Figure 1. Some examples of “typical” species found in seasonal and aseasonal environments in Mexico. Please forgive the terrible lighting of the Seasonal photos.
Reprinted from the pages of BioMH: Biology of Mexican Herps:
In 1984, Henry Fitch and David Hillis published a paper on mainland anoles that grabbed my attention decades later as I began my graduate research. In that paper, they described a number of dewlap traits and found that many dewlap scale traits were useful for species identification. They also found an interesting correlation between male dewlap size and habitat type. Species with large male dewlaps were associated with habitats in highly seasonal environments such as deserts and thorn-scrub, while those with small male dewlaps inhabited cloud forests and tropical rainforests (Fig. 1). Why might such an association exist?
Fitch and Hillis proposed a sexual selection hypothesis to explain the pattern. After all, Fitch had previously found decreased sexual size dimorphism (SVL) in anole species associated with stable environments such as cloud forests and rainforests (1976). One interpretation of this pattern is that the intensity of sexual selection is reduced in species that can breed throughout the year, decreasing body size dimorphism between the sexes. Fitch and Hillis also found increased body size dimorphism in species that had large dewlaps and lived in seasonal environments (1984). Since anoles living in highly seasonal environments can have shortened breeding seasons linked to precipitation (Fleming & Hooker 1973), the Fitch-Hillis Hypothesis posits that constraints in length of the breeding season increases male dewlap size due to strengthened sexual selection (1984).
Using new datasets for Mexican anoles, we re-investigated support for the Fitch-Hillis Hypothesis at two scales. We performed “macro” analyses across over 40 Mexican anole species and also looked at the Anolis sericeus group, the only group that occurs broadly throughout seasonal and aseasonal habitat types. In our study, we were able to do two important things differently than the original study. The first is that we were able to treat seasonality as a continuous variable thanks to modern GIS tools and environmental data (Hijmans et al. 2005), enabling a finer-scale look at the link between male dewlap size and seasonality. The original study treated seasonality as a categorical variable (“seasonal” vs “aseasonal”). The second difference is that we were able to correct for phylogenetic non-independence of species. To put it simply, species may be similar in dewlap size due to relatedness to other species (evolutionary history) rather than to the seasonality environment they inhabit. To do this, we used a recently-published phylogeny (Poe et al. 2017) and phylogenetic regression (PGLS) to verify the results of the previous study.
Interestingly enough, our standard ordinary least squares (OLS) regression analyses duplicated results from the original study; without accounting for evolutionary history, there is indeed a strong correlation between male dewlap size and seasonality in Mexican anoles (Fig. 2A, black line). Being able to replicate results using different datasets and approaches is very important and not as common as many of us scientists would like. However, as reflected in the more flattened red dotted line in the figure below, the correlation is weakened substantially after accounting for phylogeny. We therefore cannot say with confidence that seasonality affects male dewlap size in Mexican anoles.
Figure 2. Regression results from Gray et al. (2020). (A) Results from our “macro” analyses, with black line representing standard OLS regression results and red dotted line representing the PGLS results. (B) Results for the Anolis sericeus complex, with black line representing results for all three major lineages and red dotted line representing results of the Pacific and Caribbean lineages. See paper for further details or please ask questions in the comment section below!
We were not able to perform phylogenetic regressions on the Anolis sericeus complex, unfortunately. Though several of us published a phylogeographic study on the silky anoles, many populations represented in the dewlap dataset were not included in that work (Gray et al. 2019). Therefore we had to come up with another way to investigate a correlation in silky anoles. Our phylogeographic work discovered three clades which we assigned Pacific, Caribbean, and Yucatan. Incidentally, the Yucatan lineage is diagnosed in part by small male dewlap size (Lara-Tufiño et al. 2016). The Yucatan lineage also occurs in relatively aseasonal environments that fall within the conditions inhabited by the Caribbean lineage (Gray et al. 2020). So after running regressions on all populations (Fig. 2B, black line), we also ran regressions on only the Pacific and Caribbean lineages, which collectively experience the broadest range of seasonality environments (Gray et al. 2020). As you can see in the figure above, removing the Yucatan lineage flattens the regression line and makes it clear the correlation between male dewlap size and seasonality in silky anoles is influenced by phylogenetic history (Fig. 2B, red dotted line).
Does this mean seasonality is not a driver of male dewlap size? Not necessarily. We discuss other possibilities in the paper, including that anole lineages in Mexico may not have “switched” environments enough for us to be able to detect an effect. We found strong phylogenetic signal for seasonality in Mexican anoles, suggesting species from lineages preferring seasonal environments do not often switch to aseasonal environments and vice versa. As an example, one lineage of 14 west Mexican anoles consists of species that tend to have large dewlaps and live in seasonal environments. In that clade, having a large dewlap might be traceable to one evolutionary event when the most recent common ancestor of the clade evolved a large dewlap. Sexual selection and a truncated breeding season might have had something to do with that event…or the ancestor may have evolved a large dewlap for other reasons and extant species maintained the trait.
While the final result may not be super exciting, I enjoyed working on this project. Collectively, I spent about one year in Mexico catching lizards during grad school and our sample size for some species still left a lot to be desired. Datasets like this take a lot of time and effort to generate! A lot of friends and collaborators helped find and photograph animals through the years. I want to thank Adam Clause, Luke Mahler, Eric Schaad, and Britt White for taking some of the best dewlap photos in our collection.
If anyone wants to play around with the data, they are available at Dryad. And the paper is open access and short, so check it out!
References
Fitch HS (1976) Sexual differences in the mainland anoles. Occasional papers of the Museum of Natural History, the University of Kansas, 50:1-21.
Fitch HS, DM Hillis (1984) The Anolis dewlap: Interspecific variability and morphological associations with habitat. Copeia, 1984:315-323.
Fleming TH, RS Hooker (1973) Anolis cupreus: the response of a lizard to tropical seasonality. Ecology, 56:1243-1261.
Gray LN, AJ Barley, S Poe, RC Thomson, A Nieto-Montes de Oca, IJ Wang (2019) Phylogeography of a widespread lizard complex reflects patterns of both geographic and ecological isolation. Molecular Ecology, 28:644-657.
Gray LN, AJ Barley, DM Hillis, CJ Pavón-Vázquez, S Poe, BA White (2020) Does breeding season variation affect evolution of a sexual signaling trait in a tropical lizard clade? Ecology and Evolution, 10:3738-3746.
Hijmans RJ, SE Cameron, JL Parra, PG Jones, A Jarvis (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25:1965-1978.
Lara-Tufiño JD, A Nieto-Montes de Oca, A Ramírez-Bautista, LN Gray (2016) Resurrection of Anolis ustus Hallowell, 1856 (Squamata, Dactyloidae). Zookeys, 2016:147-162.
Poe S, A Nieto-Montes de Oca, O Torres-Carvajal, K de Queiroz, JA Velasco, B Truett, LN Gray, MJ Ryan, G Kohler, F Ayala-Varela, I Latella (2017) A phylogenetic, biogeographic, and taxonomic study of all extant species of Anolis (Squamata: Iguanidae). Systematic Biology, 66:663-697.
