Anolis bartschi. Pinar Del Rio Cliff Anole (Viñales, PR).
Cuba is the largest island in the Caribbean and has the highest diversity of Anolis lizards with 64 currently known species. Here I share few anole photographs taken in the wild with a Canon EOS D80 during some expeditions to the island.
Figure 1. Anolis punctatus, South America’s coolest lowland anole – literally. Picture by Renato Recoder.
In ectothermic organisms, environmental factors such as temperature and water availability constrain physiological and behavioral performance. Therefore, the occurrence of species in varied environments may be associated with local adaptation. On the other hand, experimental studies have shown that physiological function can be highly conserved within species over broad environmental gradients, which may be associated with the homogenizing effects of population gene flow. In a recently published study, we focus on widespread South American anoles to investigate whether the occurrence of species in distinct environments is linked to local adaptation and whether population structure and history have constrained adaptive differentiation.
Based on molecular data, my collaborators and I have previously found that arboreal lizard species have independently colonized the Atlantic Forest from Amazonia, subsequently expanding southward towards subtropical regions. This is the case of Anolis ortonii and Anolis punctatus (Fig. 1), whose ranges now encompass a climatic gradient from warm and wet conditions in Amazonia to cooler and less rainy settings in the Atlantic Forest. Our new study investigates whether species establishment in distinct climates is associated with potentially adaptive genetic differentiation between populations. To this purpose, we implement genome-environment association analyses on the basis of thousands of restriction site-associated DNA markers. Moreover, to estimate levels of gene flow – a force that could oppose adaptive differentiation – we perform historical demographic inference under a genetic coalescent framework. Lastly, to characterize the climatic gradients presently occupied by A. ortonii and A. punctatus, we estimate climatic space occupancy over their ranges.
Analyses of genetic structure inferred distinct populations in Amazonia and the Atlantic Forest in both anole species (Fig. 2), suggesting that separation of these forests following a period of contact in the past has favored genetic divergence. In the two species, historical demographic analyses inferred large effective population sizes, mid-Pleistocene colonizations of the Atlantic Forest from Amazonia, and post-divergence population gene flow (Fig. 3). These results support the hypothesis of recurrent rainforest expansions that connected presently disjunct biomes in northern South America.
Figure 2. Genetic clustering based on all SNPs from Anolis ortonii (A) as well as all SNPs (B) and candidate SNPs only (C) from A. punctatus. Proportions in pie charts on maps correspond to ancestry coefficients estimated by genetic clustering analyses. Grey areas on map indicate South American rainforests. Red arrows indicate A. punctatus sample MTR 20798 from Pacaraima on the Brazil-Venezuela border in the Guiana Shield region, a locality that is climatically similar to Atlantic Forest sites (see Fig. 4); this sample is genetically more similar to eastern Amazonian samples based in the entire SNP dataset, yet more similar to Atlantic Forest samples based on the candidate SNPs only.
Figure 3. Population history (from SNAPP) and historical demographic parameters (from G-PhoCS) inferred for Anolis ortonii (A) and A. punctatus (B). Parameters are the time of coalescence between populations (in millions of years, Mya), effective population sizes (in millions of individuals, M), and migration rates (in migrants per generation, m/g). Colors of terminals correspond to genetic clusters in Fig. 2.
Genome-environment association analyses found allele frequencies of 86 SNPs in 39 loci to be significantly associated with climatic gradients in A. punctatus. Among the candidate loci, eleven uniquely mapped to known protein-coding genes in the reference genome of Anolis carolinensis; two mapped non-specifically to more than four genes; and the remaining mapped against non-coding regions, which may correspond to regions that regulate gene expression or that are physically linked to genes that underwent selection. In the case of A. ortonii, no SNPs were associated with temperature and precipitation variation across space. Constraints related to population structure and history do not seem sufficient to explain discrepant signatures of adaptation between the two anole species; instead, this discrepancy may be related to species differences in climatic space occupancy over their ranges (Fig. 4).
Figure 4. Environmental space occupancy along latitude based on climatic PC1 for Anolis ortonii and A. punctatus. Samples used in genetic analyses are indicated with a black dot. Higher PC scores correspond to drier and colder sites. Dashed line indicates the approximate region of a pronounced north-south climatic turnover in the Atlantic Forest identified by previous studies. Red arrow indicates A. punctatus sample MTR 20798 from Pacaraima, a mid-elevation site (820 m above sea level) in the Guiana Shield region that overlaps climatically with Atlantic Forest sites (horizontal axis). Note that the two species experience largely similar climates in Amazonia and the northern Atlantic Forest, yet A. punctatus occupies cooler and less humid localities that are not occupied by A. ortonii in the southern Atlantic Forest.
The candidate genes identified in A. punctatus play essential roles in energy metabolism, immunity, development, and cell signaling, providing insights about the physiological processes that may have experienced selection in response to climatic regimes. Similar to our study, other investigations of anole lizards found differences in the frequency of alleles that underlie ecologically relevant physiological processes between populations that inhabit contrasting habitats. These examples support the hypothesis that adaptation to colder climates has played an essential role in range expansions across anole taxa, including mainland and Caribbean forms that span altitudinal and latitudinal gradients.
Anolis ortonii. Spotting this cryptically colored rainforest anole is quite challenging indeed. Picture by Miguel T. Rodrigues.
This investigation illustrates how studies of adaptation on the basis of genome-environment association analyses can benefit from knowledge about the history of landscape occupation by the species under investigation. Data on population structure and history can provide insight into how gene flow and natural selection interact and shape population genetic differentiation. Moreover, information about the direction and routes of colonization of new habitats can support spatial sampling design, help to characterize landscape gradients, and support the formulation of hypotheses about how organisms have responded to environmental variation in space.
To know more:
Prates I., Penna A., Rodrigues M. T., Carnaval A. C. (2018). Local adaptation in mainland anole lizards: Integrating population history and genome-environment associations. Ecology and Evolution, early view online.
Photo By Kester Dass
The latest field guide to the amphibians and reptiles of Trinidad and Tobago came out in early 2018. In it, eight Anolis species were documented. My fellow contributors on this latest article published in Caribbean Herpetology now report on a ninth anole for the country: ehe Puerto Rican Crested Anole.
Most of the other introduced anoles to Trinidad and Tobago have been spreading from their first documented sighting , such as Anolis wattsi. One wonders, how successful will these introduced anoles be in their non-native islands and what ecological effect they may have on the native fauna, including the native anoles? This is something I would like to investigate further. Any input on this from your experiences would be welcomed.
Available climatic space showing the position of each pixel predicted as presence from ecological niche modeling across all Caribbean islands.
One of the most interesting patterns in the insular anole radiation is the observation that the majority of species are single-island endemics (150 of out 166 species). This observation in the Caribbean anole lizards has been known from a while and several studies have attempted to establish the underlying causes of this striking pattern (e.g., 1, 2, 3).
In a recent study, as part of my PhD dissertation, I used a different approach to try to understand why most of these species are unable to colonize other islands. I used a recently developed conceptualization to link abundances and ecological niche requirements at coarse-grain scales; this approach has been developed in the lab of my advisor (see 4, 5, 6; but see 7, 8, 9 for discussions and counter-examples; this approach has been strongly debated in the literature in the last years).
We used ecological niche modeling -ENM- to predict species’ distributions across all Caribbean islands for each species with at least 10 occurrence records. We estimated the position of each pixel predicted as presence in the ecological space using Euclidean distances. In short, we characterize all pixels for a single species and calculated which of these were close to the niche centroid (which we assume as the best conditions for species presence) and which were close to the niche periphery (see figure above). We predicted that pixels predicted by ENM as presences within each native island will be more close to the niche centroid and those predicted as presences in other islands will be in the periphery of the niche.
We found that many species follow the predicted pattern; in other words, we found that the “best” niche conditions are in the native island regardless of climatic heterogeneity observed in each island and the “worst” niche conditions are outside native islands. We also used other metrics to corroborate our results. We interpreted these results as instances of recent climatic niche conservatism (within lineages) and therefore this operates as a constraint in the ability of each species to colonize other islands (i.e. due to the low suitable climatic conditions for successful population establishment). We only gathered data for 70 species and therefore it will be necessary more data and more studies (including physiological experiments) to corroborate our assertions.
Also, we examined the pattern of realized climatic niche shifts across the anole radiation and we found evidence of several instances of climatic niche convergence. We concluded that anoles evolved to occupy different portions of the climate space and in several cases evolved quickly to occupy some portions of this space (e.g., cold climatic conditions) and recently most of these species likely adapted very well to climatic conditions in their. native islands.
The paper was published in Evolutionary Biology.
Anolis evermanni on the boulders in the stream at the El Verde Field Station. Photo by Jonathan Losos
My former postdoc advisor and AA co-founder Jonathan Losos recently reminded me that I left some unused samples in a drawer in the lab that he has now moved out of.
In 2012, I spent some time in Puerto Rico, collecting niche data for six anole species (A. cristatellus, A. evermanni, A. gundlachi, A. krugi, A. pulchellus and A. stratulus) among other things. I collected some samples for stomach content and stable isotope analysis that I never got around to processing before I moved on to the next postdoc. As I’m now based in New Zealand and back to working on fish, it’s not worth the complications of importing samples that I don’t have immediate plans to use.
Anolis gundlachi. Photo by Travis Ingram.
At Jonathan’s suggestion, I am making the samples available to any anologists who can give them a good home. The data are unlikely to lead to anything groundbreaking, but could make for a nice integrated study of niche partitioning and could be a good student project for someone.
The samples contain:
• Stomach contents from at least 30 anoles of each of the six species, obtained via gastric lavage and stored in ethanol in eppendorf tubes.
• Tail tips taken for stable isotope analysis, dried and stored in eppendorf tubes.
• Dried tissue samples from herbivorous (katydids x 10) and detritivorous (land snails x 10) invertebrates to use as isotopic baselines.
• Additional pieces of the same tail tips, stored in ethanol in Eppendorf tubes, which could be used for genetics if needed.
The samples should still be in good shape, though they’ve spent the last six years boxed up in a drawer. All the anoles were released live, so I don’t have specimens. However, for each individual I have recorded:
• collection date, GPS location and elevation
• environmental temperature
• body (cloacal) temperature
• perch height and diameter
• body orientation and position in sun vs shade
• sex and SVL
The idea behind collecting these data was to quantify how much of the variation in different niche dimensions was attributable to differences between ecomorphs (trunk-crown, trunk-ground and grass-bush), between species (two species per ecomorph), and between sexes. I would be happy to donate the samples to someone who can make good use of them, or to collaborate with someone who would like to follow up on this small project idea.
If you are interested in taking over the samples, please get in touch with me in the next couple of weeks (after that they will likely be disposed of).
Travis (email)
Female Festive Anole (photo: Ambika Kamath)
The evolution of reproductive strategies is an interplay between phylogenetic constraints (i.e. restrictions determined by the evolutionary history of that organism) and local conditions. Organisms adapt their reproductive physiology to their environment in ways that maximize fitness; however, this occurs within the context of evolutionary history (e.g. income vs. capital breeders). When environments are seasonal, selection favors individuals that align changes in key reproductive traits (e.g., egg size, clutch size) with seasonal shifts in habitat quality. For example, some species of aphids switch from asexual to sexual reproduction in the fall of each year because offspring produced via sexual reproduction (i.e. genetic recombination) are more likely to survive the winter. Seasonal shifts in reproduction have been observed in a variety of taxa (e.g. birds, mammals, frogs, lizards, spiders).
In two previous papers, the Warner Lab demonstrated that brown anoles (Genus-pending sagrei) in Florida, exhibit seasonal shifts in reproduction (Mitchell et al 2018; Pearson & Warner 2018): females shifts from producing many, relatively small offspring early in the year to producing fewer, relatively large offspring late in the year. Pearson and Warner (2018) also demonstrated that anoles that hatch early in the season (March – May) are more likely to survive through winter than those that hatch later (July-August). Thus, the observed shift in reproduction appears to be an evolved response to the seasonal decline in offspring habitat. This shift in reproduction, however, may depend on environmental factors that are also subject to temporal changes (e.g., food abundance).
In a new paper (Hall et al 2018) published in Physiological and Biochemical Zoology, we demonstrate how prey abundance modifies seasonal changes in key reproductive traits for brown anoles. We bred lizards in controlled laboratory conditions across the length of a full reproductive season and manipulated the availability of food by providing some breeding pairs high prey availability and some low. Halfway through the season, we switched half of the breeding pairs to the opposite treatment. We measured growth of male and female lizards as well as latency to oviposit, fecundity, egg size, egg content (yolk, water, shell mass), and egg quality (steroid hormones, yolk caloric content) over this period.
Higher prey availability enhanced lizard growth and some key reproductive traits (egg size, fecundity), but not others (egg content and quality). Notably, egg quality seems unaffected by diet. This is probably because there is some minimum provisioning that is necessary to produce a viable egg. Thus, females on a low-calorie diet will sacrifice the number of eggs produced and not the quality; however, increased food supply will be primarily used to increase fecundity.
We also found that seasonal patterns of reproduction were modified by prey treatment in ways that have consequences for offspring survival (Fig 1). When prey was abundant, egg production peaked relatively early in the season and egg size increased through time; however, when prey availability was low, egg production was chronically low and egg size declined through time. Late-produced offspring are at a disadvantage because they have to compete with larger, established offspring that hatched earlier in the year. A low calorie diet prevents females from providing late-season offspring with the extra provisions they need to compensate for hatching late.
Figure 1. Egg production of brown anoles provided with a) continuously high prey availability; b) high prey availability switched to low; c) continuously low prey availability; d) low prey availability switched to high. The vertical dotted line represents the point in the experiment when the diets were changed for groups b and d.
Figure 2. The relationships between latency to oviposit and a) prey treatment and b) pre-season body condition. Dark bar/circles show the high prey treatment and white bar/circles show the low prey treatment.
Not shockingly, when the diets were switched halfway through the season (high prey switched to low or the reverse; Fig 1) females responded immediately to the new diet. This would suggest that anoles are primarily income breeders that utilize energy intake to fuel reproduction. However, we know that income and capital breeding is a continuum and many reptiles utilize both for reproduction. We also found that females with a relatively high body condition at the beginning of the experiment start laying eggs earlier than those with poorer body condition (Fig 2). These measures of condition were taken prior to the onset of reproduction and couldn’t have been confounded by the presence/absence of oviductal eggs. Like many reptiles, pre-season body condition (i.e., fat reserves) may play an important role in the initiation of reproduction (vitellogenesis) for anoles; however, once reproduction starts, income is likely the primary determinant of fecundity.
Our results demonstrate that seasonal changes in anole reproduction are dependent on fluctuations in local environmental conditions.
Photo by Dante Fenolio
From Facebook:
The results of the informal, unscientific, potentially bogus poll would seem to indicate that the answer is a resounding “No.”
Welcome to the first of what will be a series of primers on identifying Mexican Anolis lizards. When I was first becoming familiar with Mexican anoles, there were a few traits that stood out as being valuable for identification purposes. The goal is to make some posts outlining the traits and how to use them to identify anoles if you ever have the need. Let’s get started!
To begin, I want to stress how difficult it can be to identify many anole species in Mexico. The majority of species in the country are variable in dorsal patterning and roughly the same size (~40-60 mm SVL). On one of my early trips, I was shocked to find that four sympatric species in Guerrero had essentially identical size and dorsal patterns. Identifying them to species can be tricky if the individual in question is a female or juvenile, making it difficult to use dewlap coloration as the primary diagnostic trait for identification. Interestingly enough, one of the best ways to rule out species was to look at size and keeling of dorsal and ventral scales.
Scott Thomson, an administrator for Wikispecies, is pondering whether to adopt the proposed classification of anoles, splitting the group into eight genera, and wants to know what the community thinks. Here’s your chance to weigh in!
If you want to learn more, read Scott’s post and comments on it.
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