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bioRxiv · 10.1101/2024.01.29.577868

Complex Hybridization in a Clade of Polytypic Salamanders (Plethodontidae: Desmognathus) Uncovered by Estimating Higher-Level Phylogenetic Networks

Pyron, R. A.·O'Connell, K.·Myers, E.·Beamer, D.·Banos, H.
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Abstract

Hybridization between incipient lineages is a common feature of ecomorphological diversification. We examine these phenomena in the Pisgah clade of Desmognathus salamanders from the southern Appalachian Mountains of the eastern United States. The group contains four to seven species exhibiting two discrete phenotypes, aquatic "shovel-nosed" and semi-aquatic "black-bellied" forms. These ecomorphologies are ancient and have apparently been transmitted repeatedly between lineages through introgression. Geographically proximate populations of both phenotypes exhibit admixture, and at least two black-bellied lineages have been produced via reticulations between shovel-nosed parentals, suggesting complex transmission dynamics. However, computational constraints currently limit our ability to reconstruct network radiations from gene-tree data. Available methods are limited to level-1 networks wherein reticulations do not share edges, and higher-level networks may be non-identifiable in many cases. We present a heuristic approach to recover information from higher-level networks across a range of potentially identifiable empirical scenarios, supported by theory and simulation. When extrinsic information indicating the location and direction of hybridization events is available, our method can yield successful estimates of non-level-1 networks, or at least a reduced possible set thereof. Phylogenomic data strongly support a single backbone topology with up to five overlapping hybrid edges. These results suggest an unusual mechanism of ecomorphological hybrid speciation, wherein a binary threshold trait causes hybrids to shift between two microhabitat niches, promoting ecological divergence between sympatric hybrids and parentals. This contrasts with other well-known systems in which hybrids exhibit intermediate, novel, or transgressive phenotypes. Finally, the genetic basis of these phenotypes is unclear and further data are needed to clarify the evolutionary basis of morphological changes with ecological consequences.

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Pyron, R. A., O'Connell, K., Myers, E., Beamer, D., Banos, H.. 2024-01-30. Complex Hybridization in a Clade of Polytypic Salamanders (Plethodontidae: Desmognathus) Uncovered by Estimating Higher-Level Phylogenetic Networks. https://doi.org/10.1101/2024.01.29.577868

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