Anole Annals

Shea Lambert and colleagues have just published a fabulous paper in Molecular Ecology on dewlap color evolution and reproductive character displacement in species in the Anolis brevirostris species complex. Manuel Leal and I wrote a perspective piece accompanying the paper that goes something like this:

‘Sibling species’, an old term that has fallen out of use, refers to closely related species that are so similar that it is hard to tell them apart. The existence of such species raises the obvious question: How do the animals themselves tell one another apart? And indeed, this is an active area of research (Tibbetts & Dale 2007; Uy et al. 2009). Usually, the species differ in one or more traits (i.e. species recognition signals) detectable with the sensory modalities upon which they rely (e.g. raptors use visual signals, frogs use sound and electric fish use different patterns of electric discharge).

A more general question concerns how such differences evolve. Over the last decade, it has become increasingly evident that mating signals can evolve under simultaneous selection for two functions (Fleishman et al. 2009): (i) eliciting attention (i.e. detectability); and (ii) species identification (i.e. distinguishing conspecifics from non-conspecifics). Historically, species recognition has attracted a significant amount of research from evolutionary biologists based on the assumption that if hybrids suffer reduced fitness or cannot be produced at all, then natural selection should favour individuals bearing traits that prevent such matings. This idea—confusingly termed either reinforcement or reproductive character displacement—had a rocky time in the evolutionary literature for many years, though now it is widely accepted (Servedio & Noor 2003; Rundle and Nosil, 2005; Pfennig & Pfennig 2009).

Near the dawn of the era of molecular ecology, one of the first studies to employ molecular tools to study the evolution of species recognition signals was Webster & Burns’ (1973) study of the evolution of dewlap colour in Anolis lizards. Anoles possess a retractable flap of skin under the throat, termed as dewlap, that is used in courtship, aggressive interactions and even encounters with predators (reviewed in Losos 2009). Anoles can be found in communities of as many as 15 species, and sympatric species never have identical dewlaps, leading to the hypothesis that the dewlap is used in species identification (Rand & Williams 1970).

Webster and Burns studied a highly unusual pattern of dewlap distribution in the Hispaniolan bark anole, Anolis brevirostris, along a transect on the western coast of Haiti (Fig. 1, above). Starting in the south, the lizards have a white dewlap. Then, abruptly the dewlaps become intensely orange; moving northwards, the intensity and size of the orange spot diminishes until it has almost disappeared, whereupon again there is an abrupt transition back to intense orange coloration that characterizes the northernmost populations.

Using the tools of the day, Webster and Burns employed starch-gel electrophoresis to examine six geographically varying protein loci. Analysis of these data yielded three important discoveries. First, the populations sorted into three groups: the white-dewlapped forms in the south, the orange-dewlapped forms in the north and a third, intervening form that exhibited clinal variation in the proportion of white vs. orange in the dewlap. Second, at the point of contact between the groups in both the north and the south, adjacent populations did not share alleles at several loci. Third, within the middle, clinally varying group, populationsshowed little genetic differentiation despite the differences in dewlap colour among populations.

Webster and Burns concluded that they were dealing not with a single species, but three—subsequently, the middle populations were described as A. caudalis and the northern ones as A. websteri. More importantly, what had seemingly been an incoherent pattern of geographic variation in dewlap colour variation now had a clear explanation. The apposition of orange vs. white at both ends of A. caudalis’s range is most parsimoniously explained as the result of selection for differences in species recognition signals in sympatry. The fact that A. caudalis maintains the clinal variation in the face of possibly strong ongoing gene flow, as evidenced by the lack of genetic differentiation among populations, was interpreted as powerful evidence for ongoing natural selection favouring dewlap colour differences at the contact zones with the other species.

Given this provocative pattern and the great interest in evolutionary reinforcement, it is surprising that this example has not been subject to further investigation as molecular tools have developed over the past four decades. Undoubtedly, the transect’s occurrence in Haiti, a notoriously difficult place for fieldwork, has been a factor. Finally, however, this case study has come under further scrutiny.

On a trip in Haiti that was no doubt a story in itself, Lambert et al. revisited Webster and Burns’ transect and report in this issue of Molecular Ecology the results of their phylogenetic and phenotypic analyses. Examining variation at mitochondrial and nuclear loci, Lambert et al. have demonstrated that Webster and Burns pretty much got it exactly right. Chalk one up for old school electrophoresis! Not only do the three species each fall out as monophyletic, but, as with the allozymes, A. caudalis exhibits little interpopulation genetic differentiation, in contrast to the deep genetic structure apparent among populations in the other two species. Moreover, phenotypic examination of dewlap coloration reaffirmed the patterns of clinal variation within A. caudalis and the abrupt shifts in coloration between sympatric species at either end of its range (Fig. 2).

Lambert et al.’s study not only completely corroborates Webster and Burns’ conclusions, but adds several important new perspectives on this case study.

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Ray Huey giving the first talk of the symposium, illustrating that present day temperatures are more suitable for A. cristatellus than A. gundlachi at the El Verde Field Station (the red circles show average temperature through the day now; the gray circles are for corresponding temperatures 40 years ago).

This is part II of my report on the the symposium “The Biological Impacts of Tropical Climate Warming for Ectothermic Animals,” which was recently (Aug. 1-3) held in San Juan Puerto. Previously I discussed several of the talks that focused on anoles; today I summarize the rest of the symposium (the program is listed here).

Symposium co-organizer Ray Huey kicked off the symposium with opening remarks, including some important background. The symposium was funded as part of a grant headlined by Huey to investigate the effect of global warming on Puerto Rican reptiles. Huey joined forces with Paul Hertz, George Gorman, and Brad Lister, all of whom had studied Puerto Rican anoles in the 1960’s and 70’s. The goal of the proposal was to revisit their study sites to see how things had changed in the intervening time, as the climate had warmed, including as much as 2 degree  C at the El Verde Field Station. A particular species of focal interest was the forest interior montane anole, A. gundlachi. This species is adapted to low temperatures, whereas its close relative, A. cristatellus, thrives at warmer temperatures. Huey and colleagues speculated that as the forest warmed, it would become more suitable for cristatellus and less for gundlachi, resulting in a forest invasion by the former and the disappearance by gundlachi from lower elevation forests.

Imagine their surprise, then, when they found not only that cristatellus had made no inroads into the forest at El Verde, but that gundlachi, previously found only at higher elevations, could now be found at sea-level! Exactly the opposite of what had been predicted–what a conundrum!

Noted forest science Ariel Lugo explained this result clearly in the next talk. It turns out that Puerto Rico has experienced massive reforestation in the last 50 years. Consequently, even if the world is getting warmer, it is also getting more tree-covered, at least in Puerto Rico, and this latter effect has had a greater impact on gundlachi’s distribution, allowing it to occupy newly re-emerged forests at lower temperatures. An important lesson that warming is not the only thing going on in the world today and that we must consider other factors as well.

Barry Sinervo showing the grim news for lizard populations worldwide

Much of the rest of the day was pretty gloomy, with projections of massive ectotherm disappearance in the tropics as global temperatures rise (turtles, as well as lizards, as Barry Sinervo showed), the reason being that tropical species are often closer to their upper thermal limits, and so relatively small increases in temperature may push them over the edge. Michael Kearney’s talk was particularly notable in taking an extremely detailed mechanistic analysis of how increased temperatures affect all aspects of ectotherm biology through their entire life cycle. Such studies, though very elaborate, promise particularly rich insight into the specifics of how changing temperatures will affect ectotherms. One finding of particular interest is that the amount of shade available in a habitat will be critical: more shade = good; less shade = bad. In many cases, Kearney argued, it is not the warming per se, but the effect on vegetative cover that may be most significant in effecting species like lizards.

All of the talks were fascinating and I can’t discuss them all: a few particular points stick in my head: Mike Kaspari showing that the boundary layer of air around a surface is particularly important for small animals such as ants, that may experience temperatures as much as 10 degrees C higher than the air temperature a few centimers above the surface; symposium co-organizer Patricia Burrowes showing that changes in seasonality are extremely important, particularly with regard to host-pathogen dynamics; Carlos Navas discussing the relative importance of temperature and water availability for amphibians; Ana Carnival examining geographic patterns of genetic variation to understand responses to climate change in the past; and Brad Lister showing that anoles and almost everything else at his study site in the Luquillo Mountains have declined greatly in abundance in the last 40 years.

Have this many anole biologists ever been in the field together previously? And who are they? This photo was taken at the El Verde Field Station, site of James Stroud’s observations on rock-using canopy anoles.

Martha Munoz starting the all-anole morning with a comparison of the thermal niches of different species of Hispaniolan cybotoid anoles

The symposium “The Biological Impacts of Tropical Climate Warming for Ectothermic Animals,” was recently (Aug. 1-3) held in San Juan Puerto, and it was a great success. In a two-part post, I will provide a brief summary. Today will focus on four talks on the second morning, all of which focused on Anolis. In the next post, I will review the rest of the symposium.

Martha Muñoz began the day by talking about the thermal biology of cybotoid anoles (members of the cybotes species group) in Hispaniola. These species show a remarkable elevational range from sea level to over 3000 meters. Martha pointed out that in this respect, Hispaniola is a much better place to look at questions related to elevation than Puerto Rico, a comment greeted with jeering from much of the crowd. Nonetheless, she scoffed at the discussion of the “high elevation” A. gundlachi at 850 m. Why, A. shrevei, in Hispaniola doesn’t even occur that low! In any case, what Martha showed is that despite the great thermal differences in habitats at different elevations, the cybotoids maintained approximately the same body temperature at all sites and have the same preferred temperatures and critical thermal maxima. Clearly, they are using thermoregulatory behavior to buffer their thermal physiology from selection in different environments and, indeed, field observations show that high elevation species do bask more. However, anoles can’t thermoregulate at night, and there is where adaptive differentiation occurs: high elevation anoles can withstand lower temperatures than lower elevation species. To clinch the deal, Martha measured the temperatures lizards experience at night. Indeed, the species at high elevation experience temperatures that would kill low elevation species.

Luisa Otera showing a slide of her collaborator, George Gorman, in his cowboy salad days

Luisa Otera spoke next on the “Effects of recent climate warming on the reproductive phenology of Puerto Rican Anolis lizards.” Luisa revisited sites at which George Gorman had examined A. cristatellus 40 years ago. Gorman had found that at higher elevations, female reproduction tapered off in the winter, whereas at lower elevations, they continue reproducing year-round. Her prediction was that with higher temperatures, reproduction should be extended in the winter at high elevations. For the most part, this prediction was confirmed, though surprisingly not so at the sea-level site.

Most surprising, in a new twist, Luisa found that female reproduction could vary over a very short spatial scale. In particular, if a lizard has a territory in the open with a lot of sun, it can breed year round, whereas it’s neighbor under the shade of trees a few meters away may not be able to do so in the winter. Perhaps this explains the contrary finding at the sealevel sites: greater tree cover may have actually made conditions worse.

Luisa pointed out that warming isn’t always bad–for some lizards, it allows them to extend their breeding seasons

Gunderson’s data show that even lizards with body temperatures outside of their preferred range are still quite active

Alex Gunderson spoke next on “Behavioral responses to climate change: natural selection on the thermal physiology of Anolis sagrei.” Perceptive readers will note that these three talks focused sequentially on the trunk-ground anoles of three different islands. Coincidence? You be the judge. In any case, in a very thought-provoking talk, Alex pointed out that much of the literature predicting the response of species to global warming focuses on the effect that higher temperatures will have on the time in which lizards can be active, which affects factors like food acquisition. However, Gunderson note that although activity time is usually treated as a binary variable—a lizard is either active or it isn’t—his extremely detailed behavioral data (299 focal observations), indicate that, in fact, the effect of temperature on activity is continuous rather than binary. Indeed, lizards engage in all major activities—eating, mating, fighting—at temperatures substantially outside (mostly below) their “preferred temperatures.” This finding calls for a re-thinking of how we model the effects of climate change on lizard populations—they may be forced to be active at temperatures they’re not so happy about, but they will do more than stay in their hidey-holes.

Next, Michael Logan reprised his talk on the “Rapid evolution in response to climate change: natural selection on the thermal physiology of Anolis sagrei” which he gave at the Evolution meetings five weeks previously. But here he had twice as much time to speak and correspondingly gave greater details. Since I’ve reported on the talk previously, I’ll just summarize here: in a very cool experiment, he moved brown anoles from a shady habitat to a much hotter one. Before doing so, he measured the performance curves of each lizard (i.e., how their ability to sprint was affected by temperature). His prediction was that individuals that could sprint at higher temperatures would be favored by natural selection in the new habitat. And sure enough, they were! By contrast, another population in a shaded habitat experienced no selection on thermal performance. If thermal sensitivity of sprinting is a heritable trait—a big if, Mike noted—this strong selection could suggest that populations might be able to adapt very rapidly to warming climates.

Monogamy, or the formation of stable pair bonds between males and females for reproductive purposes, is thought to be relatively rare across animals. While social pair formation is observed (commonly in birds and occasionally in reptiles), genetic assessments of parentage have revealed that mating fidelity is infrequent. Social monogamy is therefore not equivalent to genetic monogamy. However, the reasons for the persistence of social monogamy despite promiscuous mating remain unclear.

Sleepy lizards are the best known example of pair-bonding in lizards (photo by J. Todd Kemper)

A new paper by Alexis Harrison revisits one of the only examples of social pair-bonding known from anoles–a population of Anolis limifrons in the La Selva Biological Station in Costa Rica. While most anoles are polygynous, with the territory of one male overlapping the territories of several females, Talbot (1979) noticed that 70% of adult A. limifrons in La Selva were found in pairs of a single male and female in close proximity to each other. However, such pair bonding has not been documented in any other population of the species, making La Selva an intriguing outlier.

A pair of Anolis limifrons (photo by Jason Weigner)

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Ken Miyata–naturalist, fly-fisherman, and photographer extraordinaire–died tragically young 30 years ago at the age of 32. Among the many items of unfinished business was his gargantuan thesis, Patterns of Diversity in Tropical Herpetofaunas, 787 pages in length and entirely unpublished. The dissertation ranges far and wide over topics herpetological and ecological–check out the Table of Contents at the bottom of the post. Over the years, Ernest Williams tried to talk a number of scientists into guiding some of the chapters into print, but the task was too large and so it has remained shelf-bound.

Anolis peraccae. Photo by Luke Mahler.

After a recent trip to Ecuador, I happened to be looking at the thesis for other reasons (parts of it were incorporated into the description of A. lyra by Poe et al. in 2009) and came across Chapter 2. This multi-part section includes separate studies on the habitat use of three anole species at the Río Palenque field station (A. chloris, A. festae and A. peraccae) and population biology and dynamics of two other species elsewhere (A. boettiger and A. gemmosus). Miyata argued that little was known of the population biology of South American anoles. Thirty years on, the situation isn’t all that different.

Anolis chloris. Photo by Luke Mahler.

As a result, the data presented by Miyata in 1983 are still very relevant today and deserve wider circulation. And for that reason, we decided to publish a lightly-edited version of parts Chapter 2 in the Bulletin of the Museum of Comparative Zoology, appropriate given that Miyata was a grad student in the Museum (this paper, like all other Bulletins of the MCZ, is available online). In addition, in an online supplementary file, a number of his friends) Jerry Coyne, Chuck Crumly, Ray Huey, Eric Larson, Greg Mayer and B Wu) provide reminiscences of Ken.

The paper ranges widely over matters of anole ecology, behavior, and population biology, providing data on five species for which almost nothing exists in the literature. The paper’s findings are summarized in the abstract:

Anolis festae. Photo by Luke Mahler.

Little is known about the ecology and natural history of South American anoles. This study reports the results of a variety of different studies on several relatively common species of Ecuadorian Anolis. In part I, habitat use and population density are compared among three species of Anolis that occur in sympatry at a number of sites in Ecuador. The three species—A. chloris, A. festae, and A. peraccae—are roughly the same body size. These species perch primarily on tree trunks, and A. chloris perches substantially higher than the other two species, which are similar in perch height. Large differences from one year to the next were observed both in mean perch height and in population densities.

Anolis gemmosus. Photo by Jonathan Losos

In Part II, natural history, growth rates, and population densities are reported for two little known Anolis species, A. bitectus and A. gemmosus. Although the two species are from nearby regions and are similar in microhabitat use, they show more differences than similarities in most aspects of their biology. The species have similar ranges in active body temperatures, but A. bitectus is thermally passive, whereas A. gemmosus appears to thermoregulate. Populations of A. gemmosus tend to remain constant through time, whereas A. bitectus undergoes moderate population fluctuations. Both species exhibit little sexual size dimorphism, but in A. bitectus females are larger, and in A. gemmosus males are larger. Anolis bitectus has a fairly high characteristic growth rate, whereas that of A. gemmosus is quite low.