A Phylogenetic Framework for the Evolution of Female Polymorphism in Anoles

Biological Journal of the Linnean Society, 2011, 104, 303–317. With 3 ﬁgures

A phylogenetic framework for the evolution of female polymorphism in anoles

EVI A. D. PAEMELAERE1*, CRAIG GUYER1 and F. STEPHEN DOBSON1,2

1Department of Biological Sciences, 331 Funchess Hall, Auburn University, Auburn, AL 36849, USA 2Centre d’Ecologie Fonctionnelle et Evolutive, UMR CNRS 5175, 1919 route de Mende, 34293 Montpellier Cedex 5, France

Received 10 January 2011; revised 19 May 2011; accepted for publication 19 May 2011bij_1742 303..317

Female pattern polymorphisms (FPP) are striking, poorly understood, and a major challenge to evolutionary theory. We examined the evolution of FPP in anoline lizards in a phylogenetic context. Accordingly, we used comparative analyses that traced the evolution of female pattern polymorphism over historical time, and overlaid the historical pattern on the biogeographical distribution of current species. Comparative analyses used a maximum likelihood approach with variable rates of trait evolution. We found that, among almost 180 well-described species, 52 exhibited FPP and most of these occurred on the Central American mainland. Pagel’s l=0.644 indicated not only a moderately strong phylogenetic signal in FPP among 162 species with sound estimates of phylogeny, but also independent evolution. Their common ancestor was not polymorphic (0.003% likelihood of FPP), and there were at least 28 gains or losses of FPP during phylogenetic history. The geographical distribution of FPP indicates that, in the Caribbean islands, it has been present for almost 20 million years, and that parallel evolution of FPP has taken place during that time, including independent evolution on Cuba, Hispaniola, and Puerto Rico. Evidence of parallel evolution of FPP in anoles was fairly strong. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 303–317.

ADDITIONAL KEYWORDS: analysis – anolis – comparative studies – dorsal patterns – lizards – neotropics – polychrotidae.

INTRODUCTION remained understudied. In recent years, the number of attempts to better understand female polymor- The incidence of multiple morphs within a population phism has increased noticeably (Stamps & Gon, 1983; (i.e. polymorphism) has inspired hypotheses about its Svensson et al., 2009). evolution ever since early explorations into evolution- Female polymorphism has been documented mostly ary biology (Darwin, 1859; Darwin, 1871). Variation for species of Lepidoptera (butterflies) and Odonata in morphological characters such as size or colour (damselflies and dragonflies) and rarely in verte- between males and females (sexual dimorphism) and brates (Tillyard, 1917; Fisher & Ford, 1929; Richards, among males led to sexual selection theory (Darwin, 1961; Wickler, 1968; Schoener & Schoener, 1976). 1871), and both have been thoroughly investigated in Although polymorphism has been described for other a wide variety of organisms (Shine, 1979; Andersson species, only a few of these have been subjected to & Iwasa, 1996; Sinervo & Lively, 1996; Houde, 1997; research on its occurrence. Multiple selective pres- Shuster & Wade, 2003; Pradhan & Van Schaik, 2009). sures may interact to maintain polymorphism that is Research on polymorphism among females has con- limited to females (Joron & Mallet, 1998; Sirot et al., centrated mostly on insects, although it has generally 2003). Female colour morphs in damselflies, for example, are considered to exert alternative techniques to balance predation and male harassment. *Corresponding author. E-mail: [email protected] Despite intensive field studies and molecular

© 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 303–317 303 304 E. A. D. PAEMELAERE ET AL. research, especially in Odonata, female polymorphism Mattern, 2008). In this case, the reason for origina- remains poorly understood (Andres, Sanchez-Guillen tion and for maintenance of the trait each require & Rivera, 2000; Svensson et al., 2009). different explanations and both are important to our Unexpectedly, most research has focused on single understanding of polymorphism. In Papilio swallow- species. Although such contributions are valuable tail butterflies, however, female polymorphism is a for our understanding of how female polymorphism derived character that evolved repeatedly (Kunte, is maintained, they usually do not address the 2009). Such macro-evolutionary studies require a question of origination. By contrast, macro- thoroughly examined group of organisms for which evolutionary approaches examine species character- phylogenetic relationships are well known. For female istics in light of their evolutionary history and polymorphism, particularly in vertebrates, such lin- consider the possibility that current characteristics eages have rarely been described. Yet, they could may have resulted from historical events, rather serve as model systems. than as current adaptations (Dobson, 1985). When a Anoles (Squamata: Polychrotidae) are a good character is shared between sister taxa, the most model system for female polymorphism because parsimonious explanation is that the trait was female variation in dorsal patterns is easily observ- retained after origination in their common ancestor. able, and patterns are known to be heritable (Cals- Thus, the trait may have evolved in an ancestral beek, Bonneaud & Smith, 2008). Females generally environment, which may differ from the current show two or three variations in mid-dorsal patterns environment. Conversely, independent evolution of a within a population (e.g., Figure 1). Savage (2002) trait in distantly-related species suggests an adap- summarized female mid-dorsal patterns into five tive character of the trait if it coincides with occu- distinct morphs: mid-dorsal light stripe with or pation of similar environments (Harvey & Pagel, without dark border, diamonds, dark chevrons, and 1991; Larson & Losos, 1996; Schluter, 2000). In this dark X marks. The patterns are already clearly case, the shared character may have evolved from expressed in juveniles and are consistent throughout different ancestral states (convergent evolution), or life. The same patterns are found across species. from the same ancestral state (parallel evolution) (Harvey & Pagel, 1991; Zhang & Kumar, 1997). In either case, adaptation can be addressed by relating the shared trait to current environmental variables. Phylogenetic approaches thus provide direction for future research and indicate a possible limitation of population-based studies (Grandcolas & D’Haese, 2003). Analogous to effects of shared ancestry, geographical distribution can promote or constrain evolutionary change. Wiens et al. (2009) emphasized the importance of a geographical context for a phylogenetic analyses. Geographical isolation is considered to stimulate convergent evolution when the different locations contain similar environments (Simpson, 1953). Furthermore, an environment could become saturated with species sharing a common trait. In this case, geographical isolation could further stimulate parallel evolution through release from this saturated environment into a similar, nonsaturated one, where the same trait can then evolve. The end result is that more species could share a particular adaptation (Wiens et al., 2009). A geographical perspective on a phylogenetic analysis of a recurring trait results in the evolutionary perspective required before further examination of the processes resulting in the evolution and maintenance Figure 1. Examples of dorsal pattern variations in of a trait. anoles. The patterns shown are seen in females within a A study of the phylogenetic context of female population of Anolis humilis at La Selva Biological polymorphism in damselflies suggested that it Station, Costa Rica. From left to right: mid-dorsal stripe was the ancestral state in two genera (Van Gossum & with dark border, blotches, and dark chevrons.

With almost 400 species and recent advances in Williams, 1988; Stejneger, 1900; Schwartz & Hender- research of their phylogenetic history, anoles lend son, 1991; Avila-Pires, 1995; Lee, 1996; Vitt & de la themselves well to macro-evolutionary approaches Torre, 1996; Campbell, 1998; Rivero, 1998; Lee, 2000; for studying female polymorphism. Anoles comprise Stafford & Meyer, 2000; Garrido & Hedges, 2001; an excellent model system for the study of ecology, Nicholson et al., 2001; Savage, 2002; Duellman, 2005; evolution, and behaviour (Losos, 1992a, 1994; van Buurt, 2005). This allowed only species-level Beuttell & Losos, 1999). The presence of female assessments, so that species were scored positive for polymorphism in anoles, however, has received sur- female polymorphism, even if some populations prisingly little attention, although its presence is lacked this. The presence or absence of dorsal pattern commonly known (Fitch, 1975; Stamps & Gon, 1983; polymorphism was based on the vertebral zone alone. Savage, 2002). A relationship between morph and Geographical variation, subspecies variation, and perch use was demonstrated in Anolis sagrei and variation as a result of metachromatism (i.e. colour Anolis polylepis (Schoener & Schoener, 1976; change) were not considered as polymorphism for the Steffen, 2010). Furthermore, effects of density on purpose of the present study. Data are available in variation in immunocompetence and frequency- the online supporting information, Appendix S1. dependent selection, although not reproductive strategy, may explain female pattern polymorphism in A. sagrei (Calsbeek et al., 2008; Calsbeek, Bonvini NOMENCLATURE & Cox, 2010; Cox & Calsbeek, 2011). Differences There are almost 400 species of anoles and, despite between morphs found thus far have focused on extensive research on their evolutionary history, some mechanisms of maintenance of female polymorphism phylogenetic relationships and the related nomencla- without considering its evolutionary origin. ture remain ambiguous. Recent phylogenies indicate Because anoles are a good model for the study of that there are several rather well-established clades female polymorphism, we examined the evolution of within anoles, even though the relationship among the presence of female dorsal pattern polymorphism some of these major clades remains unclear (Jackman (FPP) across species. In particular, we tested whether et al., 1999; Poe, 2004; Nicholson et al., 2005), and a FPP is a derived character and has evolved indepen- more practical nomenclature system eventually may dently among anoles. We also incorporated a geo- result. Because, in the present study, the use of one graphical perspective to investigate whether isolation genus name for so many species is impractical and could have contributed to the current distribution of many clades are rather stable entities, we refer FPP among species. to monophyletic clades and series within clades (Table 1). We still use Anolis as the genus name to avoid any confusion with future names that are likely MATERIAL AND METHODS to arise. DATA Species descriptions were used to determine the presence or absence of pattern polymorphism in females PHYLOGENY (Lazell, 1972; Fitch, 1975; Rand, Gorman & Rand, No single phylogeny for all anole species was avail- 1975; Duellman, 1978; Dixon & Soini, 1986; Ayala & able. Therefore, we combined recent phylogenies,

Table 1. Nomenclature applied for clades within Anolis

Clade name Node number (Poe, 2004) Series

Norops = Beta anoles 286 Cuba: sagrei series (node: 225 ) (Etheridge, 1960) Jamaica: grahami series (node: 284) Cybotes 293 Ctenonotus 216 Northern Lesser Antilles: bimaculatus series Greater Antilles: cristatellus series. Carolinensis 309 Chamaelinorops 197 Xiphosurus 190 Equestris 324 Dactyloa 352 Southern Lesser Antilles: roquet series (node: 351)

Node numbers of the phylogeny of Poe (2004) are included to indicate the speciﬁc clade on the tree.

© 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 303–317 306 E. A. D. PAEMELAERE ET AL. sensu Nicholson et al. (2005), with species added from values for the ARD model were plotted onto the Poe (2004). The latter phylogeny was also used to phylogenetic tree to visualize the chance of FPP being resolve remaining polytomies. Species synonyms were at every node. checked using the Reptile Database (Uetz et al., Finally, we tested for phylogenetic signal using 2007). The major differences between the phylogenies Pagel’s lambda (Pagel, 1999). This compares the dis- we used were the placement of the Cybotes series and tribution of a trait among taxa between a star phy- placement of some species within the mainland beta logeny (l = 0; i.e. all phylogenetic structure removed) anoles. None of the variation between the phylog- and a given phylogenetic structure (l = 1; i.e. all enies, however, affected our major conclusions. branch lengths maintained). Lambda thus varies between zero and one, and a higher value indicates a stronger covariance between the phylogeny and the CHARACTER EVOLUTION AND PHYLOGENETIC SIGNAL distribution of the trait. To determine whether To study character evolution, we applied two different lambda is significantly different from zero, a ML ratio methods: parsimony and maximum likelihood (ML). test was used in R (Yang, 2006; Harmon et al., 2008). The benefits and critiques on these techniques were reviewed in detail by Cunningham, Omland & Oakley (1998) and Cunningham (1999). Parsimony recon- GEOGRAPHICAL DISTRIBUTION struction fails to recognize rapid evolution of a trait, For the geographical distribution of FPP, all island and parsimony is not reliable for unequal rates of species were considered, even when phylogenetic evolution between loss and gain of a trait. These relationships were unresolved. Because many main- issues are largely overcome by ML methods (Schluter land species remain poorly known, only the species et al., 1997). A drawback of ML is its dependence on for which detailed descriptions were available were branch lengths, which may differ depending on which included for the mainland. To assess geographical of several standard transformations are applied. distribution of female polymorphism in anoles, we These transformations are used when accurate esti- used species distribution maps and presence/absence mates of branch lengths are lacking. Interestingly, data of FPP at the species level. This ignores the ML does not necessarily favour the most parsimoni- possible absence of FPP in certain locations of a ous path of character evolution, although, when the species’ distribution. To test hypotheses related to number of character changes is limited, parsimony the distribution of FPP, a more in-depth study of and ML methods generally result in similar recon- presence or absence of FPP per population will be structions (Pagel, 1999). required. Species distributions were included in the Because ML approaches (see below) are sensitive to phylogeny to provide a geographical perspective on branch length, this analysis was run with equal the phylogenetic analysis. Some species, however, branch lengths, as well as Grafen’s (1989) arbitrary were not included in any available phylogeny and transformation of branch lengths. The major conclu- could only be incorporated for the geographical dis- sions, however, remained unaltered, regardless of the tribution of FPP. branch length transformation applied. Only the results for equal branch lengths are presented because of its slightly more conservative approach RESULTS and because many studies apply this transformation, For 179 species of anoles, a detailed description of including evolutionary studies on anoles (Ord & dorsal pattern was found. Slightly over 75% were Martins, 2006; Poe, Goheen & Hulebak, 2007). island anoles. Of these species, 52 (approximately Unordered parsimony analysis was performed in 30%) were described as having FPP. The majority of MESQUITE (Maddison & Maddison, 2008). This the species with female polymorphism were mainland assumes equal rates of forward and backward evolu- species, even though island species constituted the tion. ML estimates were obtained with the ‘geiger’ larger part in the dataset. Not all species for which package in R, version 2.8.1 (Harmon et al., 2008). colour patterns have been described were included in First, we compared an equal-rates (ER) model of the phylogenies that we used. Therefore, the number evolution, as used in parsimony, with an all-rates- of species available for our phylogenetic analysis was different (ARD) model and found that the ARD model 162. fit the data slightly better [–log likelihoodER =-87.47;

–log likelihoodARD =-85.07; P = 0.0286; Akiake infor- PHYLOGENETIC SIGNAL mation criteria (AIC)ER = 177, AICARD = 174]. Particu- larly, forward evolution was found to be We found a signiﬁcant phylogenetic signal in the approximately two times faster than backward evo- presence of FPP among anoles (log likelihood phylog- lution (gain: 0.227 ± 0.05; loss: 0.097 ± 0.02). ML eny =-81.89; log likelihood unstructured =-90.61;

P < 0.0001). The lambda value under the ARD model least one species with FPP. Overall, parsimony analy- was 0.644. Because lambda varies between zero and sis indicated the independent evolution of FPP across one, our value indicates a moderately strong phylo- clades. However, FPP was also found in closely- genetic signal. related species, signifying that FPP likely arose in their ancestor. This was the case for island Dactyloa (Fig. 2E; loss of FPP in Anolis bonairensis). In CHARACTER EVOLUTION the remaining groups that had multiple species with Parsimony analysis FPP, including mainland Norops, Cybotes, and Parsimony analysis indicated that the ancestral state the Ctenonotus clades, alternative hypotheses on was absence of FPP (Fig. 2E). For the 162 species number of gains versus losses were possible, based on included, the evolutionary pattern of FPP required a parsimony. minimum of 28 steps. The entire Carolinensis clade Within the Norops clade, few data were available lacked FPP (Fig. 2C). Three other members of this for species endemic to Mexico, which form the basal group, which have never appeared in a published radiation for mainland Norops. Therefore, FPP could phylogenetic tree, lacked FPP. All other clades had at have arisen in an ancestor of all mainland species or

Figure 2. Evolution of female pattern polymorphism (FPP) in Anolis. A, Norops clade. B, Cybotes and Ctenonotus clades. C, Carolinensis clade. D, Chamaelinorops, Xiphosurus, and Equestris clades. E, Dactyloa clade. Presence of FPP is indicated with grey dots. Pie diagrams from the maximum likelihood analysis are shown for ancestors, with the proportion of black representing the likelihood of FPP being present in this ancestor. Species distributions are given after their name. Jam, Jamaica; Cay, Cayman Islands; GA, Greater Antilles; LA, Lesser Antilles (minus VI); MEX, Mexico; PR, Puerto Rico; NCAM, North Central America; CAM, Central America; SAM, South America; VI, Virgin Islands. The possible number of gains and losses in parsimony analysis is shown as ‘gains : losses’.

Figure 2. Continued in the ancestor of the mainland species ranging south reversal in Anolis desechensis (Fig. 2B). All species of of Mexico (Fig. 2A). In either case, the trait was lost the bimaculatus series could have evolved FPP inde- in Anolis lionotus, Anolis notopholis, Anolis pendently, with the exception of the ancestor of Anolis townsendi, Anolis lineatus, and the ancestor of A. uni- marmoratus and Anolis sabanus. There were three formis, as well as its sister species, in which a rever- equally parsimonious scenarios with FPP evolving sal to FPP appeared in Anolis woodi. An alternative earlier in the clade and subsequent loss of this trait scenario described evolution of FPP after the split of (Fig. 2B). the branch leading to A. uniformis. In this case, the ancestor of Anolis nitens and its closely-related ML estimates species evolved FPP separately from the rest of the The ML analysis supported the majority of the par- mainland species. simony analysis (Fig. 2A, B, C, D, E). Importantly, In the Cybotes clade, FPP may have developed the ancestor of all anoles only had a 0.003% likeli- independently in Anolis whitemani, Anolis armouri, hood of FPP. Where the parsimony analysis indi- and Anolis cybotes or, alternatively, in an ancestor of cated that FPP and no FPP in an ancestor were these species, with losses in Anolis shrevei and Anolis equally parsimonious, the ML analysis generally haetianus (Fig. 2B). Within the cristatellus series of resulted in values near 50% likelihood. Similarly, the Ctenonotus clade, the alternatives were evolution the presence and absence of FPP in ancestors of FPP independently in Anolis cristatellus and Anolis based on parsimony mostly resulted in high and low ernestwilliamsi, or in the ancestor of these with a ML estimates, respectively. Some of the alternative

Figure 2. Continued scenarios, however, were resolved here and the When excluding A. bonairensis, this likelihood rose ancestor of the roquet series had a high ML for to 99.5%, which was consistent with the parsimony FPP, even though parsimony suggested later result. evolution of FPP. The ancestor of mainland Norops, with the exclu- sion of the Mexican radiation, showed 0.936% like- GEOGRAPHICAL DISTRIBUTION lihood for FPP. Therefore, the parsimony scenario of The overall geographical extent of FPP encompasses independent evolution of FPP in the clade of the vast majority of the geographical distribution A. nitens is less likely. Within the cristatellus series, of the anole radiation. Within this range, FPP is not the scenario for evolution in an ancestor of A. cris- uniformly distributed among major biogeographical tatellus and sister species was well supported (ML: areas (Fig. 3). The trait appears in ﬁve of six mono- 80.1%). Similarly, a 76.0% likelihood for the evolu- phyletic lineages of island anoles, although it is rare tion of FPP in the ancestor of the bimaculatus on Greater Antillean islands, and the small ancil- series supports ancestral evolution of FPP within lary islands throughout the Caribbean and Paciﬁc. the series, although the scenario with independent It is much more common on islands of the Upper evolution in A. wattsi was better supported (ML: and Lower Lesser Antilles and the mainland. For 90.4%). In the Cybotes clade, the best supported sce- the two major monophyletic lineages of mainland nario was ancestral evolution of FPP (ML: 84.8%). anoles, one (Dactyloa) lacks FPP on the mainland Finally, the ancestor of the roquet series, including but gains it in the single lineage that invades A. bonairensis, still had a 69.1% likelihood of FPP. islands. The other (Norops) has FPP on the main-

Figure 2. Continued land, although loss of FPP has occurred when these parallel evolution. Both parsimony and ML methods lizards invade islands, as seen for example in supported the absence of FPP in the common ancestor A. townsendi from Cocos Island and A. lineatus from of anoles and the consequent occurrence of multiple Curaçao. In at least one case, however, FPP was independent evolutionary events generating FPP retained (A. medemi, Gorgona). FPP is found on across the tree. Within this context, however, we islands as large as Cuba (109 886 km2) and as small document three independent cases (Norops, bimacu- as Saba (13 km2). On the smallest islands where latus, and roquet groups) in which the derived state of FPP was present, FPP did not result from indepen- FPP is largely retained by closely-related species, a dent evolution, although it did on Grand Cayman feature that explains why a phylogenetic signal was (196 km2). Therefore, island size does not appear to found. Nevertheless, we estimate that FPP arose constrain the evolution of FPP. independently at least 15 times, so that phylogenetic relationships alone could not explain the complete DISCUSSION distribution pattern of FPP, as indicated by the mod- erate value of lambda. PHYLOGENETIC PATTERNS IN THE EVOLUTION OF Similar to the independent evolution of FPP, we FPP IN ANOLES estimate the loss of FPP at least ﬁve times across the We investigated whether FPP was a derived character tree, both for clades of species for which loss of FPP in anoles and if it could have been the result of is a synapomorphy and for single species in which loss

Figure 2. Continued of FPP is an autopomorphy. Despite the much slower of evolutionary relationships in anoles are expected to rate of loss compared to gains, independent losses be minor (Nicholson et al., 2005). Last, current were seen in both island and mainland clades. Once descriptions of FPP are sufficiently numerous and lost, FPP was not regained, except in A. woodi.The sufficiently distributed widely across the phylogenetic possibility of regaining a trait once it has been tree to make it unlikely that the general patterns of lost remains controversial (Dollo, 1893; Simpson, our analysis will be modiﬁed by additional descrip- 1953; Cunningham, 1999), and our analysis suggests tions of colour patterns. that it is, at best, unusual for FFP within anoles. Most Caribbean anoles have detailed descriptions Any analysis based on evolutionary relationships of variations in dorsal patterns generated by multiple among species relies on the accuracy of the available authors. For the mainland, fewer species have been phylogeny and the number of species for which a described as completely. Nevertheless, mainland character of interest is known. Future changes in species of the Norops clade for which colour patterns phylogenetic inference could therefore affect the are known are sufficiently numerous to suggest that results reported in the present study. Nevertheless, our inference of FPP being present in the ancestor of we expect the main conclusions concerning the evo- this group is unlikely to be altered by description lution of female polymorphism in anoles to be robust of additional species. Similarly, colour descriptions of for several reasons. First, differences between recent mainland Dactyloa are distributed sufficiently widely phylogenies did not drastically affect the evolutionary across the phylogenetic tree for this group to make it path of female polymorphism, especially in the case of unlikely that future data will reject our conclusion ML estimates. Next, future changes to the hypothesis that this group is derived from an ancestor that

Figure 3. Geographical distribution of female polymorphism in anoles. The total number of species per location is given along with the proportion of polymorphic (endemic: black, non-endemic: dark grey), proportion of species for which the presence of polymorphism was unknown (hatched), and proportion of nonpolymorphic species (white). Lesser Antilles were divided into the northern ranging (N.) bimaculatus series and the southern (S.) ranging roquet series. The arrow indicates inclusion of the nonpolymorphic Anolis bonairensis in the Southern Lesser Antilles radiation. For the two radiations of mainland anoles, the proportion of polymorphic species is given relative to the number of species for which the presence of polymorphism was known. lacked FPP. Thus, evolutionary events that we for those ancestors provide an estimate for how long describe support multiple independent origins of FPP has been present in two of those clades. Within the FPP in anoles, suggesting a response to a common roquet group from the southern Lesser Antilles, the environment (Harvey & Pagel, 1991; Larson & Losos, deepest split is estimated to be between 15.5 and 1996; Schluter, 2000), which is a hypothesis that 17 Mya (Creer et al., 2001). The bimaculatus series remains to be tested. from the northern Lesser Antilles is estimated to have diverged between 7.9 and 9.7 Mya (Thorpe et al., 2008). Within this clade, the female polymorphic sister LOCATION AND TIMING OF THE EVOLUTION OF species A. marmoratus and A. sabanus are estimated FEMALE POLYMORPHISM to have diverged from their common ancestor approxi- The results of the present study show that FPP evolved mately 1.8–3.6 Mya (Stenson, Thorpe & Malhotra, in ancestors of three clades and divergence estimates 2004). These estimates are based on molecular clocks

© 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 303–317 FEMALE POLYMORPHISM IN ANOLES 313 and should be approached with caution (Crother & pattern of FPP indicates that similar processes Guyer, 1996; Bromham, 2002; Graur & Martin, 2004). shaped colour patterns of anoles. This isolation Nonetheless, the estimates indicate that FPP may yielded multiple relatively recent independent deri- have been present in Caribbean anoles for almost 20 vations of FFP for species on the Greater Antilles, and million years. Continued presence of polymorphism three older derivations retained by most descendent over such a long period of time is an indicator of the taxa within two clades of Lesser Antillean and one presence of stabilizing selection, because random pro- clade of mainland anoles. cesses or directional selection are expected to result in The evolutionary history of FPP on Cuba, Hispani- fixation (Nei & Li, 1975; Futuyma, 1998; Richman, ola, and Puerto Rico suggests that FPP was absent in 2000). Additionally, selection for FPP to arise likely the common ancestor of the clades that established on originated long ago, when the location of Caribbean these islands. Generally, FPP evolved here in species islands and habitat characteristics of those island are that diverged relatively recently compared to the first likely to have been quite different than today (Rough- establishment of each of the clades. The absence of garden, 1995; Iturralde-Vinent, 2006). FPP in founder populations could have resulted from loss of allelic variance in the founder population. Our analysis, however, suggests that FPP may not have GEOGRAPHICAL ISOLATION AND THE EVOLUTION OF been present in the source populations for these FEMALE POLYMORPHISM islands. Although we have no explanation for why The results of the present study indicate that once FPP should be so rare on these islands, we note that FFP evolves, it is unlikely for this characteristic to large island size and northerly location of these disappear. In those cases where this has happened, islands are obvious correlates that might explain a dispersal appears likely to have been important. To lack of selective pressures generating FPP. Addition- colonize novel areas, survival of a few individuals ally, the rarity of FPP resulting from independent from dispersal events would suffice. Female polymor- evolution supports the idea of parallel evolution in phism, on the other hand, probably requires multiple these lineages. alleles and this variation must be represented in the For mainland Norops and two groups of anoles on founder population for polymorphism to be main- the Lesser Antilles, FPP was likely maintained after tained. Consequently, a larger number of individuals it arose in an ancestor. All three clades appear to be would have had to reach the new location to maintain sufficiently old to have been geographically contigu- FPP in a colonizing population. Although such a sce- ous during the tectonic activities that developed the nario is not impossible, long distance dispersal would Aves Ridge (Roughgarden, 1995; Nicholson et al., likely lead to a small founder population and conse- 2005). Thus, these three clades might have generated quent loss of alleles (Gorman & Kim, 1976; Gorman, FPP from a common history associated with geo- Kim & Yang, 1978). This idea is supported by the graphical development of the southern islands. The absence of FPP on Cocos Island and Curaçao, which female polymorphic roquet radiation only occupies the are two islands that were populated by descendants southern islands up to Martinique. The islands from from mainland Norops in which FPP was found to be Dominica north to Anguilla are inhabited by the poly- common (Williams, 1969). morphic bimaculatus series, which are more closely The wide geographical distribution of anoles should related to Hispaniolan and Puerto Rican species, and provide abundant opportunities for parallel evolution reached the Lesser Antilles from the north (Gorman of FPP. Anoles inhabit almost all islands in the West & Atkins, 1969; Williams, 1969; Guyer & Savage, Indies, most of the Neotropical mainland, and a few 1986). In both clades, FPP evolved in an early ances- islands in the Pacific Ocean. This pattern of geo- tor. Overwater dispersal between islands must have graphical isolation is assumed to increase the number occurred here too, although we hypothesize that a of times a trait can evolve independently, if similar shorter migration distance could have increased the environments are encountered in the separate loca- chance for FPP to be maintained. A shorter distance tions (Simpson, 1953; Schluter, 2000; Wiens et al., might increase the chance for adults (rather than 2009). Moreover, anoles are known for rapid evolution eggs) to migrate and some variation is considered in response to their environment (Malhotra & Thorpe, to survive bottlenecks in anoles because females 1991; Losos et al., 2006b). Indeed, geographical dis- can store sperm of multiple males (Eales, Thorpe & tribution patterns of anoles have been used to explain Malhotra, 2008). A shorter migration distance would repeated evolution of some of their morphological also facilitate multiple migration events, which can characteristics in response to habitat use and compe- contribute to maintaining variation (Kolbe et al., tition (Rand & Williams, 1969; Williams, 1972; Losos, 2004, 2007, 2008). To test these ideas, however, his- 1992b; Losos et al., 1998, 2006a; Harmon et al., 2005). torical locations of the islands along with timing of The phylogenetic and geographical distribution speciation events are required.

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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Appendix S1. Presence of female pattern polymorphism (FPP) for species included in the phylogenetic analysis and geographical distribution. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.