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Julie Wiemerslage 11/14/2014 1 The Adaptive Radiation of Caribbean Anolis Lizards Introduction Adaptive radiation is the divergence of members of a single phylogenetic lineage into several different adaptive forms. This divergence is prompted by ecological opportunities that cause a species to adapt to fill new niche spaces, and such adaptations lead to new distinct species. This is a common phenomenon in island evolution. When a single species disperses onto different islands, adaptations to adjust to the different ecology of each island occur, and can ultimately lead to evolutionary divergence of a species. One of the most widely known examples of island evolution resulting from adaptive radiation is that of Darwin’s finches of the Galapagos Islands. They exhibit different morphologies than their ancestral state based on the island that they inhabit, as a result of adapting to different niches (Pinto 2008; Calsbeek 2010). This paper will address another proposed case of island radiation- the radiation of Anolis lizards in the Caribbean. It has recently been contended whether Anolis lizards in the Caribbean are specifically an example of an island radiation opposed to just a general radiation, but either way, they are certainly a strong example of replicated adaptive radiation. In fact, their fourfold replicated radiation on islands in the Caribbean is probably the best-documented example of replicated adaptive radiation that exists. Anoles have radiated for the most part independently on four different islands (Cuba, Hispaniola, Jamaica, and Puerto Rico), yet each radiation produced the same set of habitat specialists, termed ecomorphs (Losos 2010). Ecological opportunity prompts adaptive radiation Before getting in to more detail about Anolis radiations in the Caribbean, an overall understanding of adaptive radiation is useful. It is largely accepted that ecological opportunity Julie Wiemerslage 11/14/2014 2 prompts adaptive radiation. In general, these are resources that are accessible and little used by competing taxa. What might prompt the exposure to such resources? There are four basic circumstances thought to prompt ecological opportunity. First, the appearance of new resources provides ecological opportunity, such as a new food source emerging in a certain area. Second, the extinction of a species that previously used a resource will make that resource available to new species. That is why mass extinction events often lead to rapid diversification of surviving clades (Jablonski 2001). Third, the colonization of an area with resources that were not previously used provides ecological opportunity. For example, a lineage moving from a mainland to a remote island may gain many new resource niches to fill. And finally, the evolution of a trait that allows for the utilization of a resource in a way that was not previously possible will offer ecological opportunity. These are termed key innovations, and examples may be the evolution of wings in bats and of toe pads in geckos and anoles (Baum 1991). Thus, these circumstances are important factors that can lead to the adaptive radiation of species. However, ecological opportunity alone does not automatically mean that rapid divergences will occur. (Losos 2010). In the presence of ecological opportunity, some clades radiate and others do not. For instance, Hawaiian honeycreepers are an excellent example of adaptive radiation, with up to 50 different species, yet four other songbird lineages that successfully colonized the Hawaiian archipelago failed to undergo much diversification at all from their ancestral state (Lovette 2002). There are several reasons that a radiation may not occur despite the presence of ecological opportunity. For one, even in an open niche like a depauperate island, the correct resources for a particular organism might not be available. Additionally, some groups may not be capable of Julie Wiemerslage 11/14/2014 3 speciating despite ecological opportunity. For instance many species cannot diversify on islands that are under a particular size threshold, so even if ecological opportunities are present, they will not speciate on an island that is under that size threshold (Losos, 2000). There also may be a lack of ecological access as a result of another colonizing species taking up available resources and leaving little for subsequent arriving species (Losos 2010). Finally, some species may be less capable of evolving than others, and do not diversify even in the presence of ecological opportunity. Certain taxa are limited in their ability to evolve and will change very slowly or not at all, while those that can change quickly will adapt to local circumstances (Lovette 2002). Adaptive Radiation of Caribbean Anolis lizards: Morphology The genus Anolis is an enormous genera, with over 300 described species. 154 of these species occur on Caribbean islands. The anoles of the islands of the Greater Antilles (Cuba, Hispaniola, Jamaica, and Puerto Rico) are of specific interest. On each island there are a number of different species that are morphologically distinct, behave differently, and use a certain part of the structural habitat. The hypothesis that morphological differences between species are the result of adaptation to the functional demands imposed by inhabiting different parts of the environment has been supported through detailed functional and behavioral analyses (Irschick et al., 1996; Larson & Losos, 1996; Elstrott & Irschick, 2004). Interestingly, the same set of habitat specialists which are termed “ecomorphs” recur on each of the Greater Antilles islands, and are likely the result of convergent evolution (see figure 1). There are 6 ecomorphs, each named for their typical habitat, these are: trunk, trunk-crown, trunk-ground, grass-bush, twig, and crowngiant (Williams, 1972, 1983). Phylogenetic analyses of morphological and molecular data support that these ecomorphs are independently derived on each island. Furthermore, much Julie Wiemerslage 11/14/2014 4 species diversity of the Caribbean Anolis occurs within clades of ecomorphs and thus it is important to study multiple hierarchical evolutionary levels from clades to populations in order to get a more complete understanding of evolutionary diversification and radiation (Losos 2006). Figure 1: Convergent evolution of different Anolis ecomorph types on Cuba, Hispaniola, Jamaica, and Puerto Rico. (from Losos and Ricklefs 2009) Phylogenies for most of the Anolis species in the Caribbean have been produced via recent molecular studies. These phylogenies afford the ability to thoroughly examine their Julie Wiemerslage 11/14/2014 5 radiation. Three patterns of anole evolutionary diversification on the Greater Antilles can be drawn from these phylogenies. First, ecomorphs have generally only derived once on each island. Second, ecomorphs are almost never phylogenetically nested within other ecomorphs. They are monophyletic and do not give rise to other ecomorphs. And third, ecomorphs are very old. The clock-like evolution of the mtDNA region that was examined suggests evolutionary divergence of over 30 million years ago. Another molecular clock estimation based on divergence in albumin proteins indicates a similar estimate of about 35-40 million years for the divergence of Anolis. The fossil record also supports these dates because at least one ecomorph clade was present more than 20 million years ago- fossil amber anoles have been dated to at least the early Miocene. (Losos, 2006) Adaptive Radiation of Caribbean Anolis lizards: Behavior Convergent evolution is the independent origin of similar phenotypes in distantly related species (Ord 2013). The 6 ecomorphs of the Greater Antilles are an example of convergent evolution since they evolved independently on each island as a result of the same adaptive pressures. Many examples of convergent evolution in morphology have been studied, but fewer examples have been studied from animal behavior. However, the convergent evolution of territorial communication in Anolis lizards from Puerto Rico and Jamaica has recently been elucidated. Anoles communicate using movement-based visual displays composed of both vertical movements of the body, known as headbobs, and extensions of a part of their throat, called a dewlap. These displays are used by males to advertise territory occupancy and deter intrusions (Jenssen 1977; Ord 2008). Environmental degradation can affect anole displays because potential receivers of signals are located a far distance from the signaler, so displays are Julie Wiemerslage 11/14/2014 6 under significant selection pressure to be conspicuous (Ord 2012; Ord and Stamps 2008). In particular, lizards in poorly lit or windy environments, where windblown vegetation causes distracting motion, alter their speed of display movements or the duration of displays (Ord et al. 2007, 2010). Thus, light and visual noise conditions between islands have the potential to cause convergence in display characteristics among species living in similar conditions. Therefore, the extent to which components of a display are used in the same functional context offer a behavior that can be tested for evolutionary convergence in Anolis lizards. Researchers devised an index, called PSynch, to quantify the relationship between the dewlap and headbob components of an anole’s display. The index showed the proportion of synchronized dewlap and headbob movements. The term asynchronous was used to describe species that emphasized dewlapping in their displays, and synchronous referred to those that emphasized headbobbing. They then asked whether that index was correlated, across taxa, with other display characteristics. They mapped the display phenotypes onto the phylogeny of Jamaican and Puerto Rican lizards to confirm that convergence was involved for at least one of the display types. Results suggested that habitat light likely contributed to both the evolution of alternative signal strategies through the emphasis of different display characteristics on Jamaica and Puerto Rico (Ord et al. 2010, 2011; Ord 2012), and to convergent display phenotypes, through selection within islands on several display characteristics that have led to shared display types between islands (Ord. 2013). Caribbean Anolis lizards in the context of the model of adaptive radiation When convergence results from natural selection, it provides great evidence for adaptive evolution in nature since it represents replicated examples of the same adaptation arising from separate selection events. Anolis lizards show both morphological and behavioral convergent Julie Wiemerslage 11/14/2014 7 evolution on the Greater Antilles islands (Ord 2013). With this background regarding the Anolis lizards of the Caribbean, as well as an understanding of important trends in their phylogenies, we can now address the great diversification of the Anolis genus in the context of the model of adaptive radiation. It is widely accepted that the model of adaptive radiation is an effective explanation for the diversity in Anolis lizards of the Caribbean. This model posits that when a colonizing species finds itself in an ecologically depauperate land with few competitors or predators and many available resources, evolutionary divergence occurs as descendent species evolve to specialize on different portions of the resource spectrum (Pinto, 2008). In general, Anolis lizards fit the model of adaptive radiation because their diversification is very strongly correlated with differences in habitat use. So much, that species are grouped into classes based on associations between morphology and the habitat they are most often found in. The independent evolution of these ecomorphs on separate islands suggest consistent patterns of selection on key traits such as body size and relative limb length. These traits are acted on by selection because they are ecologically related to locomotor performance and fitness in different habitats. For instance, limb length differentially affects speed and agility on broad and narrow diameter vegetation, which contributes to efficiency of prey capture and territory defense. Additionally, differences in body size effect access to resources when it is determined by fighting ability. Body size may also relate to trophic and thermal resource partitioning, as well as susceptibility to predators (Calsbeek, 2010). Thus the relationships of morphology, performance and fitness drive the selection of various characteristics that lead to evolutionary divergence, and they are clearly linked to ecological factors. Julie Wiemerslage 11/14/2014 8 Furthermore, a corollary of the adaptive radiation model is that once one species specializes for a particular aspect of the environment, other lineages should have trouble occupying that niche. For Anolis lizards, this may explain why ecomorphs have had repeated evolution across islands but rarely have multiple evolution within an island. It appears that once an ecomorph evolves on an island, it is well specialized for the niche that it evolved to fill, and will certainly outcompete any other lineage that tries to enter that niche (Losos, 2006). Additionally, Anolis behavior is in line with the model for adaptive radiation, because it is also adapted for habitat use. Anolis lizards differentially use territory displays based on habitat, such as light (Ord 2013). The role of competition and predation in Anolis adaptive radiation This gives rise to the question- what are the agents of selection in shaping the adaptive landscape for a radiation? In general, competition and predation often drive adaptation. In the case of Anolis lizards, a review of many studies show that sympatric anole species interact strongly and the more similar species are ecologically, the stronger interactions are between them (Losos, 2006). This indicates that competition plays a large role in driving Anolis adaptation. One particular study actually created a field experiment that measured the relative importance of predation versus competition as agents of natural selection. In their paper titled, Experimentally testing the relative importance of predation and competition as agents of selection, Calsbeek and Cox analyzed the roles of predation and competition in driving adaptation. They manipulated entire island populations of brown anoles, Anolis sagrei and tested the effect of predation on adaptation by adjusting the presence of bird and snake predators across 6 different islands. They also tested the effect of competition on adaptation by adjusting the population density of Anolis Julie Wiemerslage 11/14/2014 9 sagrei across those six islands. Their results showed that predators altered the lizards perching behavior and increased mortality, but did not alter selection on phenotypic traits. Yet, increased competition was found to increase selection favoring larger body size, longer limb length, and greater running stamina. These results support the hypothesis that in adaptive radiation of island species, intraspecific competition is more important than predation in shaping the selection for traits central to the adaptive radiation of Anolis ecomorphs (Calsbeek 2010). Is the adaptive radiation of Caribbean Anolis an “island radiation”? Despite being regarded as a “classic” case of island radiation throughout literature regarding Anolis adaptive radiation, such as Calsbeek 2010, one study contends whether Anolis radiations in the Caribbean are actually an island radiation. The term island radiation entails a rapid diversification of species driven by an island setting since it provides new niches that drive diversification as organisms adapt to occupy them. A corollary of this is thus that mainland species should evolve more slowly and in a limited fashion compared with island species. Since Anolis species inhabit both the mainland of central America and northern South America in addition to islands of the Caribbean, they provide an opportunity to compare mainland and island radiations. In 2008, a paper titled Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards was published. It supports that Anolis radiations in the Caribbean are not classic island radiations because the diversification of species that occurs on the islands also occurs in mainland species. Researchers found that overall mainland anoles exhibited many of the same features that are seen in Caribbean anole radiation. The extent of ecomorphological divergence was substantial in the mainland and the rate of evolutionary change was shown to be at least as great as that in the Julie Wiemerslage 11/14/2014 10 islands. Additionally, the Caribbean anoles are known for having a weak correlation between morphology and phylogeny that indicates repeated evolution of the same ecomorphs across islands, and this trend was found to be just as prevalent in mainland anoles. Therefore, this paper supports that the adaptive radiation of Anolis lizards in the Caribbean is not an island radiation (Pinto, 2008). Conclusion Lizards of the genus Anolis are highly adaptable and their location in the Caribbean provides them with many ecological opportunities. As a result, Anolis lizards are represented by many species in the Caribbean, and thus make an ideal example of adaptive radiation. They have both morphological and behavioral adaptations that have evolved independently on different islands as a result of adaptations to local habitats (Ord 2013). Investigations have found strong support that intraspecific competition is the driving force for morphological adaptations in Anolis, and predation plays a role in their adaptation too (Calsbeek 2010). Also, although this example of evolutionary radiation is frequently regarded as a classic island radiation, some researchers argue that it does not actually fit that model because the amount and rate of adaptation of Anolis lizards on islands is equal to that of those on mainland’s (Pinto 2008). Ultimately, the evolutionary exuberance of this example of an adaptive radiation evidently exposes the power of natural selection to produce biological diversity, as originally realized by Charles Darwin. Furthermore, adaptive radiations are important to study because they magnify the process of adaptation, and sometimes speciation (Losos 2010). Therefore, this fascinating topic provides a unique opportunity to investigate evolutionary processes. It offers great insight Julie Wiemerslage 11/14/2014 11 into how and why speciation occurs. For that reason, there is a wealth of research, both already published and ongoing, regarding this phenomenon. Sources Baum, D. A., and A. Larson. 1991. Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Systematic Zoology 40:1–18. Calsbeek, Ryan, Cox, Robert M. 2010. Experimentally testing the relative importance of predation and competition as agents of selection. Nature. 465(7298): 613-6. Elstrott, J . & D. J. Irschick. 2004. Evolutionary correlations among morphology, habitat use and clinging performance in Caribbean Anolis lizards. Biol. J. Linn. Soc. 83: 389-398. Irschick, D. J., C. C. Austin, K. Petren, R. N. Fisher, J. B. Losos & O. Ellers. 1996. A comparative analysis of clinging ability among pad-bearing lizards. Biol. J. Linn. Soc. 59: 21-35. Jablonski, D. 2001. Lessons from the past: evolutionary impacts of mass extinctions. Proceedings of the National Academy of Sciences of the USA 98:5393–5398 Jenssen, T. A. 1977. Evolution of anoline lizard display behavior. American Zoologist. (17) 203-215. Larson, A. & J. B. Losos. 1996. Phylogenetic systematics of adaptation. Pp. 187-220 in M. R. Rose & G. V. Lauder (editors), Adaptation. Academic Press, San Diego. Losos, Jonathan B., Glor, Richard E. , Kolbe, Jason J. and Nicholson, Kirsten. 2006. Adaptation, Speciation, and Convergence: A Hierarchical Analysis of Adaptive Radiation in Caribbean Anolis Lizards. Annals of the Missouri Botanical Garden. 93(1): 24-33. Losos, J. B., and R. E. Ricklefs. 2009. Adaptation and diversification on islands. Nature 457:830–836. Losos, Jonathon B. 2010. 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