All posts by Pavitra Muralidhar

Sex Ratios and Sexual Selection in Anolis lizards

The adult sex ratio is an important characteristic of a population, influencing the number of available mates in an area, the strength of sexual selection, and the evolution of mating systems. In our new paper in the Journal of Zoology, Michele Johnson and I use anoles to look at variation in sex ratios within and across species within a clade.

Photo by Michele A. Johnson

Photo by Michele A. Johnson

This paper had its roots when Jonathan Losos put me in touch with Michele in my first semester of grad school. Michele had compiled a massive database of detailed behavioral observations for Anolis populations and species across the Greater Antilles during her PhD on territoriality and habitat use (see Johnson et al. 2010 for more details!). While still trying to familiarize myself with the data set, I came across papers by Bob Trivers on sexual selection in anoles and his publication on the name-sake Trivers-Willard hypothesis; the combination of these topics made me curious about sex ratios and their role in sexual selection. I decided to quickly calculate the sex ratios of our localities, and given their distribution, realized that we should definitely look into this more.

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Sex ratios are generally very hard to measure in the field. You need to be certain that you haven’t had any biased sampling, or in other words, that you’ve made a fair attempt at censusing the population. This is quite difficult during short sampling periods! However, Michele conducted extended behavioral observations, and carefully tagged and monitored every individual in large habitat areas for ~3 weeks in each locality. This meant that we could be fairly confident that she had captured every individual in the population during her sampling periods, and her total counts of male and females in the population would be accurate. Even more, she had these adult sex ratios for 14 species, with some of those species being sampled at multiple localities. Given these data, we could actually both look at sex ratios across the Anolis clade, and within multiple anole species, for the first time.

We had two main questions: 1) were the sex ratios of these anole populations significantly skewed (i.e., were they very far off  from a 50:50 male-to-female ratio?) and 2) did the adult sex ratio of a population correlate with the strength of sexual selection in that population? For question 2, we used two measurements of sexual size dimorphism as a proxy for the strength of sexual selection. Sexual selection generally drives an increase in sexual size dimorphism (i.e., the difference between males and females in body size), but is also thought to be related to sex ratio skew (as the more skewed a population sex ratio, the more competition for mates or mating opportunities). We predicted that species with more skewed sex ratios would show an increase in sexual size dimorphism. Given that ecomorphs are an important component of evolution in anoles, and are commonly associated with varying levels of sexual size dimorphism, we also decided to test for a correlation between sex ratio skew and ecomorph type.

We found that sex ratios varied widely across and within anoles, ranging from a very female biased 0.32 in Anolis krugi to a male biased 0.61 in Anolis smaragdinus (sex ratios are expressed as the total number of adult males divided by the total number of both adult males and females in the population). Adult sex ratios also varied between different localities within a species (we had six species with multiple localities). We found two populations with significantly skewed sex ratios (Anolis krugi and Anolis valencienni) but based on Fisher’s test of combined probabilities, the sex ratios of anoles overall are not skewed away from 50:50.

I should note, however, that it is intrinsically extremely difficult to detect a skewed sex ratio in a natural population. We’re trying to measure deviations from a 50:50 sex ratio, and this requires surprisingly high population sizes since the binomial distribution has a broad center. For instance, to detect a true underlying sex ratio of 0.4 or 0.6 (away from our null of 0.5), we would need population sizes of >780 lizards to detect a significant skew 80% of the time. This is just an illustration, but the main point is that these population sizes might not exist for a given species – and so detecting significantly skewed sex ratios might not be possible at all. This is especially difficult when looking at small or endangered populations – there sex ratio skew might be a big problem, but impossible to demonstrate statistically. The general takeaway here is that sex ratio skew in a population can be biologically important, but not statistically significant.

We then used both the categorization of the anole species by sexual size dimorphism (low or high SSD) and the measured sexual size dimorphism of each population (calculated by average male SVL divided by average female SVL, minus 1). We used both of these estimates of SSD to test whether the sex ratio of a population correlated with the sexual size dimorphism of that population, as predicted by sexual selection theory. Turns out we were completely off – there was really no correlation between sex ratio skew and measured SSD, categorical SSD, or ecomorph (see figure 1, posted below,  for a visual of this lack of correlation!).

Figure 1 (from the paper) : Sex ratio versus sexual size dimorphism. Sex ratio is represented as the proportion of males among adults in the population, while sexual size dimorphism was calculated dividing the average SVL of the larger sex by the average SVL of the smaller sex, and subtracting 1 for each population. Each circle represents 1 of the 21 localities sampled in this study. The dashed line represents an equal sex ratio of 0.5. We found no relationship between sexual size dimorphism and sex ratio across the 21 localities (PGLS: adjusted R2 = −0.08, P = 0.86).

Figure 1 (from the paper) : Sex ratio versus sexual size dimorphism. Sex ratio is represented as the proportion of males among adults in the population, while sexual size dimorphism was calculated dividing the average SVL of the larger sex by the average SVL of the smaller sex, and subtracting 1 for each population. Each circle represents 1 of the 21 localities sampled in this study. The dashed line represents an equal sex ratio of 0.5. We found no relationship between sexual size dimorphism and sex ratio across the 21 localities (PGLS: adjusted R2 = −0.08, P = 0.86).

So what’s the general message here? Sexual size dimorphism does not correlate with adult sex ratios across anole species, and so the relationship between strength of sexual selection, sex ratio bias, and sexual size dimorphism may be more complicated than we initially assumed. However, anole sex ratios can range widely between species, and within populations. Given the variance within anole species, the adult sex ratio is probably a better description of a locality, or population, than an intrinsic quality of an entire species. We also think that the influence of various localized environmental factors may impact sex-specific mortality or dispersal, which in turn which cause differences between localities in adult sex ratio skew.

This is my first anole paper, and it’s really nice to see all the brainstorming and discussions put into print. It was also great to get to know and work with Michele, and learn more about her research and behavioral work in anoles (we even got to meet in person at the Evolution conference last year!). This paper was also my first small step into the world of sex ratio and sex determination theory which now forms a large part of my PhD work, so I’m very grateful for the introduction to the subject. Anyway, feel free to email us with any questions and we hope you enjoy the paper!

Paper here: Sexual selection and sex ratios in Anolis lizards

 

Parallel Evolution of Color Pattern in the Anoles of the Lesser Antilles

Parallel evolution and convergent evolution are big themes within anole biology, so our lab was excited to discuss a new paper by Thorpe et al looking at these concepts in Lesser Antillean anoles. The paper focused on evidence for parallel evolution across seven small islands that contained both xeric and montane habitats with at least one species of anole split between the two habitats. Xeric habitats tend to occur along island coasts and are hotter, drier, and have less canopy cover, while montane habitats occur in the interior of islands and are cooler and wetter. There are many physical differences consistently found between the anoles associated with each type of habitat, even within a species; perhaps the most obvious examples are the repeated differences in skin color and pattern between habitats, beautifully illustrated in the first figure of the paper.

Figure 1 from Thorpe et al, showing the repeated evolution of charecteristic xeric and montane color patterns in the Lesser Antilles

Figure 1 from Thorpe et al, showing the repeated evolution of characteristic xeric and montane color patterns in the Lesser Antilles

Thorpe et al. set out to conduct tests of parallel evolution among seven anole species using 18 phenotypic traits that vary between habitats, including both morphological and pattern measurements. In addition, they used mitochondrial DNA sequencing to produce a new phylogeny of these species and control for phylogenetic interference in their comparisons. The authors first used a principal components analysis to confirm that the major source of climatic variation is found within each island and between different habitats, rather than across different islands. The authors found convincing evidence for parallel morphological evolution in multiple phenotypic traits, especially those associated with skin pattern and hue: anole populations in xeric habitats consistently converge on a grey skin color and those in montane habitats converge on green. Thorpe et al. also go on to suggest that divergence in coloration may be the result of signal optimization in environments with different chromatic backgrounds (characterized by variance in background vegetation or sun exposure). The authors describe a possible evolutionary scenario in which an anole population first colonizes the coastal areas of each island after a dispersal event, and then rapidly expands into the interior montane areas of the island and adapts to new conditions there. Given the constant concern of climate change, repeated evolution in response to different climatic conditions may offer hope that anole populations can respond to rapid environmental change.

The most famous story of parallel evolution in anoles is the convergent evolution of ecomorphs across the islands of the Greater Antilles. This paper offers the tantalizing possibility of another type of convergent evolutionary pattern, this time within species but across habitat types. The smaller islands of the Lesser Antilles may be too constrained to allow for speciation driven by ecomorph specialization, but could still promote significant population divergence across habitats. More information on the adaptive differences between these xeric and montane populations, along with characterization of their genetic structure, could shed light on these possibilities. Based on these results in the Lesser Antillean populations, there is also the possibility that this type of xeric and montane divergence exists within species in the Greater Antilles, and fine-scale studies of population structure could reveal another level of convergent evolution in those species.

Thorpe, R. S., Barlow, A., Malhotra, A. and Surget-Groba, Y. (2015), Widespread parallel population adaptation to climate variation across a radiation: implications for adaptation to climate change. Molecular Ecology, 24: 1019–1030. doi: 10.1111/mec.13093