Gene flow in phylogenomics: Sequence capture resolves species limits and biogeography of Afromontane forest endemic frogs from the Cameroon Highlands

Dolinay, Matej; Nečas, Tadeáš; Zimkus, Breda M.; Schmitz, Andreas; Fokam, Eric B.; Lemmon, Emily Moriarty; Lemmon, Alan R.; Gvoždík, Václav

doi:10.1016/j.ympev.2021.107258

Cited by 12 publications

(14 citation statements)

References 127 publications

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“…Essentially, our results and those of recent authors such as Chan et al (2022) and Dolinay et al (2021) reveal the need for an analytical and computational framework that can simultaneously estimate complex phylogenetic networks and delimit candidate species with gene flow. Few if any such methods exist, especially in a computationally tractable form for a dataset of this size, containing hybridizations across multiple distant phylogenetic scales.…”

Section: Discussionsupporting

confidence: 69%

“…While admixture between genealogically distinct parental populations does not appear to significantly confound delimitation of candidate species in our analyses, it does seem to exert a strong influence on phylogenetic topologies (Degnan, 2018). An extension of the artifacts first reported by Chan et al (2020, 2022) and demonstrated by Dolinay et al (2021) suggests that hybrid individuals will form ladder‐like grades of intermediate topological position between “pure” parental populations in rough proportion to their degree of ancestry from each parent. This effect is corroborated strongly in our analyses, where the topological imbalance of candidate species is significantly related to their degree of admixture.…”

Section: Discussionmentioning

confidence: 62%

“…Crucially, a series of recent empirical studies have highlighted a potentially artifactual process by which species delimitation methods that do not account for gene flow may erroneously inflate estimates by identifying hybrid populations as distinct taxa (Chan et al, 2017(Chan et al, , 2020(Chan et al, , 2022Dolinay et al, 2021). Admixed populations resulting from spatiotemporally proximate hybridization events may consequently produce individuals with similar allele frequencies, distinct from either parental population, that are therefore grouped by clustering and phylogenetic analyses.…”

Section: Discussionmentioning

confidence: 99%

“…Recent authors (Chan et al, 2022; Dolinay et al, 2021) have provided verbal models and preliminary empirical evidence for an intuitive process: the presence of hybrid individuals in a phylogenetic analysis of phylogeographic datasets seems to create artifactual topologies. Specifically, hybrids between two parental populations seem to form ladder‐like grades between them in proportion to their individual ancestry from each.…”

Section: Methodsmentioning

confidence: 99%

“…Third, how does the existence of recent admixture events between mito‐nuclear candidate species influence topological reconstructions? The impact of heavily admixed genomes on the terminal placement of individuals and their effect on the resolution of species‐level clades is now known to be significant in many cases (Chan et al, 2022; Dolinay et al, 2021). Given the prevalence of hybrid individuals in our sampled populations of Desmognathus , we hypothesize that at least some of the phylogenetic structure detected in mito‐nuclear candidate species by previous analyses may have been influenced by gene trees from these admixed terminal specimens, resulting in artifactual “clades” interpreted as meaningful units.…”

Section: Introductionmentioning

confidence: 99%

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Candidate‐species delimitation in Desmognathus salamanders reveals gene flow across lineage boundaries, confounding phylogenetic estimation and clarifying hybrid zones

Pyron

O’Connell

Lemmon

et al. 2022

Ecology and Evolution

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Dusky Salamanders (genus Desmognathus) currently comprise only 22 described, extant species. However, recent mitochondrial and nuclear estimates indicate the presence of up to 49 candidate species based on ecogeographic sampling. Previous studies also suggest a complex history of hybridization between these lineages. Studies in other groups suggest that disregarding admixture may affect both phylogenetic inference and clustering‐based species delimitation. With a dataset comprising 233 Anchored Hybrid Enrichment (AHE) loci sequenced for 896 Desmognathus specimens from all 49 candidate species, we test three hypotheses regarding (i) species‐level diversity, (ii) hybridization and admixture, and (iii) misleading phylogenetic inference. Using phylogenetic and population‐clustering analyses considering gene flow, we find support for at least 47 candidate species in the phylogenomic dataset, some of which are newly characterized here while others represent combinations of previously named lineages that are collapsed in the current dataset. Within these, we observe significant phylogeographic structure, with up to 64 total geographic genetic lineages, many of which hybridize either narrowly at contact zones or extensively across ecological gradients. We find strong support for both recent admixture between terminal lineages and ancient hybridization across internal branches. This signal appears to distort concatenated phylogenetic inference, wherein more heavily admixed terminal specimens occupy apparently artifactual early‐diverging topological positions, occasionally to the extent of forming false clades of intermediate hybrids. Additional geographic and genetic sampling and more robust computational approaches will be needed to clarify taxonomy, and to reconstruct a network topology to display evolutionary relationships in a manner that is consistent with their complex history of reticulation.

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Section: Discussionsupporting

confidence: 69%