Speciation Hypotheses from Phylogeographic Delimitation Yield an Integrative Taxonomy for Seal Salamanders (Desmognathus monticola)

• Published in: Systematic biology 2023-05, Vol.72 (1), p.179-197
• Main Authors: Pyron, R Alexander, O’Connell, Kyle A, Duncan, Sophie C, Burbrink, Frank T, Beamer, David A
• Format: Article
• Language: English
• Subjects: Animals; Biological Evolution; Genetic Speciation; Phylogeny; Phylogeography; Urodela - genetics
• ISSN: 1063-5157; 1076-836X
• DOI: 10.1093/sysbio/syac065

Abstract Significant advances have been made in species delimitation and numerous methods can test precisely defined models of speciation, though the synthesis of phylogeography and taxonomy is still sometimes incomplete. Emerging consensus treats distinct genealogical clusters in genome-scale data as strong initial evidence of speciation in most cases, a hypothesis that must therefore be falsified under an explicit evolutionary model. We can now test speciation hypotheses linking trait differentiation to specific mechanisms of divergence with increasingly large data sets. Integrative taxonomy can, therefore, reflect an understanding of how each axis of variation relates to underlying speciation processes, with nomenclature for distinct evolutionary lineages. We illustrate this approach here with Seal Salamanders (Desmognathus monticola) and introduce a new unsupervised machine-learning approach for species delimitation. Plethodontid salamanders are renowned for their morphological conservatism despite extensive phylogeographic divergence. We discover 2 geographic genetic clusters, for which demographic and spatial models of ecology and gene flow provide robust support for ecogeographic speciation despite limited phenotypic divergence. These data are integrated under evolutionary mechanisms (e.g., spatially localized gene flow with reduced migration) and reflected in emergent properties expected under models of reinforcement (e.g., ethological isolation and selection against hybrids). Their genetic divergence is prima facie evidence for species-level distinctiveness, supported by speciation models and divergence along axes such as behavior, geography, and climate that suggest an ecological basis with subsequent reinforcement through prezygotic isolation. As data sets grow more comprehensive, species-delimitation models can be tested, rejected, or corroborated as explicit speciation hypotheses, providing for reciprocal illumination of evolutionary processes and integrative taxonomies. [Desmognathus; integrative taxonomy; machine learning; species delimitation.]