Category: New Research Page 37 of 66

Eminent herpetologist Laurie Vitt, recently retired from the University of Oklahoma (but active as ever), gave the Distinguished Herpetologist’s Lecture at the 2012 Annual Meeting of the Herpetologists League, which was part of The World Congress of Herpetology 7. The talk, the basis of a just-published paper in Herpetologica, was a paean to the fundamental importance of natural history to modern science, using vignettes from Laurie’s career as excellent examples.

The article starts in a thought-provoking way:

“Darwin’s studies provide a prime example of the importance of natural-history studies to conceptual biology… [On his voyage on the Beagle], Darwin collected a massive amount of data on geology, zoology, and botany while on land; and after returning, publishing some classic monographs, and mulling over his observations, he assembled his classic volume “On the Origin of Species,” in which a massive amount of natural-history data combined with experimental studies on selective breeding were used to support his theory of evolution by natural selection.”

And the key take-home:

“At least five key elements contributed to Darwin’s ability to put together his compelling theory, which continues to be the unifying theme of modern biology: (1) five continuous years in the field collecting natural-history data, (2) funding with no apparent restrictions on what he could do, (3) no electronic distractions, (4) time to write and think after returning, and (5) much help, including funding for the classic Zoology series, edited by Darwin but published by various authors.”

Though not extensively autobiographical at a personal level, there are some vignettes:

“I grew up with an interest in natural history, subjecting my parents to loose bats and garter snakes in the house, as well as rattlesnakes and later, Old World vipers including puff adders, Gaboon Vipers (Bitis gabonica), and Russell’s Vipers (Daboia russelii) in terraria in my bedroom (which in retrospect suggests that I was either ignorant of the potential effects of snakebite, or downright stupid!).”

And it concludes with an important, little appreciated message

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Two years ago, Castañeda and de Queiroz published a phylogeny of Dactyloa clade anoles based on molecular data for 40 species, approximately half of the clade. It was far and away the best phylogenetic work published on the clade and brought sense to a previously not well understood part of the anole world. The study revealed the existence of six geographically coherent clades and had important implications for our understanding of morphological evolution in this clade, which contains the mainland giants.

Recently, Castañeda and de Queiroz have published a follow up study in which they add morphological data for 60 species (the original 40 plus 20 more). The paper is published in the Bulletin of the Museum of Comparative Zoology and, like all MCZ publications, is freely available for download (click on Breviora or BMCZ on the left hand of the page). We’ve already previously discussed one aspect of the paper, a note added in press critiquing the Nicholson et al. proposal to split Anolis into eight genera.

The main focus of the paper, however, is to ask whether adding morphology increases the resolution or changes the story of the phylogeny based on molecular data. And the answer is: no, it doesn’t. As found in previous studies, morphology on its own does not provide a coherent picture of anole relationships, nor does it seem to substantially change the results derived from the much more informative molecular data. However, morphology certainly has one advantage–it allows us to add in taxa for which no molecular data are available.

The paper’s abstract gives much more detail and, of course, you should check out the paper itself.

ABSTRACT. We present a phylogenetic analysis of the Dactyloa clade of Anolis lizards, based on morphological (66 characters of external morphology and osteology) and molecular (4,700 bases of mitochondrial and nuclear DNA) data. Our set of morphological characters includes some that exhibit continuous variation and others that exhibit polymorphism within species; we explored different coding methods for these classes of characters. We performed parsimony and Bayesian analyses on morphology-only and combined data sets. Additionally, we explicitly tested hypotheses of monophyly of: 1) Dactyloa including Phenacosaurus, 2) Dactyloa excluding Phenacosaurus (as traditionally circumscribed), 3) taxa previously ranked as series or species groups described based on morphological characters, and 4) clades inferred from molecular data. The morphological data alone did not yield Dactyloa or any of the previously recognized series described based on morphological characters; only the Phenacosaurus clade (as delimited based on molecular data) was inferred with the morphological data, and only in the parsimony analysis. In contrast, Dactyloa was inferred as monophyletic with the combined data set, although topology tests failed to reject the hypothesis of non-monophyly. Additionally, five clades inferred based on molecular data (eastern, latifrons, Phenacosaurus, roquet, and western) were inferred with the combined data sets with variable support and including additional species for which molecular data were not available and which have geographic distributions that conform to those of the clades in which they were included. Of the previously recognized taxa based on morphological characters, only the roquet series, which corresponds in species composition to the roquet clade, was inferred with the combined data. Topology tests with the combined data set rejected the monophyly of the aequatorialis, latifrons (as traditionally circumscribed), and punctatus series but not that of the tigrinus series and Phenacosaurus (as traditionally circumscribed). Our phylogenetic analyses and topology tests indicate that a new taxonomy for Dactyloa is warranted; we therefore present a revised taxonomy based on the results our phylogenetic analyses and employing phylogenetic definitions of taxon names.

 

Think quick: how many states does A. carolinensis occur in naturally? And can you name them?

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Two months ago, Masakado Kawata summarized the ongoing collaborative research program between Tohoku University in Japan, Habana University and the National Museum and Natural History of Cuba. The first fruit of this research has now been published in this month’s issue of Ecosphere (lead author Antonio Cádiz recently received his Ph.D. from Tohoku).

The paper is the result of an impressive field research program in which 12 species of Cuban trunk-ground anoles were studied at 34 sites throughout the breadth of Cuba. The abstract pasted below provides the nitty-gritties (and, of course, read the paper yourself), but here are some of the interesting take-home messages:

1. Three species–A. allogus, A. homolechis, and A. sagrei–are widespread throughout Cuba, but the remainder have localized distributions.

2. Co-occurring species are a phylogenetically random subset of the clade, a result that obtains because of the combination of localized and widespread species that co-occur (four can occur in sympatry and five in an area).

3. Sympatric species are ecologically overdispersed, with species occupying different thermal microhabitats co-occurring.

4. Both A. allogus and A. jubar are paraphyletic with deeply divergent, geographically disjunct clades. The authors treat the clades as different species, and perhaps it is time for someone to formally describe them as such.

5. Anolis delafuentei–known, if I’m not mistaken, from a single individual–defied efforts to recollect it. Is this a real species? Is it extant?

Overall, this is an excellent study that could serve as model for the study of other species-rich ecomorph clades, both on Cuba (e.g., alutaceus group) and elsewhere.

Abstract:

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This year’s herp meetings will be held next week (July 10-15) in Albuquerque. Appropriately enough given the venue, it’s the Steve Poe Lab Show, with eight presentations emanating therefrom. Nonetheless, there are a number of other anole talks as well. Below is the list of the talks and below the fold, and attached as a pdf, are the abstracts.

AA is looking for reporters to provide eyewitness accounts of these talks. Many of the abstracts are cagey about what their actual findings are, no doubt out of paranoia and, more likely, an early abstract submission deadline combined with talks that are probably still being finalized. Those attending these talks, please let us know–any level of detail would be welcome!

Titles:

Julian Davis, Steven Poe

0702 Herp. Systematics & Evolution, San Miguel, Saturday 13 July 2013

A Phylogenetic Analysis of the Anolis pentaprion species group

 

Anthony Geneva, Richard Glor

0746 SSAR SEIBERT AWARD SYSTEMATICS & EVOLUTION, San Miguel,  Friday 12 July 2013

Reproductive Isolation in Anolis lizards

 

Levi Gray, Robbie Burger

0512 SSAR SEIBERT AWARD PHYSIOLOGY & MORPHOLOGY,  Galisteo/Aztec, Friday 12 July 2013

Do allometries reveal evolutionary constraints in Anolis lizards?

 

Aja King, Steven Poe

0610 SSAR EVOLUTION, SYSTEMATICS, AND GENETICS BEST STUDENT  POSTER AWARD, Poster Session I, NW Exhibit Hall, Friday 12 July 201

Colonization and Differentiation in the Honduran Bay Islands Populations of Anolis allisoni

 

Ian Latella, Steve Poe

0662 SSAR ECOLOGY, NATURAL HISTORY, AND DISTRIBUTION BEST  STUDENT POSTER AWARD, Poster Session I, NW Exhibit Hall, Friday 12  July 2013

Habitat Use in Naturalized Anolis Lizard Communities

 

Deidre Linden, Steven Poe

0692 SSAR EVOLUTION, SYSTEMATICS, AND GENETICS BEST STUDENT  POSTER AWARD, Poster Session I, NW Exhibit Hall, Friday 12 July 2013

Estimation of phylogeny of the Anolis cupreus (Squamata: Dactyloidae) species group

 

Kirsten Nicholson, John Phillips, Sarah Burton

0288 Poster Session III, NW Exhibit Hall, Sunday 14 July 2013

Biogeography of Norops capito: Second Example of a Contradictory Pattern

 

Steven Poe

0460 Poster Session III, NW Exhibit Hall, Sunday 14 July 2013

Identification Key for Anolis Lizards

 

Steven Poe

0455 Herp Systematics & Evolution, San Miguel, Saturday 13 July 2013

Phylogeny of Anolis

 

Bradley Truett, Steven Poe

0471 Poster Session II, NW Exhibit Hall, Saturday 13 July 2013

Revisiting the Aquatic Anole Ecomorph

 

Kristin Winchell

0664 SSAR ECOLOGY, NATURAL HISTORY, AND DISTRIBUTION BEST  STUDENT POSTER AWARD, Poster Session I, NW Exhibit Hall, Friday 12 July 2013

Phenotypic shifts in urban populations of the tropical lizard, Anolis  cristatellus

Abstracts below the fold

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A few days back, we reported on a recent paper on hybridization between the Puerto Rican grass-bush anoles, A. krugi and A. pulchellus. But what better way to get the backstory than to hear it straight from the horse’s mouth? So, check out co-author Manuel Leal’s description of how the paper came to be over at Chipojolab.

Although the Evolution meetings are coming to a close, we get to go out on a high note. Christian Cox gave one of the last talks of the day discussing the hormonal basis for gender differences in sexual size dimorphism in anoles. Sexual size dimorphism (SSD), or the tendency for the sexes to differ in the size of different traits, has been widely documented in nature. Usually the male exhibits comparatively larger features, such as bigger body size or larger ornaments. Anoles are an intriguing case of SSD, as the traits that can exhibit dimorphism can vary widely among species. Some species, such as Anolis carolinensis, exhibit SSD in multiple traits, including body size, head shape, and dewlap size. In contrast, other species exhibit minimal SSD. As an example, A. distichus from the Caribbean island of Hispaniola tends to show no SSD in body size or head shape, but has strong SSD in dewlap size.

Christian Cox and his collaborators posit that one mechanism underlying SSD may be a pleiotropic regulator that can couple and decouple dimorphism in different phenotypes and their candidate for this study was testosterone. They conducted experiments manipulating levels of testosterone in adult males and females of Anolis sagrei and assessed how body size, head shape, and dewlap traits changed. Anolis sagrei is a particularly good system for assessing the role of SSD in anoles. Male A. sagrei can be up to 50% larger and three times more massive than females.

To conduct the study, they took three year-old male and female lizards and gave them either testosterone or blank subdermal implants. They maintained lizards under laboratory conditions for two months and then gathered information on morphological dimensions and dewlap characteristics. Under testosterone treatment, males and females grew similarly, whereas males grew faster than females in the control group. This merits restating – they were able to make females grow like males just by applying testosterone! Clearly testosterone has strong effects on male-specific growth patterns.

To determine if testosterone affects metabolism, they measured metabolic rate using stop-flow respirometry. They found that testosterone treatment increased metabolic rate for males and females. Correspondingly, they found that visceral fat bodies were lower in testosterone treated animals, suggesting that increased growth is caused by shunting energy towards growth and away from storage metabolism. They further determined that testosterone treatment increased the size of the humerus and femur, but had no significant effect on jaw length and head width. Because this species exhibits little SSD with respect to head dimensions, perhaps this finding is not surprising, but I would be curious to know whether testosterone influences skull growth in species with SSD in head dimensions, such as A. carolinensis.

Finally, the authors found that testosterone led to increased dewlap size in both males and females. In fact, the dewlaps of testosterone-treated females were comparable in size to those of control males and eroded the sex differences that otherwise existed between them. Testosterone treatment decreased the saturation and brightness in the dewlap, leading the authors to suggest that it accelerates its development, as they posit that this color is representative of the fully developed dewlap in the wild.

Thus, they find strong evidence that testosterone plays a large role in modulating SSD in anoles. In particular, it abolishes differences in growth in various traits except for skull shape. And it can create male-like females as well as forge super-males. It would be interesting to see if, in addition to acquiring a male-like morphology, the females would tend to act like males, as well. Their next step is to conduct testosterone manipulation experiments in A. distichus, a species that has low SSD in body size and head shape, but strong SSD in dewlap size, to determine if the effects of testosterone are repeatable in a system exhibiting a pattern of SSD that is different from A. sagrei.

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Extreme sex differences in the development of body size and sexual signals are mediated by hormonal pleiotropy in a dimorphic lizard. Authors: Cox, Christian L.; Hanninen, Amanda F; Cox, Robert M.

Tony Gamble, a postdoctoral researcher working with Dave Zarkower at the University of Minnesota, presented his work on uncovering sex-specific markers in geckos and anoles. Recent years have seen a large impetus to understand how sex chromosomes evolve. Sex chromosomes can be involved in sex-specific adaptation, genetic conflict, and other important modes of evolution. This line of research is particularly imperative in reptiles because not only do we have comparatively little information about sex chromosomes in this group, but different types of sex determining mechanisms have evolved multiple times and so there are likely multiple sex-specific mechanisms and multiple evolutionary transitions are at play (see Figure above).

Traditionally sex chromosomes were discovered by karyotyping, which is a method of separating and identifying the chromosomes. This is problematic in reptiles because the sex chromosomes of many species are homomorphic, meaning they are similarly shaped and, oftentimes, quite small. Gamble and Zarkower tried a different approach – RADseq – for identifying sex chromosomes. RADseq uses restriction enzymes to identify sex-specific markers. Their reasoning is that in XY systems (i.e., males are the heterogametic sex), you would expect males and females to exhibit X-specific markers and males to exhibit sex-specific markers unique to the Y (i.e., the non-recombining region). In ZW systems (i.e., females are the heterogametic sex), you would expect the opposite. In theory, this could prove a cheap and fast way to determine the sex chromosomes of different species and develop sex-specific markers.

The challenge for this study was to determine the sex chromosomes for the crested gecko and for the anole. Unlike the crested gecko, Anolis is genome-enabled and we have evidence that they are an XY system, and so they used anoles to pilot their method and confirm that it works before trying it on the crested gecko. However, anoles are not without their challenges. The sex chromosomes are not only homomorphic, but they are also micromorphic, meaning they are quite small. Furthermore, the Anolis genome was built using a female anole, making finding sex-specific markers on the non-recombining region (i.e., the Y chromosome) that much more challenging. Their RADseq approach worked quite well, however, as they were able to recover a male-specific marker in A. carolinensis, which they were able to confirm with PCR amplification. They repeated their results using more A. carolinensis (from a different clade), A. sagrei, and A. lineatopus, and were able to recover the same locus. When they conducted this method in the crested gecko, they found evidence for a ZW system and, correspondingly, recoverd two female-specific markers. Thus, they found that RADseq will work in a variety of taxa, even if they are not genome-enabled, and can successfully be used to uncover sex-specific markers. A neat application of this method is that, using their sex-specific primers, you can sequence an embryo to determine its sex, something that was not previously possible.

As Nick Crawford, recent Ph.D. of Boston University, points out, the genomics era allows scientists unprecedented access to understanding the genetic basis of adaptation and, by extension, the genetics of speciation. For his doctoral thesis, Nick focused on understanding the genetics of colorful adaptation in Anolis lizards, which is genome-enabled. Adaptive radiations provide lots of variation among closely related organisms, making anoles a great system for studying the genetics of adaptation.

One feature of anoles that really stands out is how colorful they are. Just a casual glance at some of the color variation in dewlaps among species reveals that color is likely an important component of species diversification in anoles. Nick focused on Anolis marmoratus, a colorful anole from the Caribbean island of Guadeloupe. Anolis marmoratus is an excellent choice for studying the genetics underlying color. This species exhibits strong geographic variation in coloration and, as I discussed in my talk a few days ago, lacks a strong signal of genetic structure. In this case, searching for the genes underlying local adaptation can be conducted without the confounding effects of population structure.

Nick focused on A. m. marmoratus, which has red marbling on its head, and A. m. speciosus, which has a blue head and, oftentimes, a blue body and tail. These two species are clinally distributed along the eastern side of Basse Terre and A. m. speciosus ranges into the nearby island of Grande Terre (see Figure 1). Rather than use RAD tags, Nick sequenced the genomes for 20 individuals (10 each per subspecies). For every 5 kb along the genome, Nick measured divergence using various metrics of structure and assessed sequence divergence.

Overall, Nick found that about 2% of the genome falls within divergent regions for these two subspecies. Importantly, he found divergence in two genes involved in carotenoid pigmentation and one gene involved in melanosome transport. Divergence in the two carotenoid genes could very well underlie the color divergence in A. m. marmoratus, which has distinct red marbling on its head. These genes fall in regions containing several fixed single nucleotide polymorphisms (SNPs) in a row. Nick suggests that these are likely single haplotypes that are being selected in different environments. Finally, he found no evidence of coding sequence changes, and so he posits that the modifications are probably cis-regulatory in nature. For many years we have been waiting to find out how divergence in coloration occurs in anoles. After seeing Nick’s work, it appears we are closer than ever before to understanding local color adaptation at a genomic level, so stayed tuned to his work for more to come.

Yesterday, Matt McElroy presented a phylogenetic analysis of the Puerto Rican radiation of anoles. The work was focused around the “stages of radiation” hypothesis that states that divergence occurs along different niche axes at different points in time. In the case of anoles, it has long been argued that the last stage in radiation is divergence of ecomorphologically similar species into different climatic niches.

McElroy constructed a phylogeny for 180 individuals of eight species, encompassing the geographic distribution of these species (most of which occur island-wide). Ten genes were sequenced, nine nuclear and one mitochondrial. The resulting phylogeny was well-resolved and in agreement with previous phylogenetic hypotheses, indicating that ecomorphs evolved relatively early in the radiation and that closely related sister taxa pairs are usually members of the same ecomorph, but differ in climate–the one exception–which always has struck me as odd, but apparently is correct–is the sister taxon relationship between the deep rainforest trunk ground species A. gundlachi and the xeric grass-bush species, A. poncensis.

The time of divergence was estimated for each of the four sister taxa pairs, indicating that there were three phases of radiation. The deepest split, pegged at 15 mya, was between the two trunk-crown species, A. evermanni and A. stratulus. At 10 mya, two pairs split simultaneously, the aforementioned one above and the two trunk-ground species, A. cooki and A. cristatellus. Both of these pairs include one species that occurs in the xeric southwestern portion of Puerto Rico, perhaps not a coincidence? Finally, 5 mya, the two grass-bush species, A. pulchellus and A. krugi diverged. These latter two species have recently been shown to hybridize, and McElroy’s data confirms that this is the only one of the four pairs in which hybridization occurs, perhaps due to their recency of divergence?

This is a fabulous example of detailed phylogenetic work spanning both interspecific comparisons and including the extensive degree of phylogeographic divergence that occurs within many anole species. More work of this sort is needed on anoles on the other three islands of the Greater Antilles. The monophyletic Jamaican radiation would be a good starting point.