Category: New Research Page 38 of 66

The study of geographic variation has long been a foundation of evolutionary biology. As Martha Muñoz explained, in recent years attention has focused on whether geographic variation is the first stage in the process of speciation resulting from divergent selective pressures. Making the case for such ecological speciation requires demonstrating the occurrence of divergent selective pressures correlated with environmental differences and that the resulting  phenotypic differences lead to a reduction in genetic exchange among populations in different populations.

Martha reported on a study of the highly variable Guadeloupean anole, Anolis marmoratus. Detailed population level sampling confirmed that differences in body color correlate with environmental differences, with bluer populations in wetter habitats. These results strongly suggest the role of divergent natural selection as the cause, particularly because the differences were replicated across two different transects. Moreover, the fact that the color differences occur only in males suggests a role for divergent sexual selection.

Coalescent analyses of molecular genetic differences suggested that these differences occurred in the presence of gene flow, i.e., a parapatric model of divergence, rather than in allopatry. However, estimates of ongoing gene flow find no evidence of reduced gene flow across environmental  borders. In other words, even though selection is driving phenotypic differences, these differences are not leading to a reduction in genetic exchange–selection does not appear to be leading to speciation, contrary to the ecological speciation hypothesis.

These results are in agreement with studies on several other Lesser Antillean anoles. Martha pointed out that in situ cladogenetic speciation only occurs in anoles on the large islands in the Caribbean, suggesting that the lack of opportunity for allopatry on small islands precludes speciation from occurring, even in the presence of strong divergent selection.

These results were recently published in Molecular Ecology and are further discussed in a previous post.

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.

Anolis cristatellus basking in the sun. Photo by Janson Jones.

In recent years, concern has arisen about how tropical ectotherms will cope with rising temperatures. For a variety of reasons, tropical species are considered particularly vulnerable, and coarse scale modelling exercises suggest that many populations and species may face extinction in the near future. Some of the most influential studies, such as Sinervo et al.’s mammoth 2010 paper (already cited more than 200 times!), have focused on lizards.

The field of thermal ecological physiology made great advances in the 1970’s and 80’s and a, perhaps the, major player in the work was research on lizards. And amongst this work, studies on Anolis played a particularly prominent role (reviewed in Chapter 10 of Lizards in an Evolutionary Tree). Hence, it is no surprise that a reconsideration of lacertilian prospects, based on detailed understanding of how lizards interact physiologically with their environment, is stemming from in-depth studies on anoles.

Most modelling studies are based on a coarse-grained (1 km² resolution), remote sensing scale analysis of global temperature variation, with the assumption that relatively little variation in thermal environment occurs within each block. Recent papers focusing on anoles in Puerto Rico (Leal and Gunderson, 2012) and offshore islands in Honduras (Logan et al., 2013) have tested this idea and found it wanting–in open areas and, to a lesser extent, within forests–considerable thermal heterogeneity occurs. Moreover, many anole species thermoregulate behaviorally–i.e., they aren’t passive samplers of the environment, their body temperature a simple reflection of the ambient, but rather they move in and out of sun and shade, and thus can determine their temperature, mediating what is available in the environment. Thus, even if the environment gets warmer, lizards may have the option simply to switch to increased use of the cooler micro-environments, maintaining the same body temperature.

Plateau in peak sprinting performance in relation to body temperature in Anolis cristatellus. Increases in body temperature over the range of ca. 31-36 C will have little effect. Figure from Gunderson and Leal (2012).

A third point is relevant as well. Physiological performance is generally temperature-dependent, but often a broad plateau exists in which maximal performance varies over a broad range of body temperatures. Hence, populations may be buffered from effects of increased temperatures if the resulting increase in body temperature does not push them off the plateau.

Both studies ask the simple question: if global temperatures go up, will lizards in open and forested habitats experience an increase or a decrease in the quality of the thermal environment, quantified in terms of how readily they are able to achieve their optimal temperature (using sprint speed as a proxy).

Anolis bicaorum from Utila, one of the forest species in the Logan et al. study. Photo by J. Losos.

The results show interesting similarities and differences.

Read More

Anolis allisoni, the green lizard wearing a blue jumper. Photo by J. Losos.

Female A. gorgonae. Photo by Joe Burgess.

Two of the world’s coolest lizards are blue anoles, male A. allisoni from Cuba and both sexes of the fabled blue anole of Gorgona (A. gorgonae). Why the blue? Heck if I know. You can see a male allisoni on a palm from a great distance, so it amazes me that they can survive. Seems clear that they must be trying to advertise their presence. On the other hand, I’m told that A. gorgonae can be very hard to spot when one looks up toward the canopy, where the species hangs out. In this instance, the blue may actual serve for crypsis. Who knows?

Lets not forget the blue toes of Anolis bartschi! Photo by Joe Burgess.

Turns out that there are lots of blue animals and the reason for their blueness, as well as the mechanism by which it is produced, is not well known. Kate Umbers has just published a nice review in Journal of Zoology on all things blue, and it’s a worthwhile read, even if she didn’t mention anoles, or even hardly any lizards at all. Among other interesting tidbits, she points out that dichotomizing colors as structural or pigmentary is somewhat misleading, because both pigments and structure can work together to produce blue colors. Also, blue-footed boobies’ feet are bluer when they’re well-fed, and female boobies invest more in their offspring if they have brighter blue feet.  Who knows what interesting blue-related aspects of natural history remain to be uncovered in anoles?

Many anoles have blue eyes as well, and this is a trait that seems to pop up repeatedly throughout the clade, though I have no data on this. I wonder what’s up with that.

Anolis peraccae. Photo by Alejandro Arteaga.

As a final bonus, here’s a video of a blue knight anole! (and here’s a previous AA post on the same). The video itself isn’t so sharp, but it’s a blue knight anole!

httpv://www.youtube.com/watch?v=hwHhyqTmqrk&feature=youtu.be&a

Some like it hot. Anolis allisoni on Roatan, an inhabitant of open areas, will benefit from increased global temperatures. Photo by J. Losos.

Thanks to HerpDigest, a regular email compendium of herpetological news, here is a press release on a recent paper in Global Change Biology:

A new Dartmouth College study finds human-caused climate change may have little impact on many species of tropical lizards, contradicting a host of recent studies that predict their widespread extinction in a rapidly warming planet.

Most predictions that tropical cold-blooded animals, especially forest lizards, will be hard hit by climate change are based on global-scale measurements of environmental temperatures, which miss much of the fine-scale variation in temperature that individual animals experience on the ground, said the article’s lead author, Michael Logan, a Ph.D. student in ecology and evolutionary biology.

To address this disconnect, the Dartmouth researchers measured environmental temperatures at extremely high resolution and used those measurements to project the effects of climate change on the running abilities of four populations of lizard from the Bay Islands of Honduras. Field tests on the captured lizards, which were released unharmed, were conducted between 2008 and 2012.

Anolis bicaorum, a denizen of closed forest, from Utila, Honduras. Photo by J. Losos.

Previous studies have suggested that open-habitat tropical lizard species are likely to invade forest habitat and drive forest species to extinction, but the Dartmouth research suggests that the open-habitat populations will not invade forest habitat and may actually benefit from predicted warming for many decades. Conversely, one of the forest species studied should experience reduced activity time as a result of warming, while two others are unlikely to experience a significant decline in performance.

The overall results suggest that global-scale predictions generated using low-resolution temperature data may overestimate the vulnerability of many tropical lizards to climate change.

Another photo of A. allisoni, just because they’re so cool. Photo by J. Losos

“Whereas studies conducted to date have made uniformly bleak predictions for the survival of tropical forest lizards around the globe, our data show that four similar species, occurring in the same geographic region, differ markedly in their vulnerabilities to climate warming,” the authors wrote. “Moreover, none appear to be on the brink of extinction. Considering that these populations occur over extremely small geographic ranges, it is possible that many tropical forest lizards, which range over much wider areas, may have even greater opportunity to escape warming.”

An example of open habitat, from the island of Cayo Menor. Photo by Mike Logan.

An example of closed forest, from the island of Roatan. Photo by Mike Logan.

Story Source: The above story is reprinted from materials provided by Dartmouth College, via EurekAlert!, a service of AAAS.

Phylogeny of lizards from Pyron et al.

In a monumental undertaking, Alexander Pyron and colleagues have just produced a molecular phylogeny for 4,161 species of lizards (including snakes), more than 40% of the 9400+ species described to date. The paper, now available online at BMC Evolutionary Biology, is a blockbuster, containing 28 figures, one an overview of the entire phylogeny and the remainder walking through lizard-life one clade at a time.

The analysis is based on sequence data from 12 commonly used and phylogenetically informative molecular markers (seven nuclear genes, five mitochondrial). On average, 12,896 base pairs of sequence data are available per species and, as is necessary in an endeavor such as this, the data set is incomplete, with an average of only 19% of base pair data being available for any given species.

The results are generally very concordant with recent molecular phylogenies, perhaps not surprising given that these data have been used in the most recent studies. The overall picture of lizard phylogeny is little-changed from what we’ve seen in recent molecular phylogenetic publications, but there are a few surprises at lower levels. You’ll have to peruse the paper yourself to check out your favorite group, as there’s way too much in it to go through here.

Of course, what readers of AA really want to know is: what does the phylogeny say about anole relationships? And, in fact, the results are for the most part concordant with previous studies. Perhaps surprising to many readers, the analysis supports the monophyly of the eight clades recognized by Nicholson et al. as separate genera. Well, almost. In contradiction to the paper’s statement, Nicholson et al.’s Anolis is not monophyletic because A. argenteolus is placed as the sister-taxon to the Xiphosurus clade (which contains Chamaeleolis and the ricordii group), rather than occurring with other species placed into the restricted Anolis. This is an odd finding, contradicting both Nicholson et al. and the Alfoldi et al. genome paper analysis, with the implication that the transparent lower eyelids of A. argenteolus and its putative sister taxon A. lucius are not homologous, but I don’t buy it. Other than that, I didn’t find anything too exciting in this phylogeny, though further scrutiny (it’s enormous) may turn up interesting relationships I didn’t notice.

Other than this one exception, however, the Nicholson et al. eight fare well. Nonetheless, the authors of this paper do not follow the Nicholson et al. taxonomic suggestion of subdivision, stating: “since Anolis is monophyletic as previously defined, we retain that definition here…for continuity with the recent literature.”

Laemanctus longipes, a member of the sister group to Anolis. Photo by Petrovan Silviu.

Probably the most interesting finding concerns the closest relative to anoles, a topic of great uncertainty. This analysis strongly confirms that Polychrus is not the sister group to Anolis; rather, Polychrus appears related to the hoplocercids, which means that it’s dewlap must be convergent with the anole flasher. To whom, then, are anoles related? The answer appears to be the basiliscines (Corytophanidae in more modern parlance), the morphologically diverse and fascinating neotropical group containing not only basilisks, but also Corytophanes and the little-known Laemanctus.

Two last points: first, as noted above, there’s lots of missing data. Clearly, this is not the last word and, in particular, the question of the sister taxon to Anolis cries out for further study. Second, as the authors note, this paper will be of inestimable value in conducting comparative studies spanning the entire lizard radiation. To facilitate such, the authors have made available a Newick file containing the phylogeny (if you don’t know what this means, suffice to say that it’s a very helpful move that will make it easy to use this phylogeny in comparative studies).

Now, let’s get out and sequence the other 5000 species and finish the job!

[Editor’s Update, March 18, 2014]: I was mistaken in saying that the Pyron et al. tree found only one inconsistency with the Nicholson et al. genera. In addition to the exception noted above, Nicholson et al. place christophei in their Chamaelinorops clade, but Pyron et al. find it allying with species that Nicholson et al. put in Xiphosurus.

My recently published paper in Herpetological Conservation and Biology about the effects of human land use on Anolis carolinensis (abstract below) came from an exciting season of field research. The summer of 2010 in Palmetto State Park in Gonzales, Texas was my first field research experience, where I took my first steps of many (little did I know) into the world of Anole biology. I worked under the supervision of Michele Johnson with an awesome lab group: Tara Whittle (our lab technician), Alisa Dill, Michelle Sparks, and Chelsea Stehle. Yes, I was the only male, and yes, that means I did get a tent all to myself. I took so many things from this experience, both scientific and not, that started my future as a field biologist.

We spent our days out in the hot Texas summer heat, catching, measuring, and observing our new friends, the green anoles. Each of us had our own research to work on that focused on various aspects of green anoles, and so we divided up our field time amongst our projects, helping each other collect data. We designated plots throughout the state park so we could compare the anoles in those plots. I studied the ways that human land use, such as clearing land for buildings, or constructing trails through natural habitat, impacts the lizards’ prey and the lizards themselves. While we did not find any clear trends showing that human disturbance impacts insects, which in turn affects the anoles, we were able to show that human-disturbed plots had higher insect biomass. This would seem beneficial to the anoles, who would theoretically have higher body condition (BMIs: SVL divided by mass) because of the greater amount of available food. However, we found that lizards (females in this case) in plots with greater levels of disturbance had lower BMIs.

The non-straightforward results from my study reflect the complexity of the relationship between humans and the environment; our impacts on the world do not always easily appear. I am taking what I have learned from this experience and am continuing to use anoles as a system to study human impacts on the environment at a local scale. This fall, I will attend the University of Rhode Island and study anoles with Jason Kolbe.

Abstract:

ANDREW C. BATTLES, TARA K.WHITTLE, CHELSEA M. STEHLE, AND MICHELE A. JOHNSON

Abstract.—Lizards frequently occur in disturbed habitats, yet the impacts of human activity on lizard biology remain understudied. Here, we examined the effects of land use on the body condition of Green Anole lizards (Anolisvcarolinensis) and the availability of their arthropod prey. Because human activity generally alters abiotic and biotic habitat features, we predicted that areas modified by humans would differ from areas with natural, intact vegetation in arthropod abundance and biomass. In addition, because biological communities in high use areas are often relatively homogenized, we predicted that higher human land use would result in lower prey diversity. Regardless of land use, we also predicted that areas with greater prey availability and diversity would support lizards with higher body condition. We studied anoles in six plots with varying levels of human modification in Palmetto State Park in Gonzales County, Texas. We quantified arthropod abundance, biomass, and diversity in each plot via transects and insect traps. We also determined lizard body condition using mass:length ratios and residuals, fat pad mass, and liver lipid content. We found that, although arthropod abundance did not differ across plots, arthropod biomass was higher in natural than in disturbed plots. Diversity indices showed that the plots varied in their arthropod community diversity, but not in relation to disturbance. Female (but not male) lizard body condition differed across plots, with body condition higher in natural plots than disturbed plots. Together, these results suggest that land use is associated with lizard body condition, but not through a direct relationship with prey availability.