The Limits of the Metapopulation: Lineage Fragmentation in a Widespread Terrestrial Salamander (Plethodon cinereus)

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In vicariant species formation, divergence results primarily from periods of allopatry and restricted gene flow. Widespread species harboring differentiated, geographically distinct sublineages offer a window into what may be a common mode of species formation, whereby a species originates, spreads across the landscape, then fragments into multiple units. However, incipient lineages usually lack reproductive barriers that prevent their fusion upon secondary contact, blurring the boundaries between a single, large metapopulation-level lineage and multiple independent species. Here, we explore this model of species formation in the Eastern Red-backed Salamander (Plethodon cinereus), a widespread terrestrial vertebrate with at least 6 divergent mitochondrial clades throughout its range. Using anchored hybrid enrichment data, we applied phylogenomic and population genomic approaches to investigate patterns of divergence, gene flow, and secondary contact. Genomic data broadly match most mitochondrial groups but reveal mitochondrial introgression and extensive admixture at several contact zones. While species delimitation analyses in Bayesian Phylogenetics and Phylogeography supported 5 lineages of P. cinereus, genealogical divergence indices (gdi) were highly sensitive to the inclusion of admixed samples and the geographic representation of candidate species, with increasing support for multiple species when removing admixed samples or limiting sampling to a single locality per group. An analysis of morphometric data revealed differences in body size and limb proportions among groups, with a reduction of forelimb length among warmer and drier localities consistent with increased fossoriality. We conclude that P. cinereus is a single species, but one with highly structured component lineages of various degrees of independence.

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