Parallel Sensory Compensation following Independent Subterranean Colonization by Groundwater Salamanders ( Eurycea )

Lineages that have invaded subterranean environments have repeatedly evolved remarkable adaptations to life in darkness. However, observational and experimental studies in additional natural systems are needed to further our understanding of repeated evolution and convergence. In Texas, a radiation of groundwater salamanders (genus Eurycea ), with independent invasions of subterranean karstic environments, offers an opportunity to investigate phenotypic convergence, parallel evolution, and the enhancement and regression of sensory systems. Adaptations to a troglobitic life in this clade includes morphological, behavioral, and physiological changes within and among species.

Intraspecific and interspecific variation in morphology to the selective pressures of life underground allows for detailed examination of physical, behavioral, and physiological changes associated with subterranean adaptation within a comparative phylogenetic framework.

We find a tradeoff between two sensory systems repeated across multiple subterranean Eurycea lineages: the degeneration of the eye and the expansion of the mechanosensory lateral line. The increase in anterior neuromast organs in subterranean lineages was positively correlated with the expression of paired box protein Pax-6, a conserved transcription factor important for vertebrate neurogenesis. Our results show a decreasing trend of PAX-6 labeling in the neuromasts of adult surface salamanders ( E. nana ) relative to the maintained labeling in subterranean species ( E. rathbuni ).

Our results suggest a tradeoff in resource allocation between the development of optic and anterior lateral line sensory systems in surface and subterranean salamander lineages and provide a starting point for future evolutionary developmental investigations examining the genetic underpinnings of adaptive, repeated evolution in a novel system.

Significance Statement

Under-explored subterranean environments in Central Texas harbor a phenotypically and taxonomically diverse radiation of groundwater salamanders, which we used to test the molecular and developmental bases for adaptive evolution in extreme environments. Using an integrative approach, we quantify the divergence and convergence of two sensory modalities: vision loss and mechanoreception. The divergent developmental and phenotypic tradeoffs have evolved several times in parallel among populations and species in this group. Understanding the evolutionary developmental processes responsible for these changes will further our understanding of adaptive, repeated evolution in a natural system.