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When Does Sexual Dimorphism Arise in Crown-Giant Anoles?

Size dimorphism among Anolis habitat specialists from Butler et al. 2003

In recent years the Anolis community has shown greater interest in understanding the developmental bases of anole diversity. As these data accumulate, we can start to synthetically understand the ecological (ultimate) and developmental (proximate) factors that regulated different aspects of anatomical diversification in anoles. Differences between males and females (i.e., sexual dimorphism) is one area that has received a considerable amount of attention among anole biologists interested in obtaining this integrative understanding of anatomical diversity. Over the last decade a number of papers have been published examining the evolutionary patterns of anatomical differences, ecological correlations, and the developmental/physiological processes underlying dimorphism in anoles.

Variation in body proportion (i.e., shape dimorphism) among Anolis habitat specialists from Butler et al 2003.

Compared to other anoles, crown-giant anoles have relatively low levels of size dimorphism, but vary greatly in body proportion. Males and females tend to vary in relative limb length, head proportions, and in the dimensions of their adhesive toe pads. In a recently published paper Vanhooydonck et al. examine the timing of divergence between male and female A. baracoae. They raised 23 individuals (9 males, 14 females) for 3.5 years, repeatedly measuring three anatomical traits and bite force 11 times over this time period. The authors found that bite force and dewlap size exhibit significant differences in growth between the sexes. Their analysis further suggests that these traits diverge at different times during ontogeny – bite force diverges during juvenile growth while dewlap size does not diverge until sexual maturity – illustrating the independent regulation of dimorphic traits during development. Head length and hindlimb length did not appear to have sexual differences, although it would be interesting to also perform a formal analysis of adult size and shape dimorphism on A. baracoae to see if this species has similar dimorphic trends compared to other crown-giant anoles.

The developmental bases of size dimorphism in A. sagrei from Cox et al. 2009

These results are consistent with other studies that show a mosaic pattern of male and female phenotypic divergence. Using a longitudinal study of male and female A. sagrei, Cox et al. 2009 showed us that body size dimorphism in this species begins early in juvenile life, only three weeks after hatching. Sanger et al. showed that dimorphism in facial length can emerge through two distinct developmental strategies, one early in ontogeny and one at the time of sexual maturity that appears to be clade-specific. Additional research on that compares across traits and among species will further elucidate the number of ways that dimorphism can arise in anoles. Further work that overlays an ecological perspective onto these patterns will also allow a more thorough understanding of whether natural or sexual selection is the primary driver of these differences in timing. As this future work progresses new insights into the evolutionary processes of anatomical diversification are sure to follow.

Climate as a driver of tropical insular diversity

A male Red-eyed Coquí (Eleutherodactylus antillensis) courting a female coqui in St. Thomas, U.S. Virgin Islands.

A male Red-eyed Coquí (Eleutherodactylus antillensis) courting a female coqui in St. Thomas, U.S. Virgin Islands. Photo by Brittany Barker.

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A Mountain Coqui (Eleutherodactylus portoricensis) at El Yunque National Forest, Puerto Rico. Photo by Alejandro Ríos-Franceschi.

Contemporary climatic change is affecting species distributions, with important consequences for the long-term persistence and evolutionary potential of biodiversity. Endemic species on small, isolated islands are often particularly vulnerable to environmental change due to their restricted distributions and modest population sizes. Exploring how island biotas have responded to past climatic conditions may yield insights into their potential responses to changing conditions.

In our study recently published in Ecography, we sought to extend current knowledge on the role of late Quaternary climate in shaping distributions, diversification, and speciation dynamics in tropical islands. We conducted the study on two ecologically distinctive Eleutherodactylus frogs in Puerto Rico, the smallest and most easterly of the Greater Antilles. Whereas the mountain coquí (Eleutherodactylus portoricensis) is restricted to cool and moist understory montane forest habitat in Puerto Rico, the red-eyed coquí (E. antillensis) is a habitat generalist with a broad elevational distribution on most of the larger islands of the archipelago. We used ecological niche models under past and current climate to derive hypotheses regarding how stable climatic conditions shaped genetic diversity in E. portoricensis and E. antillensis. To test our hypotheses, we conducted phylogeographic and population genetic analyses based on mitochondrial and nuclear loci of each species across their range in Puerto Rico.

As predicted, regions with a large area of long-term suitable climate were associated with higher genetic diversity in E. portoricensis and E. antillensis, suggesting larger and more stable populations. Long-term unsuitable climatic conditions in the Río Grande de Loíza Basin, a warm and arid landscape that physiographically separates the Central and Luquillo Mountains of Puerto Rico, is a barrier to gene flow between populations of both species. These results are consistent with a previous study that suggested that temporally stable climatic conditions promote the accumulation of genetic diversity in the Puerto Rican lizard Anolis krugi.

Our findings illustrate the role of persistent suitable climatic conditions in promoting the persistence and diversification of tropical island organisms. The rate of climate change we’re experiencing now is faster than at any time in the last millennium, which highlights the urgency of understanding how small, isolated island endemic species respond to environmental change.

 

Brittany S. Barker

University of Arizona, Department of Ecology and Evolutionary Biology

Do Gray-Dewlapped Green Anoles Display Differently than Pink-Dewlapped Greens?

The gray-dewlapped green anole. Photo by Harry W. Greene

Everyone knows that Florida green anoles have pink dewlaps. However, one population in western Florida has a grayish-green dewlap (see above). Several years ago, AA had two posts on these lizards (1,2). The significance of the gray dewlap remains to be determined. Is this population on the way to becoming a new species?

In a recent paper in Herpetologica, Macedonia and colleagues analyzed the display behavior of the gray-dewlapped population. They found that the gray-dewlappers’ display does differ, though not greatly, from a nearby pink-dewlapped population. However, when they compared their data to yet another pink-dewlapped population, they found that there was greater variation in the displays of the two pink populations than between the gray and pink populations. Thus, it doesn’t seem that the gray-dewlapped population’s behavior is particularly distinctive. What’s up with the gray dewlaps remains to be determined.

Here’s the paper’s abstract:

Green Anoles (Anolis carolinensis) are comprised of red-dewlapped (RD) forms that are found throughout the southeastern USA and a gray-dewlapped (GD) form that is restricted to southwest Florida. Prior research has shown that RD A. carolinensis produce headbob displays of three distinct types that differ primarily in their temporal patterns. Based on known morphological, physiological, and genetic differences between GD and RDpopulations, we hypothesized that these populations also would differ in headbob display structure. To test this hypothesis we quantified 440 displays from 39 males (24 GD and 15 RD) and assigned displays to type using numerical decision criteria. Although comparison of the same display types between GD and RD males revealed differences in the durations of several homologous display units (i.e., bobs or interbob pauses), only one unit differed following statistical correction for multiple comparisons. By taking into account all display variation in both populations simultaneously, however, discriminant function analysis correctly assigned display units with high accuracy to population and display type. Nevertheless, differences in unit durations often were greater between two RD populations occurring within Florida than they were between our GD and RD study populations. Thus, despite our demonstration of differences in the display temporal structure between GD and RD forms of A. carolinensis, these differences appear to be no greater in magnitude than those observed between RD populations.

What Will Happen When This Mean Brown Anole Gets to the Sickly Green Anole?

Photo by Karen Cusick

Karen Cusick recounts this scary encounter on Daffodil’s Photo Blog.  The green turned around, to face its impending doom head on.

Photo by Karen Cusick

And then….

Predation on Puerto Rican Lizards

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In a recent paper in Life: the Excitement of Biology, Ríos-López et al. report observations of predation on a variety of Puerto Rican lizards. Iguanas and Ameiva suffer much of the brunt of predation (including a beagle with a juvenile iguana in its mouth), but reports include A. cristatellus eating both A. pulchellus and A. stratulus (which was subsequently regurgitated–perhaps because it was too large?–and immediately devoured by an Ameiva that ran up to the fallen carcass). In addition, a tody (above) brought an anole back to its nest.

cristatellus

Glow-in-the-Dark Dewlaps Allow Lizards to Be Seen in Dim Light

Leo Fleishman and colleagues have just published a cool paper in Functional Ecology, “Why do Anolis dewlaps glow? An analysis of a translucent visual signal.” Co-author Manuel Leal provides the back-story on how the paper–which he refers to as “experimental natural history”–came to be in his lab’s blog, Chipojo lab.

And the New Scientist provides a nice summary of the article in its post: ”

Luminous lizard lotharios ahoy! In the dark undergrowth of the forest, it’s not easy to be seen. Male Anolis lizards use colourful throat fans, called dewlaps, to woo females as well as ward off rivals and predators. But one species has a neat trick to make itself stand out even more – it uses an optical illusion to make its dewlap appear to glow.

The dewlaps are translucent, which means they can transmit as well as reflect light. However, because most objects in the lizards’ environment – such as rocks and tree trunks – simply reflect light, our eyes “expect” them all to appear relatively dull. By transmitting light from the background, the dewlap tricks our eyes – and the eyes of other lizards – into thinking it is actually a light source, says Leo J. Fleishman of Union College in Schenectady, New York, who has studied the lizards for years.

Fleishman’s team was curious to find out why the trick evolved – was the glowing dewlap a way to increase contrast with darker backgrounds or a way to make its colour clearer?

To explore the issue, Fleishman’s team examined the photoreceptors in the lizard’s eyes to work out how they would view the dewlaps. They found that the glow did not create more contrast with the background, which naturally contains other bright spots – where a patch of sunlight passes through the vegetation, for instance. But the glow did significantly reduce the visual overlap, as the lizard’s eyes would experience it, between the throat fans and the colours of natural backgrounds.

The glowing dewlap may be more common than we think. Only a few of some 400 species of Anolis lizards are known to carry the trait, but Fleishman has seen photos suggesting other species’ dewlaps might glow too.

“My guess is that the phenomenon will turn out to be widespread once people start looking, but very few people have looked,” he says.

Here’s the paper’s summary:

Summary

  1. Male anoline lizards utilize a colourful, expandable throat fan, called the dewlap, to rapidly and unambiguously signal their presence and species identity to conspecifics. Under some viewing conditions, the dewlaps of some species appear to glow vividly, because they transmit a great deal of diffuse light, creating a translucent signal. Translucent signals are probably found in many animal groups, but they have rarely been studied.
  2. We hypothesized that dewlap translucence might (i) increase dewlap/background luminance contrast or (ii) increase the reliability of the colour as a species recognition signal by lowering the colour discrimination threshold in low light conditions such as forest shade.
  3. We calculated dewlap colour (spectral radiance) for the Jamaican lizard Anolis lineatopus at natural perch sites with, and without, the inclusion of transmitted light.
  4. Transmitted light did not significantly increase the magnitude of luminance contrast between the dewlap and background.
  5. We plotted colours of dewlaps, background patches of habitat and dewlaps of sympatric species in an anoline perceptual colour space (the colour tetrahedron), based on the four classes of cone photoreceptors found in the retina. Using a newly developed approach, we used ellipsoidal plots of uncertainty to quantify perceptual overlap between dewlap spectral radiance and values for natural distractor colours. Diffuse transmission of light through the dewlap greatly reduced the perceptual overlap between the dewlap and natural background colours.
  6. This finding strongly suggests that selection has favoured the evolution of a translucent dewlap as a mechanism to increase the reliability of detection of the signal under the low light conditions. In general, any animal’s colour signal must emit sufficient light intensity to allow the colour to be discriminated from other distractor colours in the habitat. This will tend to favour the evolution of colours with higher total intensity (i.e. higher reflectance and/or transmittance) in animals that signal in relatively low light conditions such as forest shade.

 

 

Anolis sagrei on Rum Cay, Bahamas

Anthony and Kevin near the golf cart. This inland forest was the tallest we could get access to on the island.

Anthony and Kevin near the golf cart. This inland forest was the tallest we could get access to on the island.

A July trip to the Bahamas to sample Anolis sagrei has been documented in recent posts by Graham Reynolds and Kevin Aviles-Rodriguez. During that trip, Kevin, Anthony Geneva, and I traveled to the island of Rum Cay to collect data on anoles. With a human population of fewer than 50 clustered in an around the southeastern town of Port Nelson, Rum Cay is mostly uninhabited. Access to a majority of the island’s 30 square miles is facilitated by narrow dirt roads, several of which, particularly those on the western half of the island, are overgrown and unnavigable. Our golf cart, well-equipped with off-road tires, was pushed to its limits as we strove to find lizards across several habitat types on the island.

L. loxogrammus on Rum Cay. Photo by Anthony Geneva.

L. loxogrammus on Rum Cay. Photo by Anthony Geneva.

Anolis sagrei was abundant among most of the island’s vegetation including forests, mangroves, and beach scrub. Their mostly red dewlaps appear similar to those we saw on nearby Long Island. In each habitat, the lizards were usually perched within 1 meter of the ground but were occasionally found on the ground or perched higher than 1 meter. One exception was a shrubby forest located at (23.66501, -74.868245) which contained abundant A. sagrei along with incredibly high densities of the San Salvador curlytail lizard, Leiocephalus loxogrammus. Here we didn’t see any A. sagrei on the ground despite being present at the site for several hours on two separate days. Not an easy place to get to, but it would be a great site for studying curlytail behavior and interactions between curlytails and anoles. In our adventures we also encountered several Anolis distichus, with more on that to come in a later post.

A Salamander in Amber from the Dominican Republic

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It’s been a good couple of weeks for herps-in-amber fans. Last week, Emma Sherratt and colleagues (including me) published a paper expanding the number of known Dominican amber anoles from 3 to 38. And now comes a paper by Poinar and Wake in the journal Palaeodiversity reporting a finding perhaps even more improbable: a fossil salamander in amber from the Dominican Republic.

What is so remarkable about this discovery is that salamanders do not occur anywhere in the Caribbean today. Indeed, salamanders are one of the textbook examples of taxa thought to be unable to disperse overwater, leading to what used to be called “disharmonic faunas”–islands that are missing some elements normally found on the mainland.

Detailed analysis indicates that the specimen is a member of the Plethodontidae, the family to which all neotropical salamanders belong. How did it get to Hispaniola? One possibility is that it hopped onto the proto-Antillean landmass as it passed by and perhaps came into contact with the continental Americas around 70 million years ago. Some hold that anoles got to the islands in the same way, though molecular data suggest that anoles are too young for vicariance to explain their occurrence in the Caribbean. The alternative possibility is that salamanders got to islands the old-fashioned way, by floating on flotsam and jetsam. Sensitive to dessication, most amphibians–and plethodontids in particular–wouldn’t seem good candidates for overwater dispersal, but stranger things have happened.

Regardless of how they got there, the presence of salamanders in the Caribbean twenty million years ago is a surprising finding adding a new dimension to our understanding of Caribbean biogeography.

Land Hermit Crabs Congregate on Anoles’ Sleeping Perches

Recently I was on Long Island alongside Graham and his team capturing Anolis sagrei. For our last night survey, we collected female lizards from a beach scrub habitat in McKanns (23.38831, -75.1408). During such a survey, we used headlamps to search for sleeping lizards perched on branches and leaves. At other sites we frequently found lizards on vegetation along the trails. At McKanns, land hermit crabs (Coenobita spp.) were congregated in high numbers on such vegetation. We seldom found lizards perching on plants where hermit crabs congregated.

Photo by Alberto Puente

Land hermit crabs (Coenobita spp.) active at night.  Photo by Alberto Puente

Most lizards perched further away from the trail on the broad leaves of Cocoloba uvifera where hermit crabs were seen less abundantly. Perhaps due to their large numbers and the fact that they were active at night, land hermit crabs might be occupying perches that would otherwise be used by Anolis sagrei.

 

Anoles Talks at SSAR 2015

A little while ago, Alexis Harrison asked why there were so few anole talks at the ASIH meeting in Reno. Now we know the reason–they’re all at the SSAR meeting in Lawrence, Kansas, which began today. In total, there are 13 anole presentations (talks plus posters). You can find them in the Meeting Program (also available at meeting website)–just search for “anol”  (11) or “Norops” (2).

At the moment, we have no one lined up to provide first-hand reports from the meeting. If any readers out there are at the meeting and want to report in, we’d very much appreciate it!

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