"Promotion and constraint of adaptive evolution in cave-dwelling lineages"

Dissertation Abstract
Experiencing a novel environment is a common driver of evolutionary change. This change can be promoted by a variety of mechanisms and outcomes, such as novel selection, decreases in genetic variation due to founder effects, drift effects, and genetic admixture. Equally important are forces that impede or prevent change, including lack of suitable mutations, genetic correlations, developmental constraints, or antagonistic selection. A valuable system for studying questions related to evolutionary change following colonization of a novel habitat is the cave habitat, which has induced dramatic adaptive changes in many species that inhabit caves as a result of both adaptive and neutral forces. I studied the evolution of cave-dwelling salamanders, and in particular in the cave salamander, Eurycea lucifuga. Eurycea lucifuga is an evolutionary puzzle, inhabiting caves while having maintained brilliant coloration more typical of ancestral, surface dwelling ancestors.
I first compared body shape among salamanders within Eurycea to examine the prediction from many previous studies that cave-dwellers are elongated relative to non-cave-dwellers. I found that terrestrial species were larger than aquatic species, and also that cave species had shorter tails relative to their body size than non-cave species. These results contrast with trends generally discussed in the cave literature, and reflect a need for explicit testing of how habitat impacts morphology in salamanders. I next investigated the phylogeographic history of Eurycea lucifuga and found that divergence among major lineages happened millions of years ago, with more recent expansion within each clade. This is similar to other cave-dwellers that show extreme morphological specialization to the subterranean climate. Our results do not support the idea that a lack of time underground acts as a constraint on adaptive evolution in this species. Lastly, I compared phenotypic differentiation in color traits with neutral genetic differentiation. The findings indicated that at small scales there is evidence of local differentiation in color relative to the neutral expectation. However, the spatial structuring of differentiation differs between the color phenotype and genotype. Population genetic analyses within a cave system indicated that migration likely occurs by surface corridors, suggesting that coloration may be maintained by a more substantial reliance on non-cave habitats than has been documented for this species.
I concluded from these results that the phenotype of the cave salamander, Eurycea lucifuga, is greatly impacted by a relatively minor aspect of its ecology, and hypothesize that its non-cave morphology is selectively maintained by use of surface habitats. In general, this work emphasizes the need to examine trait change in a broad context, considering phylogenetics, ecology, and neutral processes.