Author: Martha Muñoz Page 2 of 8

Hanna Wegener giving her talk on Anolis sagrei from the Bahamas at SICB 2016

Small islands are great systems in which to study evolution, in part because their isolation and simplified landscapes makes them amenable to experimental studies. For example, previous experimental work on Anolis sagrei in the Bahamas by Losos et al. (1997) and Kolbe et al. (2012) found evolutionary changes in hindlimb length driven by adaptation to structural habitat over only a few years.

Hanna Wegener, a Ph.D. student studying with Jason Kolbe at the University of Rhode Island, wanted to know if morphological differences associated with habitat use also manifest in natural (rather than experimentally introduced) populations of Anolis sagrei from the Bahamas. She examined genetic (microsatellite) and morphological variation from male and female A. sagrei on seventeen islands in the Bahamas. Despite the islands being separated by very small geographic distances (no more than three kilometers and typically only a few hundred meters), populations on the islands were genetically differentiated. Her genetic analysis further found high levels of inbreeding on each island.

Unlike the findings on the experimental islands, Hanna did not find any correlation between perch diameter and hindlimb length. She did find that female density was high on the islands, and that density correlated strongly with head length and injury frequency, suggesting that competition influences morphological differentiation on these islands. Overall, Hanna found that morphological patterns varied considerably among islands and among males and females. She suggests that this variation is due to stochastic effects on small islands, namely genetic drift, due to the extinction and colonization dynamics in response to hurricanes.

Anolis shrevei, a species inhabiting extreme cold environments on Hispaniola.

Caribbean anoles are widely recognized as a key example of “adaptive radiation,” or the diversification of a group of organisms into different ecological niches*. Anoles in the Greater Antilles (Cuba, Hispaniola, Jamaica, and Puerto Rico) diversified into multiple types of habitat specialists, or “ecomorphs,” so-named for the portion of the structural habitat that they most often occupy. For example, “twig” anoles are found on the distal ends of branches. They have relatively short limbs (and, often, prehensile tails) for navigating their spindly habitat. The ecomorphs have evolved a myriad of morphological features suited to their microhabitat use. But diversification into different structural niches comprises only one dimension of their radiation across the Caribbean. Anoles have also diverged into distinct climatic habitats in the Greater Antilles, such as Anolis shrevei (pictured above), a montane species found at high elevation in the Cordillera Central mountain chain of the Dominican Republic. Some anoles are restricted to desert scrub habitats, others to cloud forests, and others to warm lowland environments. The list goes on!

But how does climatic evolution fit into the bigger picture of the Anolis adaptive radiation across the Caribbean? In a previous study, Mahler et al. (2010) suggested that “ecological opportunity” (roughly, the lack of competitors for ecological niche space) influences rates of morphological diversification into different portions of the structural habitat. In a study just published in Global Ecology and Biogeography, Adam Algar (University of Nottingham) and Luke Mahler (University of Toronto) sought to test the idea that ecological opportunity also influences rates of climatic niche evolution in Caribbean anoles. Although they are tropical, several of the Caribbean islands possess considerable elevational variation , which has created substantial thermal variation and the potential for climatic niche evolution in anoles (See Figure 1 below).

Portion of Figure 1 from Algar and Mahler (in press) showing temperature variation in the Greater Antilles (a) and the Lesser Antilles (b).

Algar and Mahler first quantified two temperature axes (mean temperature and temperature seasonality of species’ localities) of the climate niche for 130 Anolis species on each of the islands in the Greater Antilles, as well as from the northern and southern Lesser Antilles (i.e., the series of small, volcanic islands that dot the eastern Caribbean Sea). The first temperature axis (PC 1) correlated with thermal  minima and maxima and the second temperature axis (PC 2) correlated with temperature seasonality.

Figure 2 from Algar and Mahler showing how rates of thermal PC 1 relates to climate heterogeneity (a), and geographic area (b). (c) shows how rates of thermal PC 1 evolution correlate with climatic heterogeneity after correcting for geographic area. Relationships depicted in (b) and (c) are statistically significant.

They showed that rates of niche evolution for thermal PC 1 was significantly higher in geographically larger regions (Fig. 2b). Thermal PC 1 was, however, unrelated to climatic heterogeneity (Fig. 2a). But, when the residuals of the relationship between thermal PC 1 and geographic area were regressed against climatic heterogeneity, they did recover a significant positive relationship (Fig. 2c), indicating that, over a given area, thermal niche evolution is faster in regions with greater climatic heterogeneity. They conducted the same analyses for thermal PC 2 (temperature seasonality) and, as with PC 1, found no relationship between evolutionary rate and climate heterogeneity and a positive relationship with area. However, in contrast to their results with PC 1, even after controlling for geographic area, they did not recover a significant relationship between evolutionary rate and climatic heterogeneity.

To determine whether the relationships between evolutionary rate and island area could be due to the higher species numbers found on larger islands, they regressed the evolutionary rate against species number. They did find a strong relationship between species number and evolutionary rate. However, given that island area and species number are highly correlated, this result was not unexpected. Thus, they were unable to fully disentangle how island area and species might interact to influence rates of the climatic niche evolution.

In short, Algar and Mahler found that island area greatly influenced the rate of climatic niche evolution. It has long been recognized that island area is a major determinant of species richness and species diversification on islands – on islands above a certain threshold size, in situ speciation can occur. In this study, Algar and Mahler add climate niche radiation to the list – on islands above a certain size, climatic niches can diverge considerably. But how, specifically, does island area contribute to rates of climatic niche evolution? The authors suggest that larger islands allow more speciation along elevational gradients, such as mountains, which can result in climatic specialization (either during the process of speciation or post-speciation). On small islands, they argue, high gene flow may swamp out the effects of climatic divergence even where climatic thermal heterogeneity exists and, when such specialization does occur, those species may be susceptible to higher extinction rates (due to their smaller geographic ranges). In short, climatic niche evolution presents an equally important (though relatively understudied) aspect of the Anolis adaptive radiation in the Caribeean.

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*Scientists differ in their definition of adaptive radiation, though most can agree with the idea that it involves adaptive diversification. Here I follow the definition of Losos and Mahler (2010).

Works Cited

Algar, A. C., and D. L. Mahler. In press. Area, climate heterogeneity, and the response of climate niches to ecological opportunity in island radiations of Anolis lizards. Global Ecology and Biogeography.

Losos, J. B., and D. L. Mahler. 2010. Adaptive radiation: the interaction of ecological opportunity, adaptation, and speciation. Pp. 381-420 in M. A. Bell, D. J. Futuyma, W. F. Eanes, and J. S. Levinton, Eds. Evolution Since Darwin: The First 150 Years. Sinauer Associates, Sunderland, MA.

Mahler, D. L., L. J. Revell, R. E. Glor, and J. B. Losos. 2010. Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean anoles. Evolution 64:2731-2745.

A slide from Danielle Klomp’s talk showing how color is used in communication by some species of lizards. Check out the quick guest appearance by an anole.

The diversity of anole dewlap shapes, colors, and patterns is one of their most distinctive features. But anoles are not the only squamates with flashy dewlaps. When it comes to such accoutrements, anoles have some stiff competition from their Agamid cousins in the Indo-Pacific region, the ‘flying’ dragons (Draco). Draco lizards don’t really fly, of course. Rather, they can laterally expand their ribs and the connecting membrane to create a ‘wing’, which they use to glide between trees in their habitats. If you haven’t seen how they do this, it’s more than worth a watch. Lest you think anoles get left behind in this respect, we do know that some anoles glide, as well, even if they don’t exhibit the impressive wing-like structures that Draco lizards have.

Slide from Danielle’s talk showing Draco lizards and their geographic distribution.

As I learned at Danielle Klomp’s talk at ASH 2015 last week, their dewlaps are almost as impressive as their gliding ability. Danielle is a PhD student working with Devi Stuart-Fox and Terry Ord and her dissertation has focused on studying the evolutionary ecology of Draco lizards. This past week she presented her work on these lizards’ dewlaps and what role they may play in sexual selection. Danielle examined dewlap size and coloration in 13 species of flying dragons. Overall, she found a strong negative correlation between color contrast (meaning they stand out relative to background coloration) and dewlap area in male lizards. Thus, she found that male dragons either had big dewlaps or conspicuously colored dewlaps, but not both. These results suggest that sexual selection for male conspicuity is occurring, but why can’t lizards exhibited large, conspicuously-colored dewlaps? Danielle suggested that having dewlaps that were both conspicuous in color and size were either too risky (meaning that they would be considerably more vulnerable to predation) or too costly to produce or maintain, though the precise mechanism underlying this pattern remains uncertain.

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Emma Sherratt gives her talk on fossil anoles

The annual meeting for the  Australian Society of Herpetology (ASH) is wrapping up here today in the lovely town of Eildon, Australia. Just because we’re a continent away from the native distribution of anoles doesn’t mean that anoles were not represented at the meeting. Yesterday afternoon Emma Sherratt, new faculty at the University of New England in Armidale, Australia, presented some of her post-doctoral work on fossil anoles preserved in amber. Emma began by saying that Caribbean anoles represent one of the oldest examples of extant adaptive radiations. Despite the age of this radiation, most of the work on the Caribbean anoles (and other adaptive radiations, for that matter), has focused primarily on living species, with historical inferences drawn from DNA analyses. She pointed out that historical insights based on analyses of extant species only should be treated with caution, unless there is corroborating information from the fossil record.

We know, she said, that islands are typically inhabited by a single lineage of ecomorphs (with subsequent diversification within ecomorphs). The fact that most ecomorph groups are represented by a single lineage on an island suggests that once an ecomorph niche is filled, it cannot be replaced, an idea known as ‘niche incumbency’. She argued that we can use fossils to assess that hypothesis – if fossil anoles pertain to same lineages of ecomorphs (e.g., the cristatellus clade of trunk-ground anoles, or the carolinensis group of trunk-crown anoles), then that would support the idea that ecomorph niches were only filled once. If extinct anoles fell into different lineages of ecomorphs, distinct from those that are extant today, then that would support the idea that ecomorphs could be replaced on islands, which would suggest that niche incumbency need not be occurring. Of course, it could also be possible for niche incumbency to have occurred if there were two lineages of the same ecomorph present on the same island, as long as the incumbent lineage drove the more recent one to extinction. But the hypotheses proposed by Emma were certainly a reasonable first pass to understand the origin of ecomorphs on the Caribbean islands.

Anoles have been fossilized in Hispaniolan amber, which we know to be about 15-20 million years old. All you folks who are anxiously awaiting the next installment of Jurassic Park be advised – this means that the famous amber used to get dinosaur DNA is far too young, as the dinosaurs (save for birds, of course) went extinct about 62 million years ago. For her study, Emma accessed an impressive 38 anole fossils preserved in amber. By far this is the largest data set of fossilized amber anoles ever examined. And, beyond their utility for understanding the process of diversification, anoles caught in amber are stunning fossils and the high resolution reconstructions that Emma makes using x-ray CT scans are equally impressive.

Emma found strong evidence that Hispaniolan fossil anoles fall into known ecomorph categories. To determine this she compared morphological details from extant species to the fossil anoles. Overall she found substantial morphological variation in the fossils, particularly in 20 of the best preserved and most complete fossils. Amazingly, Emma found that some of the fossils fell very clearly into the trunk-crown, trunk, trunk-ground, and twig ecomorph classes! She was further able to determine that the trunk-crown fossils fell into the chlorocyanus group of extant Hispaniolan lizards, and, with less confidence, evidence that the trunk-ground lizards fell into the cybotes group of extant Hispaniolan lizards. Thus, the results are suggestive that, once an ecomorph niche is filled, it prevents other lineages from evolving into it, which is consistent with niche incumbency. Obviously it is not possible to fully rule out the alternative – that species of other ecomorph lineages existed in the past – but certainly the results are a tantalizing glimpse into the processes that forged the current Caribbean fauna. In short, she found that most ecomorphs recognized today are not only present in the Miocene fauna, but also are represented by members of the same clades. Together, her results were consistent with the idea that niche incumbency occurred in the Caribbean radiation of anoles, which would indicate that interspecific interactions have regulated morphological diversity for millions of years.

Greetings from Eildon, Australia, where the 2015 meeting for the Australian Society of Herpetology (ASH) is currently underway. Today is the first full day of talks and posters and I’m excited to learn what’s new and exciting in herpetology. Although the focus is predominantly on Australian amphibians and reptiles, there are several presentations on non-Australian herpetofauna, as well. Anoles are also represented as I will be giving a talk on my work on Hispaniolan anoles and Emma Sherratt will be speaking about her work on fossil anoles. If you would like to see what’s going at ASH, feel free to follow the conference on Twitter using #ASH15.