Rapid Evolution in Anolis carolinensis Following the Invasion of Anolis sagrei

If the biology of Anolis lizards is a puzzle, then a new paper by Yoel Stuart, Todd Campbell and colleagues is a crucial piece. It’s a puzzle piece that not only contains a wealth of information when held up on its own, but also brings clarity to a broader picture of anole biology when fitted into place.

Anolis carolinensis on small spoil-islands in Florida are the subject of Stuart et al. (2014)

Anolis carolinensis on small spoil-islands in Florida are the subject of Stuart et al. (2014)

A tight relationship between microhabitat and morphology characterizes variation across Anolis species in the Caribbean.  Anole biologists have long suspected that negative interactions, such as competition, are responsible for driving different species into different microhabitats, with subsequent morphological  adaptation to these microhabitats over evolutionary time. But pinning down interspecific interactions as the cause of evolutionary divergence in microhabitat and morphology has been difficult.

Why is establishing this causality challenging?  Upon observing a pattern of consistent differences between populations of a species that occur in sympatry and allopatry with an interacting species, it seems logical to attribute this pattern to the presence of the interacting species. But many processes other than an evolutionary response to negative interspecific interactions can generate such a pattern–environments may differ between sympatric and allopatric populations in a way that drives the observed divergence, individuals from sympatric populations may all be similar only because they  are closely related to each other, the divergence may be a consequence of phenotypic plasticity, or most dishearteningly, the whole pattern may simply be due to chance.

Ruling out these alternatives seems a gargantuan undertaking. Indeed, as Stuart and Losos (2013) point out, in a review that serves as a nice companion piece to this study, only a small fraction of studies describing patterns of divergence between sympatric and allopatric populations tackle the problem of eliminating these alternatives and can thus conclude with confidence that interspecific interactions cause the divergence they observe. But Stuart et al. (2014) take on the challenge.

Like recent research by Helmus et al. (2014) that exploits human-mediated anole dispersal to test classic principles of island biogeography, Stuart et al.’s (2014) research is rooted firmly in the Anthropocene. Occupying centrestage is the interaction between Anolis carolinensis, native to the United States, and Anolis sagrei, a relatively recent invader. The stage itself comprises small man-made spoil islands in Florida, created in the 1950s. When Todd Campbell began this study in the 1990s, A. carolinensis occurred on many of these little islands. Campbell introduced A. sagrei to three islands, and watched how, over the next three years, A. sagrei numbers rose steadily and A. carolinensis shifted higher into the trees on invaded islands, while continuing to perch at lower heights on nearby un-invaded islands.

Lead authors Yoel Stuart and Todd Campbell boating between spoil islands in FL

Lead authors Yoel Stuart and Todd Campbell boating between spoil islands in FL

This rapid shift in microhabitat spurred Stuart and Campbell to return to the islands 15 years later (with a team of field assistants, of whom I was one!) to ask if A. carolinensis on invaded islands had subsequently diverged morphologically from conspecifics on un-invaded islands. By this time, A. sagrei had spread widely. Nevertheless, they found five un-invaded islands. A. carolinensis still perched lower on these un-invaded islands than on nearby invaded islands.

Across Caribbean anoles, species perching higher up on trees have larger toepads and more lamellae on these toepads than do species perching closer to the ground. Recapitulating this interspecific difference, Stuart et al. (2014) found that A. carolinensis on invaded islands had evolved larger toepads and more lamellae than lizards on un-invaded islands in about 20 generations, rapidly establishing a pattern of character displacement. But is this pattern caused by the presence of A. sagrei?

It seems almost criminal to squish into one paragraph everything that Stuart et al. (2014) did to rule out alternative explanations for the pattern of divergence. They reared hatchlings from invaded and un-invaded islands to rule out phenotypic plasticity as a cause for divergence, sequenced a mind-bogglingly large number of SNP loci to establish that A. carolinensis on invaded islands were not closely related to each other, and conducted intensive habitat surveys to rule out environmental differences between invaded and un-invaded islands. This mountain of work supports the idea that the presence of A. sagrei has driven the evolutionary divergence among sympatric and allopatric populations of A. carolinensis. It’s this mountain of work that makes Stuart et al. (2014) a tremendously satisfying paper. We now have a much firmer basis from which to suggest that interspecific interactions have driven patterns of ecomorphological diversification across Caribbean anoles.

But I personally think that this study’s most exciting implications arise from it defining more clearly a part of the anole biology puzzle that still remains relatively empty, namely our understanding of within-population, among-individual variation in microhabitat use and morphology, and the consequences of this variation for behavioural interactions. This summer I came across an A. carolinensis and A. sagrei perched together thus:

A. carolinensis perched below A. sagrei on the University of Florida campus in Gainesville.

A. carolinensis perched below A. sagrei on the University of Florida campus in Gainesville.

These particular lizards couldn’t care less for Stuart et al.’s (2014) findings–clearly, the effect demonstrated in this study is a population-level effect. But this leaves us with a gap between behavioural interactions and eco-evolutionary dynamics–how exactly do we transition from individual A. carolinensis that are content to perch below A. sagrei to a population-level shift in A. carolinensis perch height in the presence of A. sagrei? Reassuringly, the divergence that Stuart et al. (2014) document is so rapid that this question becomes tractable–their results  emphasize an opportunity to integrate behavioural timescale with eco-evolutionary timescales. We can now examine individual interspecific behavioural interactions  among anoles, safe in the knowledge that ecological and evolutionary responses are not far behind.

 

Editor’s Note (October 28, 2014): Yoel Stuart provides the first perspon perspective on the study on eco-evolutionary dynamics

Editor’s Note II (November 3, 2014): The most thorough press coverage of this paper was in the Orlando Sentinel which as an added bonus had two animated talking anoles explaining the results.

Editor’s Note III (November 4, 2014): Yoel Stuart provides a more in-depth description of the study on the Howard Hughes Medical Institute’s The Conversation

7 thoughts on “Rapid Evolution in Anolis carolinensis Following the Invasion of Anolis sagrei

  1. I saw a version of this presented a few years ago at the World Congress of Herpetology in Vancouver; it was my first introduction to the study of evolutionary ecology in anoles, and it had a substantial impact on the development of my own research interests. I’m glad to see it has finally been published.

      1. I’m working on my M.S. with Sandy Echternacht and Ben Fitzpatrick. We’re investigating potential differences in habitat use, morphology, and genetic structure among A. conspersus color morphs.

          1. Grand Cayman, yes. I’m not aware of any populations that have established elsewhere, though I wouldn’t be surprised if they became successful in Florida.

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