Category: New Research Page 35 of 67

She’s looking at me, probably thinking “Will he eat me”? And I’m looking at her, thinking “How many transposable elements are in your genome?”

I wanted to bring the attention of the Anolis community to our recent publication in Genome Biology and Evolution (Tollis and Boissinot 2013), where we study the population dynamics of those fascinating features of the green anole genome – transposable elements. Transposable elements (TEs) are important components of vertebrate genomes that may seem a bit esoteric to many readers of this blog, yet the Anolis genome has already yielded great insights into how the vertebrate classes differ in terms of these DNA parasites. In a nutshell, our paper shows how microevolutionary forces such as natural selection and genetic drift account for differences which are most obvious when we make macroevolutionary comparisons (i.e. between mammals and reptiles). Even though I’ve cut to the chase a little early, I thought it might be nice to discuss what we know about the study of genomic evolution, and how the Anolis genome is contributing to the field of comparative genomics.

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A. sagrei developmental sequence. Cover illustration from Sanger et al. (2012) Proc. B.

As discussed previously in the Annals, interest in squamate development is rapidly accelerating. Our growing community makes this an exciting time to study lizard development, especially in a comparative context. A recent study by Andrews et al. capitalizes on the increasing number of developmental resources for squamates to assess variability in developmental sequences across lizards and snakes. One of our favorite anoles, Anolis sagrei, represents one of the 21 species included in this study. The conclusions of this study speak to several long-standing evolutionary questions and opens up new avenues of investigation that may be of interest the readers of this blog. 


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A while back, we discussed whether bats eat anoles. It was recently brought to AA’s attention that anolivory by the common big-eared bat has been graphically documented in a 2011 PLoS One paper by Santana et al. Using videos taken at feeding roosts on Barro Colorado Island, the researchers documented three incidents of anoles being consumed, one of which is exhibited above (the anole looks like A. limifrons, a common species on BCI. Agree?).

As reported recently, these bats have become adept at scanning leaves for stationary prey, a major advance in bat foraging. One of the paper’s authors, Inga Geipel, confirmed that the lizards were caught during the night. As a result, apparently no sleeping anole is safe! The authors describe this foraging thusly: “M. microtis hunts on the wing, checking leaf by leaf in the forest while hovering up and down the understory vegetation.”

As for how they eat the anole, here’s the author’s description. Gruesome warning!!! Not for faint of heart:

Bats generally ate arthropods by repeatedly biting and crushing the prey’s head, or cephalothorax in the case of spiders, and then biting and discarding the wings, antennae and/or legs. Bats mostly used their premolar and molar teeth for the latter task, biting with one or both sides of the jaw. Once the prey’s head had been consumed and appendages had been discarded, bats consumed the thorax and abdomen biting with their molars and premolars and rotating the prey from one side of the jaw to the other.…Bats ate lizards in a similar fashion as they did arthropods, except that legs were also eaten along with the whole body. Bats started eating the lizard at the head (figure above), where they applied multiple molar bites. They continued to consume the lizard by chewing it with the molars using one side of the jaw, a behavior that continued throughout the consumption of the whole of the lizard. Apparently, lizards were eaten completely; the tail was not dropped.

Adult male Anolis sagrei looking out over a pile of seaweed

Aloha, my name is Amber Wright and I’m a first-time poster here on Anole Annals. I did my dissertation on niche variation between native and introduced populations of brown anoles, with field sites in Hawaii, Florida, Little Cayman, and the Bahamas. I will be starting up a new lab at the University of Hawaii, Manoa in January 2014, so look forward to future posts on Anolis vs. Phelsuma, and get in touch if you’re interested in joining the lab!

As covered in previous posts on Anole Annals (e.g. 1, 2), our team has been studying the effects of seaweed subsidies on near-shore food webs in the Bahamas where Anolis sagrei is a key predator. While studies published to date have detailed the effects of seaweed on direct and indirect interactions among lizards, insects, and plants, our most recent paper focuses on how lizards are able to capitalize on seaweed-derived resources.

To briefly summarize the most relevant previously reported lizard results (Spiller et al. 2010), when we added seaweed to experimental plots we found that lizards switched from foraging on terrestrial prey to consuming seaweed detritivores, and that lizard density increased by about 60%. We saw an initial increase in density within the first three months, suggesting that lizards quickly moved into plots to take advantage of the seaweed. However, peak lizard abundance was observed a full year after the initial subsidy, which suggested that a lagged reproductive response could also be contributing to the overall increase in lizards.

We analyzed mark-recapture data from close to 500 individuals over the 20-month experiment to try and figure out how lizards could be turning resource input into reproductive output. We found that subsidized lizards did not survive better or have better body condition than unsubsidized lizards, but they did grow 30% faster.

A 30% faster growth rate may not seem like much of an advantage, but achieving reproductive size sooner could be a big deal in light of some key aspects of anole life history. While A. sagrei can reproduce over much of the year, there is a period of reproductive quiescence during the winter. Having a breeding season coupled with the fact that anoles can reproduce continuously (about an egg a week for A. sagrei) means that when you reach maturity during the breeding season constrains how many eggs you can produce.

We fit a model of individual growth to the mark-recapture data to quantify this effect, and proposed the following scenario shown in Figure 3 from the paper below. Lizards hatching very early in the season reach reproductive size before or near the start of their first breeding opportunity regardless of whether seaweed is present; the difference therefore lays in the lizards that hatch late. Late-hatching lizards without access to seaweed do not reach reproductive size in time to lay any eggs and must survive until the next breeding season to reproduce. Subsidized lizards that hatch late are able to catch up a bit, hitting reproductive size in time to take advantage of at least half of their first breeding season. Averaging egg production over all possible hatch-dates in a year, these growth differences translate into subsidized females laying an average of 16 eggs vs unsubsidized females laying an average of 8 eggs in year one. That’s a doubling in fecundity due to seaweed addition.

Model-estimated growth and reproductive phenology for females born during the study period. This scenario assumes a size at hatching of snout–vent length = 16.5 mm, a one-month incubation time, and that the peak egg-laying period is from May to September (shaded boxes). The dotted line indicates minimum reproductive size (snout–vent length = 34 mm). Growth trajectories follow lizards hatching early (June) and late (October) in the breeding season. Symbols (triangles and circles) mark when lizards reach minimum reproductive size depending on hatch date and whether seaweed was added (solid lines) or removed (dashed lines).

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The parasite in question. Photo from an Anole Annals post by Gerrut Norval.

Recently, Bryan Falk wrote an interesting report on how nematode parasites are passed from one anole to another by sexual contact. He summarized a fascinating paper by Langford et al. in the Journal of Parasitology that convincingly demonstrated this phenomenon. In reading that paper, I found one idea they suggested in the Discussion to be particularly intriguing. I’ll let them describe it:

“Our finding that C. penneri” (the nematode parasite) “is transmitted by copulation has some interesting implications for the host’s reproductive and behavioral biology. Anolis sagrei reproduces in a female-defense polygyny, wherein large males (e.g., SVL = 50 mm) establish and maintain territories containing multiple, relatively small females (Schoener and Schoener, 1980). In Anolis mating systems, young males are generally thought to have little mating success because they are excluded from females by large territorial males (Losos, 2009). In contrast, our parasitological results suggest that small male lizards are copulating with mature females and becoming infected with a sexually transmitted parasite. Thus, our results provide some support for the female mimicry hypothesis (Orrell and Jenssen, 2003) and/or the ‘‘dear enemy’’ phenomenon (Paterson, 2002) in anoles. This insight into A. sagrei reproduction should encourage anologists to reconsider the role of covert and satellite males in anole mating systems where C. penneri infects small male lizards. In conclusion, the major contribution of our study is the establishment of copulation as the route of transmission for C. penneri between lizards and the discovery of both ecological and physiological host specificity in these worms.This study also provides insight into the host’s biology, specifically support for the female mimicry hypothesis in anoles proposed by Orrell and Jenssen (2003).”

I queried Gabriel Langford, “just how small are these infected males?” He responded: “We sampled an evenly distributed group of females and males that ranged from a few days old to large (male SVL 68mm) adults. If memory serves (I’m on my tablet, no data in front of me), at least 35 of the 87 males fell into the range of 34-50 mm. Also, we had several males just above (infected) and below (uninfected) the 34 mm cut-off, which allowed us to be fairly confident about this number in A. sagrei.”

These results suggest that even quite small males may be mating, even though they are far too small to hold a territory. The idea that “sneaker” males may exist in anole populations has been suggested before, but not demonstrated. The occurrence of such matings has all kinds of interesting implications for anole sexual selection and evolution.

In 2007 a multi-disciplinary group (Yasel U. Alfonso, Florida Museum of Natural History, USA; Lourdes Rodriquez-Schettino, Institute of Ecology and Systematics, Cuba; and Denis Dennis Avila, Faculty of Biology, University of Havana, Cuba) began to investigate phenotypic plasticity in three Anolis jubar subspecies. We quantified variation in meristic traits, head shape, microhabitat use (i.e, escape behavior, thermoregulation, feeding) and dewlap colour to see if any of these characters differs at a geographic, and subspecies level. We analyzed variations on body dimensions and head shape (using geometric morphometrics) and their relationships with microhabitat use and found that A.j.albertscwartzi was the most differentiated subspecies (manuscript in prep.). Interestingly, Cadiz et. al. recently found Anolis jubar albertschwartzi to be more closely to Anolis homolechis than other A. jubar subspecies based on markers. The differences between our findings and genetic studies by Cadiz et al. (2013) highlight the need for a better understanding of how selective traits are shaped by speciation and selective forces.

For the last few years, our multi-disciplinary group included two new members (Humberto J. Morris, Center of Studies for Industrial Biotechnology, Cuba; and John E. Steffen, School of Science, Penn State Behrend, PA) and we have been investigating pigment patterns in anoles from Eastern Cuba. Our first approach was analyzing the dewlap colour variation among three Anolis jubar subspecies (A.j.oriens, A.j.maisiensis, and A.j.albertscwartzi) using two alternative methods: 1) digitally, using RGB analyses with Munsell’s colour system (manuscript in prep.) and 2) spectrophotometrically, using pigment concentration variation to analyze subspecies level variation in dewlap colors (manuscript available in Copeia, 2013 issue 2, “Dewlap Color Variation Based on Pterin and Carotenoid Pigments in Three Subspecies of Anolis jubar of the Cuban Southern Coast”).

This research was made throughout fall 2008 and fall 2009, and we focused on quantifying the subspecies-level flexibility in dewlap pigmentation using only biochemical compounds from dewlap skin. We found that Anolis jubar albertschwartzi was the most differentiated subspecies based on pigment concentration (see details, Fig. 1 & 2) giving a light yellow shade of his dewlap coloration. 

We are performing similar pigmentary studies on several other Eastern Cuba anoles (e.g., A. allogus, A. rubribarbus, A. sagrei, A. porcus, A. anfiloquioi, A. cyanopleurus) and results will be available soon (manuscript in prep.).

In addition, I am leading other ongoing projects. One will attempt to explain relationships between color production and immune system health. Because pterins can also be synthesized by nonintegumentary tissues, most notably by immune cells (e.g. monocytes, macrophages), they may illustrate a critical link between color production and immunity in a colour-signalling system.

Finally, we’re analyzing anti-predator escape behavior, microhabitat use, and thermoregulation of anoles species on the semiarid southern coast (i.e., Guantanamo) (manuscript in prep.). All of these projects will keep us busy during next year.

Up high displaying green anole. Photo from this website, which has some nice other reptile shots.

Many animals use different parts of their habitat for different activities–eating in one place, mating in another, and so on. This hasn’t been studied in many anoles, but has been documented in several. In addition, many species alter their habitat use in the presence of competitors, and this has been widely demonstrated in anoles. However, few have studied the interaction of the two phenomena: is the extent of behavioral partitioning among habitats affected by the presence of competitors?

To address this question, Ambika Kamath and colleagues studied green anoles on several islands in Mosquito Lagoon in the Intracoastal Waterway of Florida. In this area, a number of small “spoil” islands were created when the waterway was dredged half a century ago. These islands were quickly colonized by plants–and now are covered with very large trees–and then by green anoles. More recently, the invasive brown anoles have arrived on the scene on some of the islands.

Kamath et al., whose research was recently published in a paper in Breviora, chose four islands, two with brown anoles, two without (freely available, as are all MCZ publications, on the museum’s website). On these islands, they recorded habitat use and behavior. As predicted animals forage at lower heights than where they perch. One possible explanation is that they sit at vantage points looking for prey, then go down and catch them. And as predicted, males display at particularly high spots. The explanation here is not clear, but as reported recently for A. cuvieri, males seem to like to display higher than their rivals. Finally, once more as predicted, in the presence of brown anoles, green anoles shift upwards in all respects.

The interesting finding, however, is that the shift is essentially parallel for all activities. Animals move downward the same amount to capture prey and upward the same amount to display. This would suggest that there is not an optimal height for feeding or displaying, or perhaps that the optimal height changes in the presence of brown anoles. That would be readily understandable with regard to feeding–the voracious brown anoles probably vacuum up the low-lying food, so no point in dropping down as low to feed as in their absence. Why males continue to move up even higher is less obvious, though it may be just that competitors are now perching higher, so a male has to go higher yet to display above them.

This paper represents the sort of detailed behavioral study that is all too infrequent for anoles. How these lizards modulate their behavior in response to conditions is fascinating and often surprising. Much remains to be learned, and most anole species–well, at least in the Caribbean–are amenable to behavioral observation.

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.