Evolution and sensory ecology of nonvisual sensory modalities in subterranean organisms

Caves and other subterranean habitats represent one of the most challenging environments on the planet. Considerable research has focused on the evolution of traits that are lost or degenerate, such as eyes and pigment, in subterranean organisms. Several constructive adaptations, particularly those involving nonvisual sensory modalities, are associated with cave colonization and inhabitation, but these changes have received much less attention. Both abiotic and biotic conditions influence the evolution of sensory modalities, with perpetual darkness and generally limited food resources being the major factors in subterranean ecosystems. These extreme conditions offer a unique opportunity to examine the evolution of nonvisual sensory modalities. However, very little is known about how such environmental constraints influence the sensory ecology of most cave organisms.

In collaboration with Daphne Soares (University of Maryland) and Dennis Higgs (University of Windsor), we have been conducting behavioral, morphological and physiological studies in a comparative framework to understand the potential tradeoffs in sensory modalities and adaptations to subterranean environments in subterranean fauna, particularly salamanders and cavefishes. Recently, we examined hearing in a family of cavefishes. Although they are amongst the most well-known cave organisms, few comparative studies have investigated cavefish ecology and sensory biology (Soares & Niemiller 2013). Enhancement of hearing abilities may be adaptive in caves to detect faint sounds produced by prey, conspecifics, and predators, or to detect sounds of flowing water associated with dramatic changes in water levels and velocity during flood events. However, to what degree hearing is enhanced in cavefishes is largely unknown. We compared the auditory brain stem response (ABR) of three species of amblyopsid cavefishes, as well as their environmental acoustic profiles (Niemiller et al. 2013). Opposite of our predictions, cave species not only have lost their eyes but also a significant portion of their auditory range compared to their surface relatives, as they are unable to hear frequencies >800 Hz. In addition, cave species have lower hair cell counts in the sensory epithelium of the inner ear compared to surface species. Congruent audio recordings of their cave habitats show that streams and water droplets from the ceiling create loud high frequency background noise, making their hearing profiles well nested in the acoustic environment. To our knowledge, our study represents the first to report auditory regression in a subterranean organism.

We are investigating other vertebrate cave species (cavefishes and salamanders) and nonvisual sensory modalities to determine whether disparate groups of subterranean organisms have evolved the same adaptive strategies to sensory specialization or if specialization is predominantly governed by subtle differences in subterranean habitats or the sensory modalities employed by surface ancestral species.

Primary Collaborators: Daphne Soares (University of Maryland), Dennis Higgs (University of Windsor)


Matthew L. Niemiller, Ph.D. (e-mail: cavemander17@gmail.com) ©2014-2015