The Difficulty of Predicting Evolutionary Change in Response to Novel Ecological Interactions: A Field Experiment with Anolis Lizards.

AbstractDetermining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pressures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictability of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme-associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and habitat use, whereas genetic change was unpredictable and not measurably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information.

The Epigenetic Signature of Colonizing New Environments in Anolis Lizards.

Founder populations often show rapid divergence from source populations after colonizing new environments. Epigenetic modifications can mediate phenotypic responses to environmental change and may be an important mechanism promoting rapid differentiation in founder populations. Whereas many long-term studies have explored the extent to which divergence between source and founder populations is genetically heritable versus plastic, the role of epigenetic processes during colonization remains unclear. To investigate epigenetic modifications in founding populations, we experimentally colonized eight small Caribbean islands with brown anole lizards (Anolis sagrei) from a common source population. We then quantitatively measured genome-wide DNA methylation in liver tissue using reduced representation bisulfite sequencing of individuals transplanted onto islands with high- versus low-habitat quality. We found that lizard sex and habitat quality explained a significant proportion of epigenetic variation. Differentially methylated cytosines mapped to genes that encode proteins with functions likely to be relevant to habitat change (e.g., signal transduction, immune response, circadian rhythm). This study provides experimental evidence of a relationship between epigenetic responses and the earliest stages of colonization of novel environments in nature and suggests that habitat quality influences the nature of these epigenetic modifications.