Category: New Research Page 12 of 66

Figure 1. Differences in claw clipping used in Bloch and Irschick (2005) and our study. (A) Bloch and Irschick (2005) clipped the entire claw after the distal end of the toe pad. (B) In our study, we partially clipped the distalmost portion of the claw.

Toe and claw clipping are common techniques used to identify individuals in mark and recapture studies, but their impacts on whole organism performance are unclear (Dunham et al., 1988). Anoles have not only developed subdigital adhesive toe pads to promote adhesion on relatively smooth substrates, but have also retained claws to enhance attachment to rough substrates (Irschick et al., 1996; Zani, 2000). Thus, clipping entire toes or claws may have drastic effects on the clinging ability of anoles or other adhesive pad-bearing lizards. In our recent article published in Acta Herpetologica, my co-authors and I investigated how partially removing the claws of brown anoles affects their adhesive performance.

Figure 2. Mean maximum clinging force of Anolis sagrei with intact and partially clipped claws. Overall, partial claw clipping had no significant effect on maximum clinging ability.

Bloch and Irschick (2005) removed entire claws from Anolis carolinensis (Fig. 1A) and measured its impact on their clinging ability. Not surprisingly, claw removal resulted in a significant decrease in the clinging ability of A. carolinensis, likely a consequence of the severing of flexor tendons that are critical in adhesive toe pad engagement. In an effort to test this hypothesis and preserve these tendons, we used a motorized force sensor (Niewiarowski et al., 2008) to measure the maximum clinging ability of 19 Anolis sagrei before and after their claws were partially clipped (Fig. 1B).

Overall, we found that partial claw clipping did not significantly impact maximum clinging ability (Figure 2). This suggests that clipping the entire claws of anoles may indeed sever the flexor tendons crucial to toe pad engagement. Furthermore, we expected clinging ability to increase after partial claw clipping because claws should theoretically interfere with the contact the subdigital adhesive pads are capable of producing. However, this did not appear to be the case, suggesting that claws may not inhibit the engagement of subdigital pads or that morphological features and/or behavioral traits reduce the effect of this interaction.

Anolis sagrei

Although permanent marking solutions would be most beneficial for mark and recapture studies, partial claw clipping may be a useful alternative for shorter-term studies because it does not appear to reduce adhesive performance on smooth substrates. Future work should further consider the interactions between subdigital adhesive toe pads and claws, and determine the possible ramifications for adhesion and adhesive locomotion, particularly on rough substrates. Be sure to check out our full article for more details!

References

Bloch, N., Irschick, D.J. (2005): Toe-clipping dramatically reduces clinging performance in a pad-bearing lizard (Anolis carolinensis). J. Herpetol. 39: 288-293.

Dunham, A.E., Morin, P.J., Wilbur, H.M. (1988): Methods for the study of reptile populations. In: Biology of the Reptilia, pp. 331-386. Gans, C. Huey, R.B., Eds, Alan R. Liss, Inc., New York.

Irschick, D.J., Austin, C.C., Petren, K., Fisher, R.N., Losos, J.B., Ellers, O. (1996): A comparative analysis of clinging ability among pad-bearing lizards. Biol. J. Linn. Soc. 59: 21-35.

Niewiarowski, P.H., Lopez, S., Ge, L., Hagan, E., Dhinojwala, A. (2008): Sticky gecko feet: the role of temperature and humidity. PLoS ONE 3: e2192.

Zani, P. (2000): The comparative evolution of lizard claw and toe morphology and clinging performance. J. Evol. Biol. 13: 316-325.

Chris Thawley at a crossroads.

Plants and animals across the globe are dealing with increasingly changing environments resulting from urbanization. One such habitat alteration is artificial light at night (ALAN) that may affect how animals acquire or use energy. Because brown anoles (Anolis sagrei) are common invaders of urban habitats, they make good models to examine the consequences associated with ALAN. Thus, Chris Thawley of Jason Kolbe’s lab at University of Rhode Island altered the level of ALAN on female brown anoles to examine how ALAN might affect morphology, reproduction, and stress.

If this sounds familiar, Chris talked about this work at the 2017 JMIH meeting, which caught Anole Annals press. To recap, Chris found that ALAN increased female growth, advanced the start of egg laying to earlier in the season, and increased the reproductive output of smaller females. However, he hypothesized that such beneficial effects would be countered by negative effects on other traits. Thus, Chris measured levels of the stress hormone corticosterone in the blood of females, hypothesizing that those exposed to ALAN would have higher stress. Although marginally non-significant, females actually tended to have lower corticosterone levels. Chris presented new data for this presentation showing that male corticosterone levels were unaffected by ALAN too, suggesting neither adult male nor female brown anoles have a stress response to artificial light.

Thus, it appears ALAN exposure over this 7-week study was beneficial for brown anole reproduction. However, Chris cautioned that there may be negative consequences on other traits such as immunity or HPA function. ALAN might also induce negative consequences for reproduction later in life, such as a reduced lifespan. I recommend keeping an eye on the Kolbe lab to find out!

Putter, Austin, and a real big tree they visited while travelling to the meeting.

The effect of urbanization on animals was the topic of many presentations at this year’s SICB meeting. One difference in the abiotic environment of urban areas is that they are often hotter than neighboring natural areas. Sarin “Putter” Tiatragul and colleagues (Josh Hall, Nathaniel Palik, and Dan Warner) at Auburn University are interested in whether urban environments might influence the nesting ecology and development of anoles. Thus, they set to the field to search for nest sites of the Puerto Rican Crested Anole (Anolis cristatellus).

Putter predicted females would choose warm, open-canopied nest sites at both urban and forested habitats, but that the availability of such locations would not be equal between sites. As predicted, randomly available areas in urban habitat had less tree cover and were warmer than randomly available locations in the forest. In the forest, females nested in locations that were similar to what was randomly available (no preference) in terms of distance to the nearest tree, canopy cover, and nest temperature. However, urban anoles nested in less open areas and closer to trees than what was randomly available in the urban habitat. This resulted in female-chosen nests sites being cooler than what was randomly available.

These findings suggest female anoles in forested areas are not choosing nest sites, probably because the forested habitat is homogenous and provides little variation to choose amongst. However, females in urban areas search out cooler microhabitats possibly to achieve favorable incubation conditions for their offspring. Putter also suggested these females may be simply nesting close to where they normally occur, which is close to trees. Either way, females are using the habitat differently in urban areas and such variation will likely have consequences for offspring during development.

A small sample of anole dewlap diversity. Image from Nicholson et al. (2007).

Dewlaps are pretty dazzling, ranging in size, coloration, and sexual dimorphism substantially among the 400+ species of anole currently recognized. Levi Gray, a doctoral candidate at the University of New Mexico is fascinated by Anolis dewlaps, and has spent many years studying them. One of the classic hypotheses surrounding dewlap evolution in anoles is that its size follows a clinal pattern with environment (Fitch and Hillis 1984). In their formulation, Henry Fitch and David Hillis proposed that, due to a relatively short breeding season, anoles in more seasonal habitats have larger dewlaps than anoles in more aseasonal habitats. This hypothesis makes an explicit connection between the intensity of sexual selection and the size of a conspicuous ornament.

Levi set out to test the Fitch-Hillis hypothesis in 40 species of Mexican anoles distributed across environmental gradients, with some species found in aseaonal cloud forests and rainforests and others found in more seasonally dry habitats. Contrary to the Fitch-Hillis hypothesis, he found no relationship between seasonality and dewlap size in the Mexican anoles. He did detect a few clade effects: for example, a group of closely related western Mexican anoles all have large dewlaps. He then examined the Fitch-Hillis hypothesis within a single widespread species of anole, A. sericeus, to see if the pattern holds up within species, even if it doesn’t hold up among species. Again, he didn’t detect a pattern. Levi suspects that the relatively limited sampling of the original study might have led to a pattern that doesn’t hold up when a broader sampling within and among species is employed. It is possible that seasonality impacts a different aspect of the dewlap, such as coloration, but this remains untested. Levi’s results suggest that the processes impacting dewlap size might be complex, and promises more to come. Stay tuned!

Levi Gray presents his research on dewlap size evolution in Mexican anoles at SICB 2018 in San Francisco.

Winning Symposium t-shirt design by Eric-Alain Parker

Calling all anole aficionados! Spots for the Seventh Anole Symposium on March 17-18, 2018 at the Fairchild Tropical Garden in Miami, Florida are starting to fill up! We have a limited number of spots for attendees and fewer still for presentations. If you have already registered, great! If you haven’t, please do so soon to guarantee your spots. Registering now does not require you to also pay now  – registrants will be contacted in early 2018 to pay the $100 registration fee. Submitting an abstract is not also required at this stage, and can be amended to the registration at a later date.

Photographs of a subset of lacertid lizard species used in this study. From the left top to the right bottom: Acanthodactylus beershebensis, Lacerta bilineata, Dalmatolacerta oxycephala, Podarcis melisellensis, Tropidosaura gularis, Podarcis siculus, Heliobolus lugubris, Algyroides nigropunctatus, Lacerta media.

The vast array of signals used in animal communication is a continuous source of awe and a hot topic in evolutionary and behavioral research. One important factor contributing to the signal diversity we witness today is ‘signal efficacy’: the ability of a signal to travel efficiently through the environment and attract the receiver’s attention. With this in mind, natural selection is expected to mold signal design for maximum efficacy of information transmission and detectability, leading to signal variation among populations/species living in different environments. To illustrate, a recent study by Tess Driessens and colleagues assessed the degree of variation in the dewlap design of Anolis sagrei by comparing 17 populations distributed across the Caribbean (Fig. 1).

Fig. 1 — Phylogenetic relationships among 17 Anolis sagrei populations. Pie charts illustrate dewlap pattern proportions for each population per sex (black = solid; light grey = marginal; dark grey = spotted). Photographs represent male and female dewlaps of typical individuals from every population.

Their findings showed large interpopulational variation in dewlap size, pattern, and color, and more interesting, they established a link between the dewlap design of brown anoles and the environment they live in. Lizards occurring in more ‘xeric’ environments had a higher proportion of solid dewlaps with a higher UV reflectance; lizards inhabiting ‘mesic’ environments had predominantly marginal dewlaps showing high reflectance in red. This was true for both males and females. Like Ng et al. (2011) and their observations on dewlap variation in A. distichus across an environmental gradient, Driessens et al. (2017) interpret their findings as evidence for adaptive divergence of a signaling apparatus.

Surprisingly though, while there are numerous great examples of comparative studies finding support for convergent evolution in visual and acoustic signaling systems, (e.g. Endler 1992; Fleishman 1992; Nicholls & Goldizen 2006, to say a few), similar (comparative) studies, but then, on the phenotype of chemical signals are almost entirely lacking. This is probably due to the combination of only very recent developments in chemical analytical and statistical comparative tools, the time researchers need to assemble a large-scale multi-species chemical dataset, and perhaps due to our own predisposition to visual and auditory signals. Currently, the proper analytical tools for studying natural products chemistry are available and affordable, permitting comprehensive taxon-wide research on the evolution of chemical signal diversity and design. Ultimately, there has never been a better time as now to be a comparative chemical ecologist.

Photograph of the cloacal region of a male lacertid lizard (Lacerta agilis), showing his numerous femoral pores with protruding glandular secretion.

Finally, three Belgians, two Spaniards and one Greek (sounds like the start of a joke with ample potential) took up the challenge to examine variation in the chemical signal design of lizards. Although underrepresented in studies on chemical signal diversity, lizards are an excellent group for investigating chemical signal evolution, as many of them they bear numerous glands on their thighs that secrete waxy substances, which they deposit while moving through their habitat. These secretions are often considered the leading source of chemical signals involved in lizard communication.

The study started with a quest. A quest to collect gland secretions of as many species as possible (within a PhD timeframe). Luckily, we were fortunate enough to be able to count on the help of many collaborators (Shai Meiri, Chris Broeckhoven, …). We focussed on lacertid lizards, as they are a species-rich family distributed over a wide geographical area, and known to rely strongly on chemical communication in several contexts.

In total, we sampled secretions from 64 species throughout, Europe, Africa, and Asia, covering a wide array of habitats and climate regions: from the Mediterranean maquis over the alpine meadows in the Pyrenees Mountains, to the sandy Israeli dunes and the Kalahari Desert of South Africa (Fig. 2). Back in the lab, we determined the chemical composition and chemical ‘richness’ (number of different chemical compounds) of the secretions using GC-MS, and obtained climate data for all catch-localities from online databases.

Fig. 2 — Map showing the sample localities of the 64 lizard species under study.

Our gathered data showed considerable variation in the chemical richness and composition of lacertid secretion. Shared-ancestry failed to explain among-species patterns of variation, hinting that chemical signals may change relative rapidly. Most interestingly, our findings revealed a strong relationship between the environmental conditions species live in and the chemical composition of their glandular secretions. On the one hand, lizards living in ‘xeric’ environments, characterized by high temperatures and arid conditions, contained higher proportions of stable and heavy-weight compounds in their secretions. Hot and dry conditions increase the evaporation rate of chemicals, and so, decreasing the longevity of a signal. Stable and heavy-weight compounds most likely reduce evaporation rate and counteract the rapid signal fade-out through evaporation, generating a highly persistent scent-mark. On the other hand, species inhabiting wet, humid conditions produced highly aromatic and low-weight secretions containing numerous different compounds. This chemical mix probably creates a volatile-rich signal that can be used for long-distance airborne communication.

While we cannot deny that these findings of convergent evolution in the design of chemicals signals are fascinating, some would say this outcome is not unexpected.

“[…] a cadre of scientists has taken the […] view, that convergence is the expectation, that it is pervasive, and that we should not be surprised to discover that multiple species […] have evolved the same features to adapt to similar environmental circumstances. From this perceived ubiquity, the scientists draw a broader conclusion: evolution is deterministic, driven by natural selection to repeatedly evolve the same adaptive solutions to problems posed buy the environment. — J. Losos (Improbable Destinies, p. 33)

Nonetheless, I am confident to state that using by far the largest comparative dataset amassed to-date to examine patterns of chemical signal divergence, we have provided strong evidence for a significant relationship between chemical signal design and prevailing environmental conditions, which may results from differential selection on signaling efficacy (Baeckens et al. 2017).

A male slender anole (Anolis limifrons)

A walk through a tropical rainforest can reveal astonishing forms and colors of organisms – from vibrant poison frogs and coral snakes to the vegetative camouflage of stick insects and other cryptic creatures. Perhaps some of the most dramatic displays of variation can occur between the sexes, where males and females can differ so greatly in appearance that they resemble different species. Research in many systems has demonstrated that much of this variation is driven by sexual selection, the force responsible for the evolution of traits that are important for acquiring mates. Individuals may invest as much energy as possible into such sexually selected traits because doing so will give them a competitive advantage for mate acquisition. These traits are therefore considered condition dependent, as their expression is dependent upon the energetic condition of the individual that possesses them. While condition dependence has been the subject of many studies, it is not well known how it may vary between closely related species that share the same traits. If closely related species vary in condition dependence of their shared traits, then this implies that condition dependence could be important for the evolutionary diversity of sexually selected traits.

The lowland rainforest at the La Selva Biological Station in Costa Rica

Together with students from Grinnell College and Reed College, and as part of an OTS (Organization for Tropical Studies) course that I took as an undergraduate at the University of Virginia, we took to the lowland jungles of Costa Rica to answer this question. We studied two anole species from Costa Rica, the slender anole (Anolis limifrons) and the ground anole (Anolis humilis). Specifically, we tested whether several traits that they had in common exhibited condition dependence, including dewlap size, aspects of jaw morphology, and sprinting speed. To test for condition dependence, we first calculated two conventional indices of body condition, the residual index and the scaled mass index, which both take into account an organism’s mass, given its length. We then obtained residuals from the relationship between our variables of interest (dewlap size, jaw width, jaw length, and sprint speed) and snout-vent length (a measure of body length), which allowed us to control for the fact that trait sizes often scale with the overall size of an animal. Finally, we used bivariate linear regressions to test the effect of our indices of body condition on our residual traits of interest, with a significant positive relationship suggesting condition dependence. We found that dewlap size (a trait important for sexual signaling) and jaw width (a trait important for bite force and male combat) exhibited condition dependence in ground anoles, but not in slender anoles. In contrast, neither sprint speed nor jaw length were condition-dependent in either species. Importantly, the presence of condition dependence in one species, but not the other, implies that the condition dependence of shared traits is evolutionarily labile. Additionally, by detecting condition dependence in the dewlap of ground anoles, which have a larger dewlap given their body length when compared to slender anoles, our findings may indicate that the strength of sexual selection differs between these two species. Lastly, our research suggests that variation in condition dependence of the dewlap among species could contribute to the extraordinary diversity of dewlaps in the Anolis genus.

If you would like to read the full paper, published in the Journal of Experimental Zoology Part A, go to:http://onlinelibrary.wiley.com/doi/10.1002/jez.2076/epdf