Developmental environment contributes to rapid trait shifts among newly colonized subterranean habitats

Abstract

Recent colonization events to extreme environments provide unique opportunities to study the early steps of adaptation and the potential for rapid convergent evolution. However, phenotypic shifts in recent colonization may also be due to plasticity in response to changes in the rearing environment. Here we analyzed a suite of morphological and behavioral traits of paired surface, subterranean, and facultatively subterranean Mexican Tetra, Astyanax mexicanus from recent introductions in two separate watersheds outside of their native range. We find a variety of phenotypic and behavioral shifts between subterranean and surface populations that mimic more established subterranean populations in Mexico. Despite this rapid morphological divergence, we find that most of these traits are due to plasticity in response to rearing environments, as common-garden, lab-raised fish do not maintain the phenotypes from the parental populations, and lab-born fish resemble each other for most traits more than any wild population. Interestingly and similar to wild-caught fish, subterranean-derived, lab-born subterranean fish exhibit more wall-following behavior than their lab-born surface counterparts, suggesting that this trait is genetically determined and rapidly diverging between subterranean and surface populations. Thus, our study sheds light on the early steps to subterranean evolution, is indicative of potential rapid behavioral evolution of navigational tactics and suggests that plasticity in traits involving exploratory behavior may facilitate or be in response to subterranean invasions.