Bailey Howell, a rising senior in Travis Hagey‘s lab at Mississippi University for Women, presented a poster at Evolution on differences in toepad morphology between urban and non-urban populations of Anolis cristatellus. The two of them coauthored the work with Kristin Winchell, who has been investigating morphological effects of urbanization in that species, and who captured A. cristatellus for the study. Bailey mapped their toepad landmarks and quantified a suite of toepad traits, including length and width, in a whopping 160 of them! She did this to investigate differences between individuals from urban and non-urban sites, with the goal of contributing to our understanding of the species’ adaptation to cities.
She ran some neat statistics for the project: first, a principal component analysis of all toepads scanned, which found differences in the degree to which urban and non-urban toepads are bent. She went one step further by running a canonical variate analysis to find which factors are maximally different between the urban and non-urban lizards. A scaled (pun unintended) figure from her poster of the theoretical most-urban and most-non-urban toepads is below (urban is in gray, non-urban is in green).
This CVA explained significant variation between the two populations, and accounted for 14.5% of the difference! Taking things a step further, Bailey analyzed size as well as shape from the traits she measured, and saw that urban toepads were wider, and, in particular, longer, than non-urban ones. Next steps for the project include adding more toepads to the dataset, analyzing the data in light of more (toepad and non-toepad) traits in these individuals, and looking for an effect on performance. It seems like they’re well on their way to understanding this important effect of urbanization in this species!
Emmanuel D’Agostino presenting his undergraduate research at Evolution 2019.
Emmanuel D’Agostino, a (recently graduated) undergraduate in the Losos lab at Harvard presented his undergraduate thesis at Evolution 2019. Working with Colin Donihue, Anthony Geneva, and Jonathan Losos, Emmanuel analyzed genetics, morphology, and mating behavior of Anolis sagrei collected from across their Bahamian range. Anolis sagrei differ pretty drastically in ecomorphological and sexually selected traits on different islands throughout the Bahamas. Emmanuel wanted to find out if this differentiation created barriers to mating among divergent populations on different islands.
Emmanuel analyzed an impressive 184 videos of recently paired males and females from different islands under laboratory conditions. (Emmanuel informs me that there were actually 234 videos but many he could not score because of uncooperative lizards hiding behind the planters and out of view of the camera – who knows what they did back there!). He then quantified latency to mate to see if individuals from different islands would mate freely and if willingness to mate was related to morphological differences. He combined his video analysis with genomic and morphological data to understand how genetically and morphologically distinct populations are.
Emmanuel found that individuals from different populations mate freely, suggesting no effect of premating isolation related to morphological disparity. He also analyzed a large number of linear models to tease apart the relative contributions of genetics and morphology and found that the most important predictor of mating success was relative head size – males with smaller head sizes correlated with increased likelihood of mating success! Intriguingly, in his final analysis he found that males that mated the quickest had decreased offspring survival rates. So even though smaller-headed males may mate more readily, their offspring are less likely to survive.
Anolisdistichus is a highly variable species from Hispaniola. It’s especially variable in its dewlap color, ranging from white, to orange, to red. In the past, A. distichus has been broken up into 16 subspecies based on its dewlap variation! Previous work by Rich Glor and his students used genetic data to identify six candidate species, although these six candidate species didn’t correspond well with the 16 dewlap-based subspecies. In order to get a better handle on how justified these candidate species are, undergraduate Tanner Myers, working with Pietro Longo Hollanda de Mello and Rich Glor, from the University of Kansas, presented a poster titled Identifying species when boundaries are blurred.
Myers collected morphological data from populations of A. distichus from across Hispaniola. The authors expected their morphological data to also partition along with the previously identified genetic candidate species. They found this to not be the case! When the authors looked at their morphological data (linear body, limb, and head measurements), to see if these 6 candidate species had any morphological divergence, they found no strong pattern. All of the candidate species clustered together to support one morphological group. In the end, the authors suggest that Anolis distichus may represent a highly variable group in in the early stages of speciation, but at this point, they do not support any taxonomic revisions of the species.
Tanner Myers will be starting graduate school with Jamie Oaks at Auburn University in the fall.
Climate change on earth is accelerating. These changes will have important impacts on all species, but some types of organisms are predicted to be affected more strongly than others. One such group is ectotherms which use the temperatures available in surrounding habitats to regulate their body temperatures. Another such group is mountaintop endemics. These species are restricted to one or several mountain peaks by climate and/or competition with other organisms. As such, they cannot easily disperse to other areas if climate makes their current habitat unsuitable!
Mountaintop endemic species may be particularly vulnerable to climate change (Chand Alli, CC BY SA).
Hispaniola contains several high elevation areas home to mountaintop endemic species, including anoles (NASA).
Many studies use correlative modeling approaches (often termed ecological niche models [ENMs] or species distribution models [SDMs]) to assess a species’ current distribution and predict its future distribution by projecting it into simulated future climate scenarios. This approach has some advantages including ease of implementation across many species. However, it has at least two potential drawbacks: the environmental data used in building such models are often measured at a fairly coarse scale that does not represent how many organisms use their environments, and the models do not explicitly include biological processes such as physiology and behavior.
Anolis armouri in a montane rock meadow (Reptile Database).
Vincent Farallo, a post doc at Virginia Tech, and his advisor, Martha Muñoz (both moving to Yale in a few weeks!), investigated whether incorporating physiology and behavior into modelling might affect predictions of climate change impacts on two mountaintop endemic anoles of Hispaniola, Anolis armouri and Anolis shrevei. Correlative SDMs (via BioMod2) predicted both species would lose much or all of their suitable habitat under climate change, perhaps leading to extinction. However, when Vincent constructed mechanistic niche models (via NicheMapR) that included knowledge about the thermal physiology and habitat use behavior of these species to predict activity time, they showed that habitat would increase in suitability under climate change, the opposite result! Interestingly, these models also predicted increased suitability for a widespread anole, A. cybotes. This result suggests that while climatic changes may not be a direct threat to these mountaintop anoles, increased competition with another anole, an indirect impact of climate change, may be.
Activity time of Anolis shrevei is predicted to increase across its range in Hispaniola with climate change (Farallo and Munoz).
As a whole, Vincent and Martha’s work shows that incorporating more mechanistic knowledge into models, including physiology and behavior, may be critical to predicting the impacts of climate change on organisms and making sound conservation decisions.
Periodically here on Anole Annals, we have posts about three-legged lizards. The most recent such post was last year from Miami. Here’s another lizard, with a twist: it’s got four legs, sort of. Looking at the floppy left hindleg of this lizard, caught in the Bahamas two years ago. An x-ray confirms that this is odd–there’s no bone in most of that limb! I’ve never seen anything like it, and wonder how it happened.
Despite this seeming impediment, the lizard looked quite healthy, and as the video shows, could run quite adeptly up a note pad.
And here she is when we released her back at the place where we caught her. Pretty nimble!
It seems hard to believe almost a year has passed since the last Evolution meeting. Last year we brought you coverage of the anole talks and posters in Montpelier, France. This year, we’re coming to you live from Providence, Rhode Island from June 22nd – 25th! This year there are eight talks and eight posters scheduled *(searching the schedule for keywords “anole” and “Anolis“). There’s some pretty fascinating topics on the schedule – here’s what you have to look forward to each day:
Saturday:
Habitat use, competition, and phylogenetic history shape the evolution of claw morphology in Lesser Antillean anoles (Yuan, Jung, Wake, Wang)
The effects of volcanic activity on the phylogeographic history of the Plymouth Anole, Anolis lividus, on Montserrat (Poster board #72) (Jung, Yuan, Wang, Frederick)
Identification and assembly of an anole sex-chromosome: Rapid degeneration since autosomal fusion? (Poster board #160) (de Mello, Hime, Glor)
Effects of urbanization on toe pad shape and lamellae size in Anolis cristatellus (Poster board #174) (Howell, Hagey, Winchell)
Monday:
Using archival DNA to elucidate anole phylogeny (Mayer, Gamble)
Comparative landscape genetics and epigenetics of two trunk-ground anoles (Wang, Wogan, Yuan, Mahler)
Ancient hybridization in the adaptive radiation of Anolis lizards on Puerto Rico (Wogan, Yuan, Wang)
Urban adaptation in anole lizards of the Greater Antilles (Poster board #7) (Winchell)
Cities in the Spotlight: Does Tolerance of Artificial Light at Night Promote Urban Invasions? (Poster board #97) (Thawley, Kolbe)
Adaptive radiation in the multidimensional phenotype (Bodensteiner, Muñoz)
Patterns of morphological diversity in Draconura clade anole lizards (Huie, Prates, Bell, de Quieroz)
Did we miss any? If so, let us know in the comments so we can be sure to add it to our schedules! We will be live blogging the meeting as usual, so check back starting June 22nd to hear about the latest in anole evolutionary research. And if you are attending the meeting, consider blogging a talk or poster for us (new contributors welcome!). Just send me an email and I will fill you in on all you need to know.
Anolis (Phenoacosaurus) heterodermus, a mainland anole that co-occurs with few or no other anole species
One of the most important questions in ecology and evolution is about the role of biotic interactions in driving phenotypic and behavioral changes across species. The insular Anolis species are a good model to address this kind of question due to their high abundance and pervasive ecological interactions across islands. Some insular species, however, live in isolation on small islands across the Pacific and Caribbean islands (21 species). These species have evolved similar morphologies across islands. For instance, Poe et al (1) found that body size evolved by exaptation (remember the classic Gould and Vrba 1982 paper) to colonize these small (and depauperate) islands successfully. By contrast, Poe et al. (1) showed that sexual size dimorphism (SSD) evolved by adaptation likely after island colonization to minimize intraspecific competition.
In brief, these solitary insular anoles evolved phenotypic (body size and SSD) traits by two different processes. Cool! But, what happens in mainland areas? Much work has been devoted to Caribbean species, but the mainland offers many more species and very little research has been conducted there to understand ecological and evolutionary processes. So, we decided to establish whether solitary ecology can be extended to mainland species or whether it is an island ecological phenomena.
The first problem that we had to resolve was trying to establish whether mainland species tend to live in geographical/ecological isolation as insular species. We adopted a novel concept in macroecology (the diversity field concept) developed by Mexican macroecologists (Hector Arita and Fabricio Villalobos see 2, 3) implemented here using extensive distributional information for almost all known Anolis species (377 spp), which I generated during my Ph.D. thesis (see 4 for an example using these maps). The diversity field concept allows us to establish how many species co-occur with a given species across its geographic range.
We calculated how many congeners can co-occur within the distributional area of each Anolis species using the range maps (see figure below). We divided mainland species into two groups: those co-occurring with few congeners (i.e., “solitary-like”, I had to say that his term did not like to reviewers, so we used a “species-poor” forms in the paper). Then, we test whether these “solitary-like” mainland species are different from other mainland species using a randomization approach. Our results revealed that “solitary-like” mainland species exhibit different traits from random mainland assemblages. These unique traits (i.e., uniform body size and greater SSD) suggest that solitary ecology from insular anoles can be extended to mainland settings.
Figure. Diversity fields for some Anolis species. Note that the diversity field is the set of richness values of co-occurring anoles inside each distributional area.
The next question was focused to establish whether similar (ecological and evolutionary) processes affected body size and SSD patterns in a similar way. We found that the phylogenetic position of body size and SSD shifts did not coincide and also with the evolutionary transitions to solitariness (i.e., reduced level of sympatry). We suggested that both traits are decoupled across the entire Anolis radiation and likely that both traits evolved exaptatively. In other words, it is possible to think that “solitary-like” species retained body size and SSD from their most recent common ancestors to facilitates the lonely life.
The paper is very short (less than 2500 words) and was published in the May number of Biology Letters(5).
In the most recent issue of Nature Ecology & Evolution, first-author Rob Pringle gives the inside skinny on the recent paper about the interaction of predation and competition among lizards (see the video description of the study).
Herewith, the essay:
I was heavily influenced by a handful of papers that were published during my first few years of graduate school. Some of these — Fine et al. (2004) on how herbivores promote habitat specialization in trees, Rooney et al. (2006) on food-web structure and stability — resonated because I could connect them to problems that I was working on. Others, such as Schmitz et al. (2004) on the ecological importance of predator-avoidance behavior, made an impression because they seemed to herald seismic shifts in the outlook of community ecology. And then there was a set of papers that captivated me with their sheer elegance: beautifully designed and executed field experiments that inspired me and made me jealous.
A string of papers by Tom Schoener, Dave Spiller, and Jonathan Losos belonged to this last category. There was a new one each year, with titles like “Predator-induced behaviour shifts and natural selection in field-experimental lizard populations” (2004) and “Island biogeography of populations: an introduced species transforms survival patterns” (2005). These studies used tiny cays in the Bahamas as arenas for a simple yet powerful experiment. On some islands, the investigators had introduced top predators — curly-tailed lizards (Leiocephalus carinatus), which occurred naturally on larger islands just a few stone-throws away from the experimental islands. A major aim of this work was to understand how the introduced predators affected populations of brown anoles (Anolis sagrei), which were native to the experimental islands.
The results were dramatic. Curly-tailed lizards are stocky, ground-dwelling animals, and they devastated brown-anole populations. The brown anoles that survived did so by climbing into the vegetation, beyond the reach of the curly-tails, and this behavioral shift was associated with natural selection on hindlimb length — an evolutionary consequence of predator-avoidance behavior. When I was a kid, we used to play a game called ‘the floor is lava’; if your feet touched the ground, you were dead. It seemed kind of like that for the brown anoles on these islands.
Left: Brown anole. Right: curly-tailed lizard. Photos: Jonathan Losos and Kiyoko Gotanda.
When I started a post-doc at the Harvard Society of Fellows in 2009, I met Losos and we started discussing ideas for a new experiment. I thought that a minor innovation on the earlier experiments could open up new conceptual territory. Losos said that he’d been wanting to do the same thing for years. To wit: if we introduced not just curly-tailed lizards, but also a second species of anole — green anoles (Anolis smaragdinus) — then we could ask questions about predation, competition, and the interaction between the two. Among other things, this design would enable us to test classic ideas about how predators affect the ability of competing prey species to coexist.
Green anole, characteristically perched on a thin branch in the canopy.
The risky thing about this idea was that so much of it had already been done to one degree or another. Previous work had painted a rich picture of the interaction between curly-tailed lizards and brown anoles — our odds of discovering something new on that front were low. And there were dozens of studies about competition between sympatric Anolis lizards. The novelty of our approach hinged on the interaction between predation and competition, which was a thin thread on which to hang such a massive undertaking. But I felt supremely confident that the experiment would work. Todd Palmer, Rowan Barrett, and a raft of other collaborators must have been confident too, because they joined me in setting up and monitoring the experiment.
Left: Aerial view of island 926; at left is a larger island, similar to those where we collected green anoles and curly-tailed lizards for introduction onto the experimental cays. Right: Naomi Man in ‘t Veld conducts a population census; squirt guns with water-soluble paint were used to mark lizards from a distance. Photos: Day’s Edge Productions and Kiyoko Gotanda.
By 2013, two full years into the study, my confidence was giving way to panic. I had started a job as an assistant professor in 2012; I was anxious about my professional survival, and I had ploughed large amounts of time and money into an experiment that did not seem to be working after all. The introduced curly-tailed lizards were firmly established in their new homes, and the brown anoles were responding by becoming more arboreal, as previous work had indicated they would. But the introduced green-anole populations seemed to be struggling. It looked as if they might die out, in which case our experiment would amount to a very expensive confirmation of the earlier work by Schoener, Spiller, and Losos. Our project had some original twists — Tyler Kartzinel was spearheading an effort to monitor the lizards’ diets using DNA metabarcoding — but it wasn’t at all clear that we would discover anything new or noteworthy.
Our break came in 2014, when it became clear that the green-anole populations were indeed thriving on some islands — just not on any of the islands with curly-tailed lizards. When we returned to the Bahamas in 2015, buoyed by the emerging results and freshly funded by the US National Science Foundation, we found that green anoles had disappeared on one island with curly-tailed lizards (the largest such island). Sometime during 2016, a second green-anole population vanished, this time from the smallest island with curly-tailed lizards. That left just two islands where green anoles still persisted in the presence of curly-tails, and one of those populations looked like it might soon join the list of casualties. Was this because the curly-tailed lizards were simply eating the green anoles to extinction on those islands? Probably not. The green anoles were highly arboreal; they rarely descended to the ground and instead moved by scampering through the twigs and leaves in the canopy. The chunky curly-tailed lizards, by contrast, lumbered across the ground, rarely climbing higher than 50 centimeters — and then only on the thickest of tree trunks. Indeed, the curly-tails didn’t seem to be eating many lizards of any kind. We saw them feasting on cockroaches, and occasionally snacking on fallen fruits and dead hermit crabs, but it wasn’t until 2016 that we finally saw one eat a small female brown anole. Isotopic analysis revealed that curly-tailed lizards actually occupied a slightly lower trophic position than did either anole species, which suggested that the top predator was subsisting more on insects than on other lizards.
Left: Curly-tailed lizard eating a cockroach; the lizard’s paint marks signify that it had been seen on the first two days of the three-day population census. Center: Mating green anoles were a welcome sight in 2013. Right: Green anole clinging to a thin twig, where we often found them, especially on islands with curly-tails. Photos: Kiyoko Gotanda and Rowan Barrett.
The more plausible explanation for our results was that the presence of curly-tailed lizards intensified competition between the two anole species within the predator-free arboreal refuges, and that this competition — not direct predation — was the primary reason why the introduced green-anole populations failed to increase on islands with curly-tailed lizards. Molecular analysis of fecal samples subsequently reinforced this impression. DNA metabarcoding produced evidence that curly-tailed lizards exacerbated the competition between brown and green anoles for insect prey. And a quantitative PCR assay — conducted by Charles Xu at the behest of one of the four very thoughtful reviewers for Nature — detected the DNA of brown and green anoles in just 4% of the curly-tailed lizards that we sampled. Curly-tailed lizards really were the top predators; they just didn’t catch anoles very often.
We concluded that indirect effects of the top predator destabilized the coexistence of competing prey species. In the landscapes of fear created by curly-tailed lizards, the clear niche partitioning exhibited by brown and green anoles on predator-free islands — a product of adaptive radiation — was no longer evident. Instead, these species were trapped together in the top story of the small islands, competing for the same space and food, afraid of getting burned by the hungry predators on the ground. Green anoles, despite being better adapted to arboreal life, got the shorter end of the stick (both literally and figuratively). This might be because brown anoles, as the incumbents on the islands, had greater strength in numbers. If we had introduced both brown and green anoles at identical starting numbers, would the green anoles have come out on top? Or, now that the combination of competition and predation has greatly diminished brown-anole populations, might green anoles stage a comeback? In 2018, we reintroduced green anoles on the two islands where they had been extirpated, with the hope of answering this question.
In any event, our findings ran counter to one of the motivating hypotheses of the project. Early studies, notably Bob Paine’s classic experiment in the rocky intertidal habitats of Makah Bay, suggested that predators tend to ameliorate competition between species at lower trophic levels by preventing any one species from becoming too abundant and excluding the others. Many ecologists, myself included, love this idea of ‘keystone predation’. Not only is it an elegant concept, but it also validates top predators as linchpins of ecological integrity. But when can we expect predators to play this role? In rocky intertidal communities, where keystone predation is a powerful force, sea stars feed on sessile invertebrates; but prey that are attached to the substrate have a limited ability to escape predators in space. In predator-prey interactions involving fast-moving prey that can rapidly adjust their behavior to avoid predators, I would expect keystone predation (sensu stricto, as opposed to the broader concept of ‘keystone species’) to be infrequent, and competition for enemy-free space to be both frequent and strong.
Left: The crew of the Sand Crab prepares to disembark on an island (from left: Naomi Man in ‘t Veld, Todd Palmer, Rowan Barrett, Tim Thurman). Center: When the Sand Crab got stuck at low tide, we had to walk (from left: Palmer, Pringle). Right: When the seas were rough, we contemplated our own mortality (from left: Palmer, Man in ‘t Veld, Pringle, Thurman). Photos: Kiyoko Gotanda and Rowan Barrett.
It has now been almost a decade from the conception to the publication of this work. What started out as a post-doc project has become an enduring annual ritual, and one that I have (usually) been able to enjoy thanks to a talented group of collaborator-friends: Palmer, Barrett, Kartzinel, and Xu, along with Tim Thurman, Kena Fox-Dobbs, Matt Hutchinson, Tyler Coverdale, Josh Daskin, Dominic Evangelista, Kiyoko Gotanda, Naomi Man in ‘t Veld, Hanna Wegener, and Jason Kolbe — and, of course, Schoener, Spiller, and Losos.
The research team left it all on the field. Tim Thurman (left) required stitches after one nasty fall; later (center), he was possibly sick (or simply didn’t want anybody to steal his water). Todd Palmer (right) was forced to become arboreal in his search for green anoles. Photos: Rowan Barrett and Kiyoko Gotanda.
The interdisciplinarity of this team enabled what is to me the most satisfying feature of our work. We were fortunate to have access to a replicated set of small cays on which to manipulate species composition. That is a rare opportunity and would have made for a nice study in itself. But by also integrating molecular assays (to quantify diet composition and intraguild predation) and stable-isotope analyses (to quantify trophic position and food-chain length), we were able to gain deeper insight into the mechanisms underlying the population dynamics. Indeed, without these additional assays, our suppositions about the relative importance of consumptive and non-consumptive effects would have been equivocal at best. Molecular techniques have fully entered the mainstream of ecology over the past decade, yet they are still rarely paired with the kind of manipulative field experiments that so inspired me as a first-year graduate student. The fusion of sound natural history, rigorous experimentation, and forensic mechanistic exploration offers tremendous power to resolve the kind of messy complexity that has long frustrated ecologists.
