Anole Annals

In part II of the day’s Bahamian Anolis sagrei talks, Bob Cox addressed the question: How do males and females evolve different phenotypes despite sharing the same genome? And what better organism with which to study that question than anoles—lots of variation in dimorphism occurs not only among species, but also among populations within species.  This study focused on two populations of Bahamian A. sagrei in which the extent of male-biased dimorphism in body sizes varies—on Exuma, males are 33% bigger than females, whereas on Eleuthera, they are only 22% bigger. The difference is entirely the result of differences in male body size.

Cox asked three questions:

1. Do populations differ in sex-specific natural selection on body size?

2. Are sex-specific growth trajectories that give rise to sexual size dimorphism (SSD)?

3. Are differences indicative of differences in genetic correlations between sexes?

To address the first question, animals were caught at the start of breeding season; measured, marked and released; and then recaptured three months later to test for selection on body size. They found that selection is stabilizing on size in females, whereas there is strong directional  size for large size in males. However, selection doesn’t seem to differ among populations, so differences in selection would not seem to account for the differences in SSD.

However, their recapture studies allowed them to measure growth rates, and they found that males grow significantly faster on the island with higher SSD (Exuma). Animals were then raised in a lab common garden to see if the same differences in growth occur. Preliminary results show that males from Exuma grow faster in the common garden, suggesting either genetic differences or something early in development lead to growth differences (these are wild caught animals).  To further test this hypothesis, lab-raised juveniles were tested and early results indicate no differences in growth rates, which suggests that differences in SSD may not be genetically based, but these results are very preliminary. Despite lack of evidence for sex-specific growth trajectories, there is evidence for sex differences in genetic correlations between the sexes for body size (i.e., are growth rates correlated in opposite sex siblings). These correlations are much weaker in the high SSD population than in the low SSD population—these results, too, are preliminary.

“How do ectotherms evolve in response to changes in their thermal environment?” asked Mike Logan of Dartmouth University. Logan and colleagues studied adaptive evolution in the thermal performance curve—what is the optimal temperature for performance? How does selection work on components of the curve—i.e., optimal temperature, performance breadth (range at which organism can perform at 80% of maximum) and maximal performance capability.

Logan made four predictions:

1. Optimal temperature should be coadapted with mean body temperature, which may be related to mean environmental temperature;

2. Performance breadth should be coadapted with variance in body temperature;

3. Specialist-generalist temperature. Individuals faced with broad range of temperatures can’t specialize as well to particular temperatures;

4. thermodynamic effect—the “hotter is better” hypothesis, i.e., that a positive correlation will exist between maximum performance and optimal performance temperature

The study focused on two populations of A. sagrei, a natural population on the island of Great Exuma and an experimental transplanted population on Eleuthera. The transplant involved moving lizards from a shady site similar to the natural one to a more exposed, warmer site. The researchers measured running speed at five temperatures and calculated a performance curve for each individual, then marked animals and let them go, recapturing them at end of season to quantify selection on performance curve characteristics. They also measured operative temperature at the sites. Natural population and the source location for the transplant were similar and cool, with a mean environmental temperature of about 29. The warm transplant site was about 2-3 degrees higher, also with higher variance.

Positive directional selection for optimal performance temperature was detected in the transplanted population—lizards with higher optimal temperature survived better. No such selection occurred in baseline population. Moreover, selection on performance breadth was stabilizing in the natural population and directional in transplanted population.

This fabulous study has important implications, as Logan noted. Anolis sagrei is known to thermoregulate strongly, but these data suggest that behavior won’t inure individuals from strong selection in a novel, warmer habitat. Moreover, the study has important implications for the ability of populations to adapt to changing climates.

Ian Wang kicked off the anole portion of this year’s Evolution meetings by presenting his Young Investigators Prize lecture on the role of geographic distance and environmental differences as causes of genetic differentiation among populations. Teasing out the effects of these two variables is difficult because they tend to be correlated–nearby populations tend to share similar environments, whereas more distant populations are more likely to occur in different environments.

Ian reported on a new program he has developed, entitled MMRR (pronounced “merrrrr”–I can’t remember what it stands for) to statistically disentangle the two effects. He presented case studies on Yosemite toads and strawberry poison frogs where application of this new method revealed a previously unappreciated effect of environment in determining genetic differentiation. He then reported on a comparative analysis of 17 Caribbean Anolis species in which, as a generality, geographic distance (“isolation-by-distance”) accounted for twice as much of the variation in genetic differentiation as did environmental differences (“isolation-by-environment”).  Interestingly, and inextricably, the major exception was the three species on Jamaica, for which IBE accounted for very little variation. These results were recently published in Ecology Letters and the subject of a previous post.

Ian then presented new results examining geographic variation in morphology in two co-occurring Puerto Rican species, Anolis cristatellus and A. stratulus. In an extension of the structural equation modelling approach used in the anole work, Ian investigated the extent to which morphological variation among populations could be accounted for by environmental variation, controlling for geographic and genetic differences among populations. The results indicated that body size variation in body species was correlated with environment, with larger lizards in hotter/drier areas  (see photo above). In addition, in A. cristatellus, longer-limbed lizards also occur in hotter/drier areas. This is an exciting approach that opens new doors to the study of geographic variation in morphology, and I anticipate that it will be widely emulated.

Anolis krugi, a grass-bush anole from Puerto Rico. Photo from the Reptile Database.

Anolis pulchellus. Photo by Emelia Failing

Although closely-related, the Puerto Rican grass-bush anoles Anolis pulchellus and A. krugi are easy to tell apart based on body shape and color and, particularly, dewlap color. Moreover, they are ecologically different, A. pulchellus preferring hotter microhabitats. Their population genetics, however, are not so straightforward. In a paper now available online at The Journal of Evolutionary Biology, Teresa Jezkova, Manuel Leal and Javier Rodríguez-Robles show that there’s some interspecific hanky-panky going on, or at least there was in the past.

The evidence comes from examination of their mitochondrial DNA. To make a long story short, A. pulchellus in western Puerto Rico seem to have nothing but A. krugi mtDNA. Moreover, there is variation within A. krugi in mtDNA, and this variability is matched geographically by A. pulchellus. That is, western A. pulchellus have the appropriate mtDNA for the A. krugi at their particular locality. The authors suggest that this mitochondrial introgression has occurred many times independently. To make things more complicated, some western A. pulchellus that occur in areas in which A. krugi does not occur—and probably hasn’t for a long time—still have the krugi mtDNA.

And, in case you’re wondering, a pulchellus looks like a pulchellus regardless of its mtDNA. Moreover, one of two nuclear genes examined fell out nicely, with one clade containing A. pulchellus and the other containing A. krugi. Go figure! I’ve pasted the abstract below which gives more details and the authors’ hypothesis of how this came to be.

Abstract

Hybridization and gene introgression can occur frequently between closely related taxa, but appear to be rare phenomena among members of the species-rich West Indian radiation of Anolis lizards. We investigated the pattern and possible mechanism of introgression between two sister species from Puerto Rico, Anolis pulchellus and Anolis krugi, using mitochondrial (ND2) and nuclear (DNAH3, NKTR) DNA sequences. Our findings demonstrated extensive introgression of A. krugi mtDNA (k-mtDNA) into the genome of A. pulchellus in western Puerto Rico, to the extent that k-mtDNA has mostly or completely replaced the native mtDNA of A. pulchellus on this part of the island. We proposed two not mutually exclusive scenarios to account for the interspecific matings between A. pulchellus and A. krugi. We inferred that hybridization events occurred independently in several populations, and determined that k-mtDNA haplotypes harboured in individuals of A. pulchellus can be assigned to four of the five major mtDNA clades of A. krugi. Further, the spatial distribution of k-mtDNA clades in the two species is largely congruent. Based on this evidence, we concluded that natural selection was the probable driving mechanism for the extensive k-mtDNA introgression into A. pulchellus. Our two nuclear data sets yielded different results. DNAH3 showed reciprocal monophyly of A. pulchellus and A. krugi, indicating no effect of hybridization on this marker. In contrast, the two species shared nine NKTR alleles, probably due to incomplete lineage sorting. Our study system will provide an excellent opportunity to experimentally assess the behavioural and ecological mechanisms that can lead to hybridization in closely related taxa.