Speciation with gene flow in a narrow endemic West Virginia cave salamander (Gyrinophilus subterraneus)

Authors

Evan H. Campbell Grant, U.S. Geological Survey
Kevin P. Mulder, Smithsonian Institution, Universidade Do Porto, National Zoological Park
Adrianne B. Brand, U.S. Geological Survey
Douglas B. Chambers, U.S. Geological Survey
Addison H. Wynn, Smithsonian Institution
Grace Capshaw, Smithsonian Institution, University of Maryland
Matthew L. Niemiller, The University of Alabama in Huntsville
John G. Phillips, University of Idaho
Jeremy F. Jacobs, Smithsonian Institution
Shawn R. Kuchta, Ohio University
Rayna C. Bell, Smithsonian Institution, California Academy of Sciences

Date of this Version

6-1-2022

Citation

Conservation Genetics (2022) 23:727–744. https://doi.org/10.1007/s10592-022-01445-7

Comments

U.S. government work and not under copyright protection in the U.S.

Abstract

Due to their limited geographic distributions and specialized ecologies, cave species are often highly endemic and can be especially vulnerable to habitat degradation within and surrounding the cave systems they inhabit. We investigated the evolutionary history of the West Virginia Spring Salamander (Gyrinophilus subterraneus), estimated the population trend from historic and current survey data, and assessed the current potential for water quality threats to the cave habitat. Our genomic data (mtDNA sequence and ddRADseq-derived SNPs) reveal two, distinct evolutionary lineages within General Davis Cave corresponding to G. subterraneus and its widely distributed sister species, Gyrinophilus porphyriticus, that are also differentiable based on morphological traits. Genomic models of evolutionary history strongly support asymmetric and continuous gene flow between the two lineages, and hybrid classification analyses identify only parental and first generation cross (F1) progeny. Collectively, these results point to a rare case of sympatric speciation occurring within the cave, leading to strong support for continuing to recognize G. subterraneus as a distinct and unique species. Due to its specialized habitat requirements, the complete distribution of G. subterraneus is unresolved, but using survey data in its type locality (and currently the only known occupied site), we find that the population within General Davis Cave has possibly declined over the last 45 years. Finally, our measures of cave and surface stream water quality did not reveal evidence of water quality impairment and provide important baselines for future monitoring. In addition, our unexpected finding of a hybrid zone and partial reproductive isolation between G. subterraneus and G. porphyriticus warrants further attention to better understand the evolutionary and conservation implications of occasional hybridization between the species.