Anole Annals

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.”

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.

Reptiles are important models for studying phenotypic plasticity because they are quite sensitive to environmental conditions experienced during development, and naturally experience a broad range of environmental conditions during this time.  There are a number of interesting biological traits of reptiles that make them particularly interesting models for research on phenotypic plasticity. For example, temperature-dependent sex determination, where incubation temperature irreversibly determines sex during development, is a fascinating polyphenism that is widespread among reptiles.   Additionally, the sensitivity of developing embryos to environmental factors (like temperature or hydric conditions) has been implicated as a primary force behind the evolution of various maternal reproductive strategies including viviparity or nest-site choice. Accordingly, there exists a rich literature documenting the effects of embryonic environments on the phenotypes and survival of reptiles during early life.

A major shortcoming of this literature, however, is that the vast majority of studies terminate shortly after hatching. That is to say, our understanding of phenotypic plasticity in reptiles is biased towards phenotypes apparent in early life. Yet we rarely know if these phenotypes are persistent or transient, or if conditions experienced during development have delayed effects, or effects on reproductive traits.  Together with my coauthors Fred Janzen and Dan Warner, we have recently published a review that discusses the shortcomings of terminating plasticity studies during early life, and highlights the important contributions that have come from the relatively few long-term studies in existence.  We call for studies that specifically look at the effects of  embryonic environments on adult phenotypes, and offer a number of approaches to address this problem.

Enter the Anole.  There are a number of anole species that are very tractable models for experiments addressing the influence of embryonic conditions on adult phenotypes, reproduction, and survival.  Anolis sagrei, for example, readily breeds in captivity, is highly fecund, and reaches reproductive maturity in a matter of months. Anoles are tractable for detailed assays on reproduction in the laboratory, and raising anoles from egg to adult in the lab is entirely feasible under reasonable timelines.  Though it is no small task, it is very possible to incubate hundreds of anole eggs under different conditions, mark the babies upon hatching, and then release them into the field in a place where migration is not possible (like a small island).  Periodically sampling that island can give insights into the effects of incubation conditions on adult phenotypes and survival under natural conditions. Phil Pearson and Dan Warner recently published a paper using such a methodology.

Of course, we also encourage such long-term studies for everyone working with reptiles, even those that are very long-lived (like turtles).  But there is a dearth of studies that address the effects of embryonic environments on adult phenotypes in reptiles, and I hope that anoles are a key group that help address this shortcoming. So let’s get after it, Anolologists!!!!

From Nicholson et al. (2018)

Anole Annals has dropped the ball on staying current with recent papers about the systematics and taxonomy of anoles. So, here are two highlights over the last two years.

Last year, Steve Poe and 10 co-authors from five countries published a phylogeny including all species of anoles based on all available data. It was a tour de force and the paper was far-ranging, discussing the many implications of their phylogeny for anole evolution, biogeography and other topics. Among other topics, the paper sank a number of anole species, presented a phylogenetic taxonomy of anoles and argued that this taxonomy solves the problems posed in the debate on generic classification of anoles in the traditional Linnean taxonomic framework.

Here’s the abstract from that paper, published in Systematic Biology:

Anolis lizards (anoles) are textbook study organisms in evolution and ecology. Although several topics in evolutionary biology have been elucidated by the study of anoles, progress in some areas has been hampered by limited phylogenetic information on this group. Here, we present a phylogenetic analysis of all 379 extant species of Anolis, with new phylogenetic data for 139 species including new DNA data for 101 species. We use the resulting estimates as a basis for defining anole clade names under the principles of phylogenetic nomenclature and to examine the biogeographic history of anoles. Our new taxonomic treatment achieves the supposed advantages of recent subdivisions of anoles that employed ranked Linnaean-based nomenclature while avoiding the pitfalls of those approaches regarding artificial constraints imposed by ranks. Our biogeographic analyses demonstrate complexity in the dispersal history of anoles, including multiple crossings of the Isthmus of Panama, two invasions of the Caribbean, single invasions to Jamaica and Cuba, and a single evolutionary dispersal from the Caribbean to the mainland that resulted in substantial anole diversity. Our comprehensive phylogenetic estimate of anoles should prove useful for rigorous testing of many comparative evolutionary hypotheses.

This year in Zootaxa, Nicholson, Crother, Guyer and Savage published a paper following on Poe et al.’s. The paper does not have an abstract, but the title says it all: “Translating a clade based classification into one that is valid under the international code of zoological nomenclature: the case of the lizards of the family Dactyloidae (Order Squamata).” In short, the article argues that the traditional Linnean classification system is not going away any time soon, and that the clades recognized by Poe et al. are easily translatable into genera in the traditional system, as revealed in the figure above.

In a post just published, an administrator for Wikispecies asks if they should follow this proposed reclassification of anoles. If you have comments, please make them on that post.