Sex Chromosomes Conserved Across Anoles and Beyond

Cusick_FL_carolinensis_3 matingThough temperature-dependent sex determination is one of the most interesting things about reptiles, this mode of sex determination unfortunately does not extend to anoles. In iguanid lizards, sex determination has long be known to be a consequence of sex chromosomes, males being the heterogametic (XY) sex.

Reptilian sex chromosomes occupy a strange middle ground within vertebrates: on one hand, amphibian and fish sex chromosomes are marked by rapid turnover in precisely which chromosomes determine sex ; on the other hand, bird and mammal sex chromosomes are characterized by their stability over millions of years.  In an early-view paper in Evolution, Rovatsos et al(2014)  show that sex chromosomes are stable in at least some reptiles–in anoles, they have been conserved since before the diversification of the genus. 

The authors began by picking five X-linked and three autosomal genes from the recently published Anolis carolinensis genome, and use quantitative PCR to confirm that the X-linked but not the autosomal genes have double the gene dosage values in female vs. male A. carolinensis. Next, they extend their sequencing efforts to seventeen other species from across Anolis as well as three species of phrynosomatid lizards. Remarkably, similar patterns of gene dosage differences between males and females are seen across the sampled taxa, suggesting that the same genes are X-linked in all these species. This result implies the stability of the X-chromosome for at least 70 million years, pre-dating the divergence of Dactyloidae and Phrynosomatidae.

This finding puts a dent in a long standing hypothesis for why birds and mammals have stable sex chromosomes–their stability was attributed to “the lower susceptibility of homoiotermic endothermic vertebrates (mammals and birds) to thermally-induced sex reversals due to their effective thermoregulation.” Rovatsos et al. (2014) call for new explanations for “why some vertebrate lineages possess frequent turnovers of poorly differentiated sex chromosomes, while others show a long-term stability of sex chromosomes connected with their progressive differentiation,” explanations that must take into account the stability of sex chromosomes across anoles and potentially across all iguanian lizards.

Are Bark Anoles (Anolis distichus) Native to Abaco Island, Bahamas?

Bark anole, A. distichus

Bark anole, A. distichus

I’ve been working on Abaco, in The Bahamas for several years now. The Bahamas, Abaco in particular, is famous for the abundance of terrific science that originates there. Currently, Abaco has three species of anole: A. sagrei, A. smaragdinus, and A. distichus. However, only A. sagrei has been considered native to the island, the others likely introduced relatively recently from islands of the Great Bahama bank such as New Providence or Bimini. However, a recent study reports fossil evidence of A. distichus in peat deposits from about 950 YBP supporting a long history of A. distichus on Abaco.

One interesting aspect of this find is that the contemporary distribution of A. distichus on Abaco appears to be limited to the main port town of Marsh Harbour. I always suspected that this limited distribution suggested that A. distichus was not native to the island, but rather came in on landscaping plants over the last several decades.

So why are there conflicting observations here? Is it possible that A. distichus was extirpated on Abaco due to settlement by indigenous peoples (seems to be contemporaneous with the fossil sediment formation)?  While it might seems rather hard to extirpate such a small, abundant animal, there is growing evidence that the Bahamas were reptile-dominated ecosystems at the time of human arrival. Therefore, the coincident extirpation of tortoises, Cuban crocodiles, and rock iguanas places the modern hiatus of A. distichus in a different light. I am guessing that the altered (intensified) fire regimes initiated by ancient human civilizations may have contributed to the absence (rarity) of A. distichus from contemporary, natural ecosystems. This is admittedly, a lot of conjecture, but how else might one explain their ancient presence, yet contemporary confinement to a human-dominated habitat?

I look forward to hearing more from the interesting work that Dave Steadman, Janet Franklin and Nancy Albury are doing on these ancient Bahamas communities. And it looks like there is a lot more to come! Also, the name of the journal is The Holocene. How cool is that?!

Steadman DW, NA Albury, P Maillis, JI Mead, J Slapcinsky, KL Krysko, HM Singleton, and J Franklin. 2014. Late-Holocene faunal and landscape change in the Bahamas. The Holocene. DOI: 10.1177/0959683613516819.

 

 

 

 

The Reptiles and Amphibians of Mindo, Ecuador: New Book

The team at Tropical Herping has done it again! This time, a fabulous, lavish, luscious, information-packed guide to the spectacular herpetofauna of Mindo Parish, Ecuador. Originally available online, the book is now available in print. I had the privilege of writing the foreword, appended below. More information is available on the TH website, as well as an order form.

Foreword:

Small in size, but a global giant in biodiversity, Ecuador is awash in all manner of fauna and flora. Birds, butterflies, trees—the country is a hotspot for just about everything. But no group of organisms is more beautiful, more charismatic, more scientifically captivating than Ecuador’s reptiles and amphibians. The Amazon rainforest dominates the attention of the public, but other parts of the country, especially the mountainous regions, are just as biologically rich. One such area is the small parish of Mindo in Pichincha Province, home to 102 species of creepy crawlies. And what an ensemble! Brilliant colors, toxic skin and venom, sweet serenades, menacing looks, gorgeous displays—this region is an encyclopedia of herpetology in just 268 square kilometers.

Field guides play an essential role in making the fauna and flora of an area widely accessible. They are at the front line of nature education and conservation, the place where the fruits of scientific exploration are distilled, synthesized, packaged, and presented to the public at large. Since the time of Roger Tory Peterson, field guides have played another role, being a venue for beautiful, yet accurate, scientific illustration, allowing readers to not only understand the identifying marks of each species, but also to appreciate them esthetically.

Despite its bountiful herpetofauna, until now no field guides existed for Ecuador’s amphibians and Reptiles. The Tropical Herping team has brilliantly stepped into this void, producing a guide to the herps of Mindo that hopefully will serve both as a model of how guides should be produced and an inspiration to the production of similar efforts elsewhere in Ecuador and beyond. The Amphibians and Reptiles of Mindo is particularly notable in three respects. First is the breadth and depth of information provided for each of Mindo’s species. These authors know their fauna in exquisite detail and have synthesized that knowledge in a clear and lucid manner. The inclusion of frog calls, recorded by the authors themselves, is an added bonus bridging the paper and digital eras. Second, the public often does not understand the connection between scientific research and the information presented in field guides, magazine articles and nature documentaries. Unlike most field guides, The Amphibians and Reptiles of Mindo makes this link crystal clear, providing citations so that readers know where to turn to learn more. Indeed, especially impressive is the fact that the authors did a great deal of field work themselves to round out knowledge of these species, presenting that information for the first time here. Finally, third, the book is simply beautiful. The photographs are simply stunning and the maps and other illustrations lovely as well.

The publication of The Amphibians and Reptiles of Mindo could not come at a better time. The Mindo region is a microcosm for all that ails the natural world. Deforestation, habitat fragmentation, pollution, overharvesting—all are threats. Mindo has one thing going for in its favor—it has become a nature vacation travel destination, providing jobs and economic rationale for preserving natural habitats. But, ecotourism can be a two-edged sword, as people and development are drawn to the area with potentially negative consequences. Mindo has the opportunity to show how responsible stewardship can be mutually beneficial to man and nature, and this lovely book shows what is at stake. Three cheers for the three authors of this magnificent volume. Long live the herpetofauna of Mindo!

Genetic Differentiation in the Beach Anole, Anolis onca, in Venezuela

DSC_0010x

Everyone’s favorite beach anole, A. onca. Photo by J. Losos

Anolis onca, the only padless anole, occurs in sandy habitats in Venezuela. Little is known about the evolutionary history of this quite distinctive species (we had a discussion of its natural history last year [1,2]).

Now a recent paper appears in the journal Saber  in which a team of Venezuelan scientists led by Alejandra Tejada used starch gel electrophoresis methods to measure the degree of genetic differentiation among populations. The paper can be downloaded, albeit a bit slowly, and is in Spanish, but here’s the English summary:

Anolis onca is a lizard species located in the Araya peninsula, in northern Venezuela. Populations of this species may have been isolated in the late Cretaceous and later recombined during the Quaternary through a new isthmus by sedimentary processes. To test this assumption, in five populations of A. onca, starch gel electrophoresis was used to estimate genetic variability within populations, interpopulation differentiation (FST), and gene flow (Nem). Additionally, under the premise of genetic differentiation between subpopulations under the isolation by distance (IBD) model, we conducted a phylogenetic analysis for five subpopulations of this lizard. Increases of genetic distance values (D) between subpopulations arranged consecutively between the Chacopata and Guayacán locations and a clear structuration as estimated by the FST parameter, evidence isolation by distance as indicated by the IBD model. However, Nem values did not conform to this model, suggesting that the subpopulations, although actually connected, may have been shaped by independent evolutionary processes. The two clades resulting from the phylogenetic analysis do not group populations closer geographically since clade B (Chacopata+Istmo Sur) lies in areas geologically ancient whereas clade A [(Istmo Centro+Istmo Norte)+Guayacán)] occupies areas of recent sedimentary origin. It is thus reasonable to infer that other factors besides the geographical distance between subpopulations may have also conditioned the structure found.

 

Orange Coloration in Anolis cristatellus

A couple of days ago as I was feeding my Anolis cristatellus hatchlings and I noticed something really strange – one of the hatchlings had a bright pink/orange tail!  I was really amazed at how bright and unusual it was so I immediately emailed Ambika Kamath who pointed out that this conversation is not a new one to Anole Annals and suggested I post on my anomalous pink lizard.

2014-01-17 13.22.20

The pink-orange color is only on the tail and hind limbs and when I picked the lizard up the color faded as the lizard turned darker brown. The mother was unremarkable (not pink!), but one of the siblings also has some reddish tint to its tail, although not as apparent. I have not noticed this in any of my other hatchlings.

I’m curious if this is the same sort of coloration that other people have observed in Anolis sagrei. Some of the pictures look very similar to what I observed. Has anyone else observed this in A. cristatellus or any other species? Or maybe this sometimes happens in hatchlings and fades with age? For reference, here are the previous posts on Anole Annals regarding this topic:

It might be noteworthy that the hatchling is the offspring of two urban lizards from Mayaguez, Puerto Rico.  In the other posts, it seemed like many of the observations of the red-orange A. sagrei were in urban areas. One of the posts mentions an orange color of palm trees and other manmade substrates in the suburban area where they observed multiple orange lizards. I wonder if this is an adaptation to something in the urban environment? Now that I think of it, I recall catching some lizards at my urban sites that had striking orange coloration on them, but none were completely orange and none looked pink. Also, I don’t recall my study site having a large amount of orange substrates, although many of the houses are painted bright orange, yellow, pink, etc. Any thoughts on this?  I’ll keep an eye on this lizard and let you know how the color develops as it gets older.

2014-01-15 15.58.19

Mystery Growth on Anolis smaragdinus

In the course of our research on  small-island populations of A. smaragdinus (A. carolinensis series) in the Bahamas, we’ve encountered a number of animals with mysterious lumps. These are sometimes quite conspicuous, as in the photo below. The question is, what are they? Tumors? Parasites? Has anyone encountered something similar?

Photo by Rowan Barrett.

Photo by Rowan Barrett.

The growths do not appear to be restricted to any particular part of the body — we’ve also observed them on the base of tails and on limbs. The lizards in question are currently distributed across several islands, but all are descendants of small founding populations (10 individuals) originating on Staniel Cay. Eager for any insights from the anole community! (Rank speculation is also welcome.)

SICB 2014: Testosterone Regulation of Multiple Traits


Anolis sagrei has impressive sexual size dimorphism, but what causes it? (Photo by Bob Reed)

Sexual dimorphism is always a hot topic at SICB, and this year it was no exception for anoles (1, 2). Christian Cox, a postdoc in the laboratory of Bob Cox (no relation) at the University of Virginia, sought to explain how testosterone might lead to phenotypic divergence in a number of sexually dimorphic traits. As many of us are aware, sexual dimorphism varies widely among lizard species, and evolutionary shifts to and away from dimorphism are common, including in anoles. Testosterone has been shown to be an important regulator of growth in several lizard species, so Cox experimentally tested this effect in Anolis sagrei.

Both males and females were given a testosterone or blank implant and allowed to grow to maturation. One group was manipulated as juveniles, just as phenotypic divergence was beginning, and the other group was manipulated as subadults after divergence. Testosterone addition increased growth in body size and mass, increased metabolic rate, increased dewlap size, and changed dewlap coloration in both sexes and both juveniles and subadults. Fat storage was reduced as expected, in both sexes and age classes. These results are intriguing, because a sex difference in testosterone production may play a role in the degradation of between-sex genetic correlations. The next question is how that happens, as both sexes produce testosterone, just to different extents.

Is Living in Urban Areas an Acquired Taste?

IMG_1443We all know that some of our favorite anole species are abundant in urban settings, yet many others are not. Why is this? Do species have to evolve and adapt to city living? Maybe not. In what may be a surprising preliminary analysis, Kristin Winchell over on her blog Adaptability suggests that Caribbean anoles ancestrally had what it takes to live in human settings, and not being able to do so is an evolutionarily derived trait. Sounds crazy at first, right? Until you remember that anoles colonized these islands over water, and so to be successful, had to be flexible and able to cope with whatever life through at them–including, apparently, concrete sidewalks, trashcans, cars, and cats. Check out the details on Kristin’s post.

Functional Genomics Comes to Anolis Lizards

One of the major experimental advances in recent decades has been the battery of methods capable of functionally validating hypotheses regarding the molecular networks that regulate biological processes. For biologists, these emerging methods allow us to move beyond descriptive and correlational studies to new dimensions where we can experimentally validate our observations. Until recently these technologies were, by and large, reserved for the most well developed laboratory model systems (e.g., mouse, chicken, zebrafish, Drosophila), systems that rarely have direct utility to ecologists and evolutionary biologists. But the topography of biology is changing. These methods are rapidly becoming more easily applied to non-model systems, such as our favorite genus Anolis. In an upcoming paper from the Menke Lab, the tools of functional genomics are applied to anole limb development, taking another step towards making Anolis a truly integrative model system.

 

In situ hybridization showing expression of of early limb genes in A. sagrei.

In situ hybridization showing expression of of early limb genes in A. sagrei.

Park et al. describe a micromass culture system to explore the molecular regulation of anole limb morphogenesis. In their protocol, Park et al. collect cells from early limb buds of A. sagrei, dissociate the cells from one another, and then add them to a dish as a small (i.e., micro) bolus (i.e., mass) of cells with the appropriate growth media. Even when removed from the embryo, these cells maintain the characteristics of limb cells, developing cartilage after about two weeks and maintaining their molecular signature for at least eight days. This small mass of cells can be grown for up to 30 days and, therefore, provide a useful template for experimental manipulations. More details of this protocol are described in great detail in the paper. Compared to other technologies which require far greater investment, their protocol should be accessible to anyone with access to a tissue-culture laboratory.

Anolis is an emerging model of limb development, but previous studies have focused on describing morphometric patterns of limb growth, not the molecular regulation of limb development. In fact, there have been no studies systematically dissecting the molecular regulation of limb development in any squamate species despite broad interest in this topic in the laboratory mouse and chick systems for 40 years. To study the molecular mechanisms regulating limb morphogenesis, Park et al. forced the expression of the gene Pitx1 – a hindlimb-specific molecule in mouse and chick – in micromass cultures derived from both forelimb and hindlimbs. This experiment verified that one step of the limb regulatory network, the relationship between Pitx1 and Hoxc11, is likely conserved among amniote lineages. While at this time this  may have been a proof of principal experiment, this protocol may have future implications for both developmental and evolutionary research in Anolis. For example, multiple transgenes can be readily cloned and incorporated into the micromass cultures. In addition, micromass cultures derived from species with distinct limb morphologies may also open to door to finding pathways that are regulated in novel ways across Anolis lizards.

Park et al. Figure 4

Binding domains of Pitx1 in the intergenic region of Hoxc11. Note conservation of binding region throughout mammals (shaded arrows), but lack of conservation among amniotes (white arrows).

SICB 2014: Phenotypic Selection in Anolis sagrei

Numerous variables can affect an organism’s survival, including its age and sex, the demographics of the population in which it resides, and environmental conditions like climate, and habitat. However, the relative importance of these factors is poorly understood. Dan Warner described his investigation into factors affecting natural selection in wild populations of anoles in his talk titled, “Spatial and temporal variation in phenotypic selection in the lizard Anolis sagrei.”

A sagreiWarner measured directional selection on A. sagrei on six islands in the Matanzas National Estuarine Reserve in Florida. These islands were intentionally founded with populations having unequal adult sex ratios. Half of the islands were founded with more males than females (male-biased), and the other islands received more females than males (female-biased). This manipulation was done to strengthen the effects of male-male competition on the male-biased islands. Warner measured survival selection on adult and juvenile body size by marking and recapturing individuals over the last three years.

Warner found a lot of variation in the strength of directional selection on adult and juvenile body size both across islands and within each island in different years. However, there was no relationship between the strength of selection on each island and either habitat structure (represented by canopy openness) or island size. Thus, the probability of survival at a particular body size does not seem to depend on environment.

However, population demographics did seem to affect survival at different body sizes. There was a negative correlation between the strength of selection on body size and the density of adult lizards, indicating that smaller body sizes are favored at high population densities (and vice versa). This trend was observed in both adults and juveniles, but was more pronounced in juveniles. Warner hypothesized that it was the density of adult males in particular, rather than the total density of adults, that was driving the observed trend. To test this idea, he tested for a correlation between the strength of selection on juvenile body size and the adult sex ratio. He found a negative correlation, indicating that large juveniles are favored in more female-biased populations while small juveniles do better in male-biased populations. One possible explanation is that on islands with male-biased sex ratios, large juveniles are more likely to come into contact with territorial adult males, are more likely to be perceived by these males as a possible competitor, and are therefore more likely to be harassed by these males. The presence of adult males might even reduce recruitment, as evidenced by slower population growth rates on male-biased versus female-biased islands.

These results suggest that patterns of natural selection on individuals can depend on characteristics of the population. Only with long-term field studies such as this one can we begin to unravel the many factors affecting selection in wild populations.

Page 168 of 300

Powered by WordPress & Theme by Anders Norén