<img src="https://www.anoleannals.org/wp-content/uploads/2020/05/Anole-Annals-Logo-375w.png"> Anole Annals

Species divergence is driven by a wide variety of forces, but two of the strongest predictors of speciation are the amount of time a lineage has persisted in a landscape, and the ability of lineages to move through a landscape. Lineages are more likely to diverge when they have occupied a landscape for a long time, and/or if their ability to move is restricted, thus limiting gene flow.

In his talk titled “Geographical factors promoting diversification of the northern Andes and Brazilian Cerrado regions: the case of frogs and Anole lizard species,” Carlos Guarnizo described his efforts to test whether these patterns hold true in both different landscapes and different taxa. He surveyed two herpetofaunal communities in two diversity hotspots in South America: frogs in the northern Andes mountain range and Anolis lizards in the Brazilian Cerrado. The montane Andean landscape is structurally complex and covers a range of altitudes, while the Cerrado region is a more uniform savannah-like environment, with intermediate structural complexity. Guarnizo used species distributions and genetic data to look at patterns of diversification across these landscapes to explore which landscape characteristics lead to higher levels of divergence and speciation.

He found that in both areas, topography was a strong predictor of divergence; specifically, more structurally complex landscapes led to higher levels of genetic divergence between sister lineages. These genetic breaks are also often deeper than previously realized, likely representing cryptic species. Despite these strong genetic splits, the niches occupied by sister taxa are generally well-conserved, lending support to the conclusion that landscape structure – rather than adaptive divergence – is responsible for the genetic divergence observed. Interestingly, in Andean frogs, Guarnizo found that the strongest genetic breaks did not occur across mountain peaks as previously thought. Instead, valleys appear to be the strongest geographic barrier to dispersal.

These cases show that landscape topography is a strong factor determining genetic divergence across different landscapes and taxa (including anoles), and may lead to high levels of cryptic speciation.

Evolution 2016: Using Anoles to Understand Shifts in Forests

By Kristin Winchell

Ivan Prates presents his poster at Evolution 2016.

Here at Evolution 2016 there have been a lot of anole talks and posters. In fact, there have even been several that pretend to not actually be about anoles. Ivan Prates presented a poster which he insisted, despite multiple pictures of anoles and the use of anole DNA, was not actually about anoles… Instead, this poster was actually about the historical extent of Brazilian forest cover (or so he says).

In short, Ivan used genomic data to understand historical patterns of dispersion and distribution of South American anoles in order to infer patterns of rainforest expansion and contraction. He suspected that the geological data gave a false interpretation of rainforest patterns in Amazonia and the Atlantic Forest in Brazil, and that anoles could help tell the true story of how the forests have changed over time. By looking at species with strong genetic signals associated with forest shifts he hypothesized that true forest patterns could be elucidated based on the historical demography of these species.

Ivan and coauthors looked at three species of lizards: Anolis punctatus, Anolis ortonii, and Polychrus marmoratus. They used the next-generation sequencing technique Genome by Sequencing (GBS) to answer three main questions: (1) Did all 3 species experience range expansions simultaneously? (2) Did populations expand and contract at similar points in time? (3) How did population sizes vary over time? While all three of these questions are about anoles, don’t forget that this poster was actually about the forest.

Ivan found that the Atlantic Forest individuals composed a monophyletic group nested within the Amazonian lineage. This suggests that the anoles of the Atlantic Forest on the coast actually arose from a single colonization event from Amazonia. The land between Amazonia and the Atlantic forest is presently quite arid compared to the rainforest – more like grassland. This presumably forms a barrier to contemporary dispersal, which implies that historical dispersal must have involved greater habitat connectivity. So Ivan’s results support the hypothesis that the forests experienced a drastic historical expansion creating a contiguous habitat that enabled dispersal around 1 million years ago. Interestingly, the timing for the dispersal of all 3 species was approximately the same. A million years ago seems to have been the ideal time to move to the coast for Brazilian anoles.

Ivan and his colleagues also looked at how populations size changed over time. He found that whereas Anolis punctatus experienced a trend of population expansion, Anolis ortonii and Polychrus marmoratus experienced population contractions. It was surprising to the authors that these species did not respond the same – why did only one of the species experience population expansions? They suspected that the expansion of one species might be related to the population contractions of the others, perhaps because of competition. However, their analysis on synchrony of population trends proved otherwise. They found that although trends within species were synchronized across populations, between species the shifts in demography were asynchronous. In other words, when one species expanded or contracted in population size, the others were stable. Ivan concluded that this was support for the idea that these populations were not influencing each other and that instead there was some other factor independently controlling population size fluctuations – perhaps precipitation patterns.

In conclusion, Ivan told me a lot about the demography of anoles during the Quaternary, and a little about the forest. I look forward to hearing more about his “forest” research on these understudied mainland anoles!

Click for a larger version of Ivan’s poster!

Evolution 2016: Ecomorphology in Caribbean Eleutherodactylus Frogs

By mjohnson216

Stephen Jay Gould famously claimed that evolution is “utterly unpredictable and quite unrepeatable,” and we Anolis biologists have relished in proving that statement wrong. In his talk in Austin this week, Alejandro Gonzalez Voyer of UNAM (with coauthors Alvaro Dugo Cota and Carles Vilá) showed that anoles aren’t the only Caribbean herps to exhibit the independent, repeated evolution of ecomorphs across islands – Eleuthrodactylus frogs have joined the club!

Among the remarkably diverse Caribbean Eleuthrodactylus species, nine ecotypes exist, including terrestrial, leaf-litter, aquatic, riparian, bromelicolous, arboreal, fossorial, cavernicolous, and petricolous specialists. Gonzalez and his coauthors first determined that these ecotypes evolved repeatedly, and showed that their distribution resulted from both invasion across islands and intra-island speciation. They also found that eight of the nine ecotypes cluster in morphological space and exhibit significant convergence. (The ninth, the fossorial ecotype, is composed of a monophyletic clade from Hispaniola and so convergence could not be tested.)

In sum, it appears that Eleutrodactylus ecotypes are indeed ecomorphs, and that evolution may be utterly predictable and quite repeatable after all.

Evolution 2016: Niche and Morphological Evolution in a Phylogenetic Context in Liolaemus

By Sofia Prado-Irwin

Photo by Nsimean

It’s true, they’re not anoles, but lizards of the genus Liolaemus form another extremely diverse clade, occupying one of the broadest climatic and elevational niche ranges of any vertebrate. Whether the ecological and phenotypic diversity of this genus are correlated, as is the case in adaptive radiation, remains an open question. Studies of the whole genus have shown that body size diversification is consistent with expansion into different ecophysiological niches, but other morphological traits don’t show the same pattern. Yet much of the ecology of the genus is unknown, so it is difficult to draw any definite conclusions.

In her talk “Evolution of niche and ecomorphological traits in a phylogenetic context in lizards of the Liolaemus bibroni complex,” Dan Edwards sought to address this gap in understanding of Liolaemus by focusing on one species complex within the genus, L. bibroni. The L. bibroni species group is composed of 26 species that occupy a broad range of habitats representative of those occupied by the genus as a whole. To explore their history of genetic and morphological diversification, Edwards constructed a phylogeny of the group, characterized rates of diversification, and measured a suite of relevant morphological traits. She found that there has been an increase in trait diversification over time, consistent with the colonization of new habitat types. In addition, she found that ecology and body size are significantly correlated, supporting previous results from studies of the genus as a whole. Other morphological traits were not as clearly associated with habitat type, but there do appear to be possible patterns of ecomorphological divergence in response to divergence in habitat. Edwards plans to further characterize the evolutionary relationships and explore more ecomorphological traits of Liolaemus species to resolve this question.

Evolution 2016: Combat and Display Traits Are Condition Dependent in a Central American Anole

By Sofia Prado-Irwin

Many exaggerated phenotypic traits, such as the large and colorful dewlaps of male anoles, increase fitness of individuals who possess them. But these traits are often energetically costly. Too high an investment in showy or extreme traits can come at the cost of an individual’s health and performance. Such traits are therefore said to be condition-dependent; that is, individuals will not develop them unless they are already in a healthy condition.

John David Curlis and colleagues explored several potential condition-dependent traits in two closely related Central American Anolis species, A. limifrons and A. humilis. He quantified a number of sexually and naturally selected traits and tested whether they varied by body condition to see whether any of them were condition dependent, and whether the degree of condition dependence varied between two closely related species. None of the traits he tested were condition dependent in A. limifrons, but two traits – jaw width and dewlap size – were condition dependent in A. humilis. He therefore concluded that the degree of condition dependence of these traits is evolutionarily labile. In addition, A. humilis dewlaps are generally larger than A. limifrons, which suggests that condition dependence may be a more important force affecting traits that are subjected to stronger sexual selection. Taken together, these results suggest that condition-dependence of sexually-selected traits may be playing a role in dewlap diversity (and perhaps other phenotypic traits) throughout Anolis lizards.

Evolution 2016: Evolution of the Thermal Niche in Anolis

By Sofia Prado-Irwin

Studies of adaptive radiation often focus on two main axes of divergence: the structural niche (e.g., where a species lives) and resource niche (e.g., what a species eats). In his SSE Symposium talk titled “The physiology of adaptive radiation,” Alex Gunderson explained the importance of a third, under-appreciated axis of species diversification: the thermal niche. Gunderson and colleagues tested whether different approaches to estimate the rates of evolution of the thermal niche lead to different conclusions, and whether thermal traits evolve at similar rates to classic ecomorphological traits like body size and limb length.

Scientists generally use three main approaches to quantify the thermal niche and estimate rates of thermal niche evolution: ecological niche modeling (ENM), organismal body temperatures, and physiological data (tolerance/sensitivity to different temperatures). Different studies use different approaches, but few use all three. Each of these metrics addresses a different scale of thermal biology, from broad environmental variables (ENM) to individual organisms (physiology). Gunderson and colleagues therefore predicted that estimated rates of evolution would vary based on the metrics used, and they used data from a number of Anolis species to test this prediction.

Specifically, the authors predicted that: a) ecological niche modeling approaches would estimate greater rates of thermal niche evolution, because environmental factors like temperature and precipitation used in ENM are very broad metrics, and are not necessarily directly correlated with individual thermal niche; b) organismal temperature data would estimate intermediate rates of thermal niche evolution, while it is a measure of individual thermal niche, it is also quite plastic; c) physiological measures would estimate the most conservative/low rates of evolution, because measures of thermal maxima and minima most accurately reflect the possible tolerance and sensitivity of individuals to thermal environments. They found that physiological data does indeed produce the most conservative estimates of thermal trait evolution, but their predictions about the performance of ENM and body temperature differed. Estimates of thermal niche evolution were highest when using body temperature data, and were intermediate when based on ENM. The fact that body temperature-based estimates of evolution rates were higher than ENM-based estimates suggests that researchers are generally underestimating error in body temperature measurements in the field.

After evaluating the results of these three different approaches in relation to thermal niche evolution, the researchers then compared rates of evolution of thermal traits to those of classical ecomorphological traits. When they used ENM, thermal traits seemed to evolve much more rapidly than morphological traits. In contrast, when they used physiological data, they found the opposite. Clearly, different metrics of climatic niche lead to different conclusions about evolutionary patterns. Gunderson therefore recommends incorporating aspects of multiple ecological and physiological scales when studying divergence of the thermal niche.

Evolution 2016: Genomic Insights into Anolis carolinensis Phylogeography

By Kristin Winchell

Anoles, in particular Anolis carolinensis, have long been considered an ideal group for studies investigating thermal physiology, reproductive endocrinology, and even regeneration. With the recent publication of the A. carolinensis genome (see AA posts on this here and here), the possibilities for new genomic studies in this new model species have significantly increased.

Joseph Manthey and co-authors used this new resource to clarify the phylogeographic relationships of A. carolinensis. Previous research on the phylogeography of A. carolinensis using both mitochondrial DNA and nuclear DNA showed that there were 5 clades. However, the relationships between these groups differed between the two approaches. Joseph looked at the genomes of 42 individuals from 26 localities across the native range to determine the true evolutionary relationship between regional groups and to shed light on the demographic histories of the groups. Manthey sequenced 500 loci using an anchored hybrid enrichment approach.

STRUCTURE analysis showed that the clusters had little admixture

Manthey et al. found that the genomic data predicted 5 genetic groups, in agreement with both the nuclear and mitochondrial analyses previously done. Their results also indicated that the 5 genetic clusters were distinct with little admixture. However, the relationships between groups did not agree with either the mitochondrial or nuclear trees, yet all nodes had extremely high support (93-100%)

Finally, Manthey commented on the likely timing of this diversification and associated demographic trends. Their results indicate that the initial split occurred during the late Miocene or early Pliocene and that the remaining diversification occurred during the Pleistocene. They also found that the most Southern population had a significant number of fixed genes while other populations did not. This suggests that this group was likely the oldest and most stable and supports an “out of Florida” hypothesis of diversification.

Evolution 2016: “Lightning” Strikes Three Times on Anoles in Afternoon Session: Character Displacement, Performance Trade-Offs and Opsin Evolution Matching Dewlap Color in Anoles

By mjohnson216

In this afternoon’s round of lightning talks, anoles were the focus of three fantastic (but short!) presentations on adaptation. It’s not easy to summarize a whole project in five minutes, but that’s just what these three speakers did, and each left me wanting to know more!

First, James Boyko, a Masters student working with Luke Mahler at the University of Toronto, described his work on morphological evolution in Lesser Antillean anoles. When similar species compete over a shared resource, there are two possible outcomes: extinction or divergence (i.e., character displacement). Lesser Antillean anoles are an excellent system in which to study the role of character displacement, as these islands all have either one medium-sized species, or one large and one small species. Further, the species on these islands represent two colonization events – one from the north, and one from the south. James first confirmed the classic pattern on body size evolution, finding that a three peak Ornstein-Uhlenbeck model (i.e., one that predicted large and small lizards on two-species islands, and medium lizards on single-species islands) best fit the observed data (consistent with Butler and King 2004). But when he analyzed 20 other ecologically-significant morphological traits, this three peak model did not predict trait evolution better than a model based on random chance, although the northern and southern clades significantly differed in these morphologies. In summary, to understand the evolution of Lesser Antillean anoles: body size matters, as evolution in body size is clearly an important factor to reduce inter-species competition, but lineage matters too, as body shape was predicted by ancestry.

Next came Ann Cespedes, a Ph.D. student with Simon Lailvaux at the University of New Orleans. Ann is studying functional trade-offs in green anoles (Anolis carolinensis), focusing on relationships between fitness and performance. Many studies have searched for these trade-offs in the past, and some have found them, but others haven’t. Why the discrepancies? Ann proposed that previous studies haven’t always considered sex differences in functional trade-offs, that measuring only two traits (one associated with fitness and one with performance) may not reveal real trade-offs, and that differences in individual quality are often ignored. To consider all of these factors, she measured a suite of performance and morphological traits in 60 male and 60 female green anoles. Illustrating the limitations of examining raw data on sprint speed and endurance, Ann found no suggestion of the predicted trade-off between these traits. But when using a composite measure of all performance measures (sprint speed, bite force, clinging ability, exertion, endurance, jumping ability, and climbing ability) as a control for individual quality, the trade-off between speed and endurance became clear. Males and females also differed in their speed-endurance trade-offs, as body size predicted performance in different traits between the sexes, and body shape predicted male but not female performance. So performance trade-offs do exist, but you have to know how to look for them!

To conclude the session, Alexander Stubbs, a graduate student in Jimmy McGuire’s lab at the University of California, Berkeley, described the differences between opsin gene expression in two Cayman Island anoles: Anolis sagrei (a species with a red dewlap that reflects long wavelength radiation) and Anolis conspersus (a species with a blue dewlap that reflects short wavelength radiation). Alexander proposed that these different dewlap colors might provide different selective pressures on opsins in the two species to allow better color discrimination and angular resolution. Using RNAseq to measure mRNA in the eyes of six males of each species collected at solar noon or at sunset, the results were exciting. As predicted, Anolis conspersus had higher expression of opsins that increase visual sensitivity to UV, blue, and green wavelengths, and Anolis sagrei had higher expression of opsins that increase long wavelength sensitivity. Alexander also found that gene expression different substantially between noon and sunset, and further, there was surprisingly little variation in opsin expression between lizards, in stark contrast to the wildly varying opsin expression observed in humans.

Evolution 2016: It’s Getting Cold in Here!

By Kristin Winchell

Tamara Fetters with her poster at Evolution 2016

Tamara Fetters, from the McGlothlin lab at Virginia Tech, reported on her ongoing work on thermal physiology in Anolis sagrei during the first poster session here at Evolution 2016 in Austin, Texas. Tamara looked at thermal tolerance and sprinting abilities at different temperatures and how that related to the latitude of the population. Specifically, she asked if lower temperatures regularly experienced by the Northern populations influence cold tolerance and performance at those temperatures. She expected that Anolis sagrei, native to Cuba and the Bahamas and introduced into the Southern U.S., would show signs of adaptation to its new, colder home in the more Northern mainland populations compared to the native range island populations in the South.

Tamara’s poster focused on two main experiments. In the first she calculated thermal tolerance to cold temperatures using a classic critical thermal minimum (CTmin) setup: with an ice bath she slowly lowered the body temperature of each animal until it was unable to right itself. This method approximates the minimum temperatures that the animals can handle in the wild. She found a clear trend showing a decrease in the minimum temperature tolerated as latitude increased. In short, Northern populations could handle the cold and Southern populations could not.

In the second experiment, Tamara acclimated the lizards to 6 temperatures ranging from 12-41 °C before running them up a track to calculate sprint speed. Tamara used an impressive 25-50 animals from each of 5 populations! She calculated sprint speed from the high-speed video she took using the program Kinovea. Tamara found that across all temperatures the most Southern population ran the slowest while the most Northern population ran the fastest, with the differences remaining fairly constant.

So what’s next for Tamara? She is planning on rearing animals in a common garden setup with some animals in hot temperatures with low variability between day and night (mimicking the native range, Southern habitats) and some animals in cool temperatures with high variability between day and night (as is experienced in the Northern habitats). She hopes that these studies will help her understand the genetic basis of this thermal tolerance and the extent of plasticity in thermal adaptation.

One last note – Tamara wanted to thank Anole Annals for helping her determine her study locations. She was able to determine which areas were likely to have Anolis sagrei and how far North they have spread because of Anole Annals posts (like this one) and comments.

Click to view a bigger version of Tamara’s poster

Evolution 2016: A Peculiar Case of Mitochondrial DNA Introgression in Puerto Rican Grass-Bush Anoles

By Jonathan Losos

On June 18, 2016