Download Julie Wiemerslage 11/14/2014 The Adaptive Radiation of Caribbean

Julie Wiemerslage
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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
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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
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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
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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
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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
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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
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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.
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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
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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
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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
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into how and why speciation occurs. For that reason, there is a wealth of research, both already
published and ongoing, regarding this phenomenon.
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