I’ve been re-watching some of my Sitana videos from 2012, and was reminded of an odd interaction between an Indian robin and a male fan-throated lizard (Sitana ponticeriana), from a population in Kutch, Gujarat, in western India. Usually, Indian robins and fan-throated lizards don’t pay much attention to each other. Here’s a video in which a lizard displays when a pair of robins pass by. His dewlap remains extended for a while, which is uncharacteristic, but the interaction doesn’t escalate:
But in the same population, an Indian robin chases after a male fan-throated lizard, after the lizard first ran in the direction of the robin. He starts perched on the rock in the centre of the screen. Here’s a video, slowed down to half-speed. When filming, I had no idea what was happening, or even where the lizard was, which explains why the camera deviates from the lizard for a while (apologies).
I’m not sure what’s going on. I didn’t think robins eat lizards–do they? Maybe it thinks the lizard’s tail is a worm? Maybe it’s just playing? Any further ideas?
If you followed the barrage of blogposts we wrote from SICB 2014, you might recall some discussion of the information actually conveyed by anole displays and dewlaps (1, 2). The upshot of these studies is that anole displays are complex. We see unexpected relationships between various traits and the probability of success in male-male competition, and different traits correlate with different measures of male success. A recent study by Steffen and Guyer (2014) adds to our growing knowledge of the information conveyed by different dimensions of multimodal anole displays. When viewed together with previous research, this study presents us with an even messier picture than before of how Anolis lizards communicate with each other.
Steffen and Guyer (2014) set up paired competitions between size-matched male Anolis sagrei in a lab setting, implementing two treatments–males either compete for access to a single perch, or for mating access to a single female. All interactions were recorded, and display behaviours–headbobs, push-ups, dewlap extensions–were quantified. Further, the spectral reflectance of both the centre and the margin of the dewlap (which can be strikingly different in A. sagrei) was also measured. The question asked by the paper was straighforward: which display and dewlap traits are related to an individual lizard’s status as a winner or loser of competitions?
In both competitive contexts, only two traits seem to be important–a composite axis of behavioural variation, and one of three composite axes describing the colour of the margin of the dewlap. Lizards who headbob, push-up, and extend their dewlaps more during competitive interactions are more likely to win than lizards who display less. Curiously, lizards with lower UV reflectance of the dewlap margin are more likely to win than lizards with brightly UV-reflecting dewlap margins.
Of the two variables, display behaviour was more highly correlated with the probability of success than dewlap margin UV-reflectiveness. I’m curious about how the two variables are themselves related–do lizards that display more also have less bright dewlap margins? The authors propose that a dewlap’s reflectance might relate to its conspicuousness, and it would be interesting to know if different individuals are conspicuous in different ways.
Each of the studies conducted so far on how anoles convey information to each other has examined different dewlap and display variables, studied different competitive contexts, and used different measures of male quality. It therefore isn’t surprising that we seem far from reaching a consensus on what the dewlap says.
In species of Anolis where females have dewlaps, we know very little about exactly how females use their dewlaps. Losos (2009) describes this lamentable situation thus:
“Unfortunately, little is known about how females use their dewlaps, and the little information that is available from three species permits few generalities. Anolis carolinensis females only rarely use their dewlaps in intersexual displays (Jenssen et al., 2000), whereas female A. valencienni use their dewlaps primarily to discourage courting males, including those of other species (Hicks and Trivers, 1983). Both A. carolinensis and A. bahorucoensis females use their dewlaps in intrasexual displays (Orrell and Jenssen, 1998, 2003); in A carolinensis, females use the dewlap more at close range and less at long range in female-female interactions compared to dewlap use in male-male interactions (Jenssen et al., 2000; Orrell and Jenssen, 2003). Unfortunately, without more information on how females use their dewlaps, we will not be able to explain sexual dimorphism and dichromatism in anole dewlaps.”
Since then, Martha Muñoz has added an observation from A. armouri, but the numbers are still small.
Attempted forced copulation in Anolis cristatellus
In July 2013, I spent ten days observing A. cristatellus in Mayagüez, Puerto Rico, and can add one more species to the list of female anoles that use their dewlaps to dissuade males from mating with them. I was mapping male territories and counting male-male interactions in a park in one of Mayagüez’s fancier neighbourhoods, and came across a male chasing after a female. I sat down to watch the interaction, and was struck by how determined the female seemed to avoid mating with this male. You’ll notice how the male is biting the female much lower down the body than is normal during mating, indicating how the female is trying to get away. Her dewlap is completely extended during this interaction.
The chase went on for several minutes before the female ran to the end of a thin branch and another male showed up to chase the first male away. I proceeded to catch and mark this second male, and later observations revealed him to be the resident territory holder of the tree.
A little later, we caught a male in the tree adjacent to one in which the showdown occurred. In a fantastic stroke of luck that anyone whose work depends on identifying individual animals in the field will appreciate, we were able to determine that this male from the adjacent tree was in fact the first of the two males observed earlier.
How, you ask, did we perform this forensic wizardry? Observe the second tiny tail of the interloper attempting the forced copulation:
Caught red-handed!
I was showing these photos to Jonathan Losos the other day, and he immediately noted that the observation of a female using her dewlap was pretty rare. Of course, the obvious response was to write a blogpost about it, but then we realised that with Anole Annals‘ daily viewership of up to 1500, we could do more than just write a blogpost–we could do citizen science! So this, ladies and gentlemen, is an invitation to all of you to help build a dataset. It’s more than the usual request for participation and comments that I end many posts with–it’s a challenge to all of us AA readers to keep an eye and camera out for examples of females using their dewlaps, so that we can together figure out a pretty basic piece of Anolis biology.
We’ve done this sort of citizen science before, quite successfully: here’s Kristin Winchell’s call for data on urban anoles, and here’s the resultant analysis. And there’s all sorts of exciting natural history questions that would be impractical for individuals to tackle on their own, but that we can solve easily as a team. Let’s make this blog a citizen science hotspot!
Though 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 publishedAnolis 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.
Though we now understand that post-copulatory sexual selection (such as sperm competition and cryptic female choice) can be as important in determining variance in reproductive success as pre-copulatory sexual selection, and though we recognize that the expression of traits subject to pre-copulatory sexual selection is often condition-dependent, it turns out that we know almost nothing about the condition-dependence of traits under post-copulatory sexual selection.
Sperm of Anolis sagrei. Picture by Ariel Kahrl.
In a session devoted to post-copulatory sexual selection, University of Virginia graduate student Ariel Kahrl described her research on the condition-dependence of sperm characteristics in Anolis sagrei. By feeding size-matched male lizards differentially for a period of four months, Kahrl not only generated differences in the body condition of these males, but also ensured that their sperm had developed under her imposed dietary regime. Kahrl predicted that male body condition would affect sperm morphology and sperm count. Pairs of males reared under different dietary conditions were also mated to a single female (making sure to control for mating order by using a reciprocal mating design), thus putting the sperm of two males with different body conditions into direct competition. Kahrl predicted that the fertilization success of males would depend on sperm morphology and count.
Not surprisingly, males with higher body condition had higher fertilization success. It turns out that variation in fertilization success may be influenced by a tradeoff between sperm mid-piece size and sperm number. This situation is interesting, because one can reasonably predict that males on either end of the tradeoff could have high reproductive success—having many sperm per ejaculate could increase the odds of fertilization, akin to purchasing multiple lottery tickets, but having sperm with larger mid-pieces, and thus potentially more mitochondria, perhaps might provide sperm with the burst of energy necessary to win the fertilization race.
In fact, Kahrl found that males with high sperm counts but small midpieces achieve high reproductive success. Intriguingly, she also found that high-condition males had sperm with less variable morphology than low-condition males, and hypothesizes that the dimensions of these uniform sperm match the dimensions of the tubules in females where sperm is stored. Kahrl’s results link pre-copulatory to post-copulatory sexual selection through condition-dependence, and represent a sizeable piece in the puzzle of how sexual selection works in Anolis lizards.
Anolis carolinensis from Miami. Photo by J. Losos.
I’m often a little skeptical of studies that suggest how lab results can have implications for natural systems without actually examining the problem in nature, and studies that address the same question in both lab and field are still rare. That it investigated the same broad question in the lab, in enclosure-style experiments, and in the field is what made Trinity University student Jordan Bush’s poster remarkable.
Bush was interested in the traits associated with dominance, and began by running a tournament of agonistic interactions between a set of male Anolis carolinensis. She used a number of different Markov Chain Monte Carlo algorithms, widely used in predicting winners of sports tournaments, to convert pairwise fight outcomes into individual ranks of “fight-winning ability.” Bush found that rank could be predicted by size-corrected head length, as well as the propensity for aggressive behaviours such as push-upping and crest-raising.
But do these same traits predict dominance in nature? Not exactly. Bush took the question to the field, and found that none of the traits that predict dominance rank in the lab are correlated with territory size in the wild. In the final piece of the puzzle, Bush constructed experimental enclosures to measure the territory sizes of males with known ranks (by conducting another dominance tournament). As predicted by the first two parts of the study, territory size was not correlated with rank.
By harnessing the power of both lab and field experiments to observations made in nature, Bush’s study will change the way behavioural ecologists think about territory formation. I’ve always assumed that winning agonistic encounters is the means by which anoles increase the sizes of their territory, but like everything in nature, it’s more complicated than that!
Modifying behaviour is often an animal’s first line of defence against a changing environment. We know from Martha Muñoz’s research that high elevation relatives of Anolis cybotes—A. shrevei and A. armouri–modify their perch use to better thermoregulate in colder climates. In a talk entitled “Behavioural divergence along an altitudinal gradient in a clade of tropical lizards,” graduate student Katie Boronow investigated a number of other behavioural traits, asking whether shifting to high altitudes necessitates a suite of behavioural modifications in the cybotoid anoles.
Boronow measured basking, display, escape, and locomotor behaviour in four anole populations–a high-elevation and a low-elevation site in each of two mountain chains in the Dominican Republic. Sites differed substantially in habitat openness–high-elevation sites had a higher proportion of exposed substrate and lower canopy cover than low-elevation sites.
In both mountain chains, individuals basked more and fled more readily at high-elevation sites than at low-elevation sites. The first result is easily attributed to variation with altitude in thermoregulation–it’s not surprising that lizards bask in direct sunshine more when it’s cold. While the differences in escape behaviour might also be driven by high-altitude lizards being thermally disadvantaged, Boronow found no differences in lizard body temperature between high- and low-elevation sites. Predation risk (as measured by attacks on clay models) also did not differ between sites at high and low elevations, so this variation in escape behaviour remains a mystery.
Given that locomotor behaviour is thought to be tied closely to ecomorph and that both high- and low-elevation cybotoids are still trunk-ground anoles, it is also unsurprising that rates of locomotion (measured by movements per minute, a common metric of foraging behaviour) did not vary by elevation. Patterns of display rates were interesting–while there was no altitudinal effect on display rate, the variation in display rate among populations of cybotoid anoles was comparable to the extent of variation seen across ecomorphs in previous studies. Boronow’s results suggest that differences in macrohabitat can be an important driver of intra-ecomorph behavioural diversification in anoles.
While we all know that the dewlap of Anolis lizards must provide some information about the signalling lizard to receiver lizards or predators, we remain uncertain about the exact nature of this information. By measuring aspects of dewlap design as well as myriad features of Anolis sagrei locomotor, immune, and behavioural performance, Tess Driessens of the University of Antwerp has begun to unravel the web of information conveyed by the dewlap.
Driessens’ results are complex, to say the least. Different features of the male dewlap relate in un-intuitive ways to various aspects of performance. For example, dewlap brightness was inversely proportional to jumping ability as well as immunocompetence, but directly proportional to haematocrit levels. Most surprisingly, given contrary results from previous work in A. carolinensis, size-corrected bite force in males was not related to any dewlap design variable in A. sagrei. In contrast to the male dewlap, no features of the female dewlap were found to relate to any measure of performance.
Though not unique to anoles, dewlaps are a defining feature of the genus, and I’ve always been amazed at how little we actually know about what dewlaps can say about the individual lizards that bear them. Driessens’ study is an important step towards answering that question.
A majority of biomechanical studies focus on eliciting maximal performance from animals in laboratory conditions, an approach that can make it difficult to apply results from the lab towards understanding performance in nature. Jerry Husak addressed this issue in his talk entitled “Maximal locomotor performance and sprint sensitivity in green anole lizards (Anolis carolinensis).”
By measuring sprint performance on a variety of perches (two different dowel widths, as well as a broad perch with pegs functioning as obstacles) and comparing these performances to sprint performance on a broad, flat surface, Husak showed that green anoles are substantially worse at running on narrow perches and through obstacles than at running on broad, flat surfaces. This confirms that animals moving through their natural habitats are almost certainly sprinting sub-maximally–in nature, green anoles are found most often on perches even narrower than those tested.
Crucially, the morphological correlates of performance varied by perch, suggesting that fine-scale studies of selection on limb and muscle morphology in the wild will require knowledge of how often and in what circumstances lizards navigate different microhabitats and move on different substrates. Coupled with behavioural observations in the wild, this study can pave the way for a more nuanced understanding of body shape evolution in our favourite lizards.
Continuing with my theme of posting about non-anoles that anolologists find interesting, here’s a summary of a fascinating poster about tail-curling in two species of Leiocephalus: L. carinatus (the famous consumer of A. sagrei in the Bahamas) and L. barahonensis. Tail-curling is known to function as a predator-deterrent signal in L. carinatus, but its potential as a social signal has remained unexplored. Bonnie Kircher, a student in Michele Johnson’s lab at Trinity University, set about rectifying this gap.
Having never seen a curly-tail myself, I was surprised to learn that these lizards exhibit a variety of tail-curling behaviours.
A figure from Bonnie Kircher’s poster describing how tail-curling was scored in this study.
By scoring the intensity of tail-curling during social encounters as well as during non-social periods, Kircher showed that tail-curling was not used as a social signal in either Leiocephalus species. In an elegant control, she demonstrated that head-bobbing was more frequent in social than in non-social contexts, thus verifying that social contexts were indeed accurately identified.
Kircher also simulated predation by approaching the lizards and observed their use of tail-curling while fleeing. A comparison of the frequency of tail-curling between disturbed and undisturbed lizards confirmed that L. carinatus uses tail-curling as a signal during encounters with potential predators. The same pattern was not observed in L. barahonensis–we therefore don’t yet know why this species curls its tail. Kircher speculates that the behaviour might have been directed at other, undetected, predators, or perhaps plays a role in lending stability to the lizard during locomotion.
This variation in the utilization of the same signal between two closely-related species points to the lability of signal use, and with almost 30 species in the genus, this system is a prime candidate for future work on signal evolution.
