dwarfed populations flower earlier than the tall populations. Second, there is no evidence of pollen flow from the tall populations to the dwarfed populations despite a thorough examination of variation at microsatellite loci. However, the genetic basis of isolation, compatibility among dwarfed populations, and the selective advantage of being dwarfed still need to be confirmed in this example.Other promising cases includeLasthenia californica[81] (Appendix A) andSchizanthus grahamii[96] (Appendix A). Lasthenia californicahas strong evidence for parallel evolution of two races that have different flavonoid pigments and are found in different edaphic environments using phylogenetic analyses of ribosomal and chloroplast sequence and allozyme variation [81–84]. Race A is more tolerant of Na+ and Mg2+ and race C flowers earlier and produced more seed heads under drought conditions [85, 86]. However, isolation and compatibility between and within the races need to be confirmed. Conversely, there are clear reproductive barriers between Schizanthus grahamiiand Schizanthus hookerias they have different primary pollinators and experimental interspecific crosses produced no seeds [96]. However, it is not certain that these barriers arose multiple times independently because only chloroplast sequence data has been analyzed.There are a few commonalities among the candidate examples. In many of the candidate systems ancestral and descendent forms have evolved particular edaphic tolerances and/or specific changes in reproductive phenotype or mating system. Under divergent ecological selection, these traits are likely to make ecological speciation relatively easier because they can cause assortative mating as a byproduct of divergent selection.


## 5. Why Is Parallel Ecological Speciation Seemingly Rare in Plants?

### 5.1. Lack of Data

The lack of strong examples of parallel ecological speciation in plants is probably because botanists typically do not do the necessary tests. Perhaps this is because botanists have never doubted the importance of ecology in speciation [1, 7, 9] or because other methods of inference have been successful. However, we believe that it is useful to examine parallel ecological speciation explicitly in plants given how fruitful such studies have been in animals. In the present paper, this has allowed us to not only identify the key information that is missing in most potential case studies of parallel ecological speciation in plants, but also to recommend the experimental tests that are likely to be most profitable. For example, immigrant inviability is likely an important barrier in cases of parallel ecological speciation in plants. Therefore, reciprocal transplants between the new habitat types (as a test of isolation) and among sites in a single habitat type (as a test of compatibility) are crucial. A second essential set of tests that should be conducted is crosses between ancestral and descendent populations and crosses among populations in each habitat. It is surprising that these data are lacking given that both an explicit framework for studying parallel ecological speciation [6] and a list of possible cases [12] have been available for many years.Furthermore, the signature of parallel speciation is easily lost. For example, if gene flow occurs between independently derived populations, the signals of phylogenetic independence may be lost. Conversely, if descendent lineages are geographically isolated (i.e., allopatric) but otherwise reproductively compatible, they will likely eventually evolve reproductive isolation from one another even if they were not originally isolated. Thus, the window of time in which parallel speciation can be detected may be relatively narrow. Interestingly, some of the strongest animal cases (Littorina, threespine stickleback, and whitefish) are no more than 40,000 years old (postglacial) [23, 108], and some are thought to be as young as 10,000 years [19]. However, we see no reason why this window would be narrower in plants than animals. Thus, while the narrow window of detectability may account for the overall paucity of convincing examples of parallel ecological speciation in either the plant or animal kingdoms, it cannot explain why there are fewer examples in plants than in animals.


### 5.2. Plants Are Different

It is also possible that parallel ecological speciation is truly rare in plants. Considerable work would need to be done to validate this conjecture. However, should this pattern exist, there are several potential explanations. First, it is possible that the types of habitat distributions that promote parallel speciation in animals are more rare for plant populations. Many but not all of the animal examples involve adaptation to systems such as lakes or streams which are common, offer geographical isolation, and provide relatively homogeneous ecological environments. Perhaps these kinds of ecological opportunities are less frequent for plants? We think this explanation unlikely given that patchy environments (especially edaphic environments) are common in terrestrial ecosystems and parallel adaptation into those habitats occurs frequently.It is also possible that plants have certain characteristics that make parallel ecological speciation unlikely or lack characteristics that promote parallel ecological speciation. This potential difference between plants and animals may be in part because behavior is not particularly relevant to plants. Behavior, especially behaviorally based mate preference, may be an important component of parallel ecological speciation in animal systems (though pollinator behavior in flowering plants may act analogously). Perhaps plants have no trait equivalent to body size in animals, which can act as a “magic trait” [145] to serve in both assortative mating and ecological adaptation. However, flowering time could be such a trait, and there are many examples of flowering time changing in new edaphic environments (e.g., Lord Howe Island palms [146]). On the other hand, flowering time may be quite constrained because partitioning flowering time requires narrower windows of flowering, which can have strong negative fitness consequences. Other potential traits are floral morphology and edaphic tolerances. Floral morphology may adapt to attract different pollinators and, consequently, lead to pollinator isolation. Similarly, the evolution of edaphic tolerance often leads to selection against immigrants.The lack of evidence for parallel ecological speciation in plants is a mystery that may represent a key to understanding how species arise in plants. If parallel ecological speciation is more common than our survey suggests, then we can bolster existing evidence that ecology plays an important role in plant speciation. On the other hand, if parallel ecological speciation is determined to be rare, we can conclude that speciation may be less repeatable and more complicated than sometimes believed. We do not intend to imply that ecological speciation does not happen in plants. In fact, we believe it to be common. However, evidence of parallel ecological speciation in plants is not yet as convincing as it is for animal examples. We hope our study will spur additional investigation of the promising systems identified here, as well as provide guidance regarding the kinds of studies that should be performed in each system.


## 5.1. Lack of Data

The lack of strong examples of parallel ecological speciation in plants is probably because botanists typically do not do the necessary tests. Perhaps this is because botanists have never doubted the importance of ecology in speciation [1, 7, 9] or because other methods of inference have been successful. However, we believe that it is useful to examine parallel ecological speciation explicitly in plants given how fruitful such studies have been in animals. In the present paper, this has allowed us to not only identify the key information that is missing in most potential case studies of parallel ecological speciation in plants, but also to recommend the experimental tests that are likely to be most profitable. For example, immigrant inviability is likely an important barrier in cases of parallel ecological speciation in plants. Therefore, reciprocal transplants between the new habitat types (as a test of isolation) and among sites in a single habitat type (as a test of compatibility) are crucial. A second essential set of tests that should be conducted is crosses between ancestral and descendent populations and crosses among populations in each habitat. It is surprising that these data are lacking given that both an explicit framework for studying parallel ecological speciation [6] and a list of possible cases [12] have been available for many years.Furthermore, the signature of parallel speciation is easily lost. For example, if gene flow occurs between independently derived populations, the signals of phylogenetic independence may be lost. Conversely, if descendent lineages are geographically isolated (i.e., allopatric) but otherwise reproductively compatible, they will likely eventually evolve reproductive isolation from one another even if they were not originally isolated. Thus, the window of time in which parallel speciation can be detected may be relatively narrow. Interestingly, some of the strongest animal cases (Littorina, threespine stickleback, and whitefish) are no more than 40,000 years old (postglacial) [23, 108], and some are thought to be as young as 10,000 years [19]. However, we see no reason why this window would be narrower in plants than animals. Thus, while the narrow window of detectability may account for the overall paucity of convincing examples of parallel ecological speciation in either the plant or animal kingdoms, it cannot explain why there are fewer examples in plants than in animals.


## 5.2. Plants Are Different

It is also possible that parallel ecological speciation is truly rare in plants. Considerable work would need to be done to validate this conjecture. However, should this pattern exist, there are several potential explanations. First, it is possible that the types of habitat distributions that promote parallel speciation in animals are more rare for plant populations. Many but not all of the animal examples involve adaptation to systems such as lakes or streams which are common, offer geographical isolation, and provide relatively homogeneous ecological environments. Perhaps these kinds of ecological opportunities are less frequent for plants? We think this explanation unlikely given that patchy environments (especially edaphic environments) are common in terrestrial ecosystems and parallel adaptation into those habitats occurs frequently.It is also possible that plants have certain characteristics that make parallel ecological speciation unlikely or lack characteristics that promote parallel ecological speciation. This potential difference between plants and animals may be in part because behavior is not particularly relevant to plants. Behavior, especially behaviorally based mate preference, may be an important component of parallel ecological speciation in animal systems (though pollinator behavior in flowering plants may act analogously). Perhaps plants have no trait equivalent to body size in animals, which can act as a “magic trait” [145] to serve in both assortative mating and ecological adaptation. However, flowering time could be such a trait, and there are many examples of flowering time changing in new edaphic environments (e.g., Lord Howe Island palms [146]). On the other hand, flowering time may be quite constrained because partitioning flowering time requires narrower windows of flowering, which can have strong negative fitness consequences. Other potential traits are floral morphology and edaphic tolerances. Floral morphology may adapt to attract different pollinators and, consequently, lead to pollinator isolation. Similarly, the evolution of edaphic tolerance often leads to selection against immigrants.The lack of evidence for parallel ecological speciation in plants is a mystery that may represent a key to understanding how species arise in plants. If parallel ecological speciation is more common than our survey suggests, then we can bolster existing evidence that ecology plays an important role in plant speciation. On the other hand, if parallel ecological speciation is determined to be rare, we can conclude that speciation may be less repeatable and more complicated than sometimes believed. We do not intend to imply that ecological speciation does not happen in plants. In fact, we believe it to be common. However, evidence of parallel ecological speciation in plants is not yet as convincing as it is for animal examples. We hope our study will spur additional investigation of the promising systems identified here, as well as provide guidance regarding the kinds of studies that should be performed in each system.



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*Source: 939862-2012-04-10.xml*