Phylogenomic Signatures of Ancient Introgression in a Rogue Lineage of Darters (Teleostei: Percidae)

Abstract

Evolutionary history is typically portrayed as a branching phylogenetic tree, yet not all evolution proceeds in a purely bifurcating manner. Introgressive hybridization is one process that results in reticulate evolution. Most known examples of genome-wide introgression occur among closely related species with relatively recent common ancestry; however, we present evidence for ancient hybridization and genome-wide introgression between major stem lineages of darters, a species-rich clade of North American freshwater fishes. Previous attempts to resolve the relationships of darters have been confounded by the uncertain phylogenetic resolution of the lineage Allohistium. In this study, we investigate the phylogenomics of darters, specifically the relationships of Allohistium, through analyses of approximately 30,000 RADseq loci sampled from 112 species. Our phylogenetic inferences are based on traditional approaches in combination with strategies that accommodate reticulate evolution. These analyses result in a novel phylogenetic hypothesis for darters that includes ancient introgression between Allohistium and other two major darter lineages, minimally occurring 20 million years ago. Darters offer a compelling case for the necessity of incorporating phylogenetic networks in reconstructing the evolutionary history of diversification in species-rich lineages. We anticipate that the growing wealth of genomic data for clades of non-model organisms will reveal more examples of ancient hybridization, eventually requiring a re-evaluation of how evolutionary history is visualized and utilized in macroevolutonary investigations.

Rapture‐ready darters: Choice of reference genome and genotyping method (whole‐genome or sequence capture) influence population genomic inference in Etheostoma

“…Most previous phylogenetic work in darters has focused on Sanger sequencing of a small number of mitochondrial and nuclear genes (Near et al., 2011), while conservation genetics, landscape genetics and molecular ecology studies have mainly used microsatellite markers developed for single species but with some applicability across the clade (Gabel et al., 2008; Hudman et al., 2008; Khudamrongsawat et al., 2007; Saarinen & Austin, 2010; Switzer et al., 2008; Tonnis, 2006). Recent work has begun to incorporate HTS methods, employing single‐digest RADseq (MacGuigan & Near, 2019; Moran et al., 2018, 2020) and double‐digest RADseq (ddRAD, George, 2018; Moran et al., 2017) to investigate phylogeny, phylogeography and reproductive barriers among species. While ddRAD and RADseq represent a huge leap forward in terms of the amount of data generated, these methods often increase the number of loci genotyped at the expense of missing data and low coverage (MacGuigan & Near, 2019).…”

“…Recent work has begun to incorporate HTS methods, employing single‐digest RADseq (MacGuigan & Near, 2019; Moran et al., 2018, 2020) and double‐digest RADseq (ddRAD, George, 2018; Moran et al., 2017) to investigate phylogeny, phylogeography and reproductive barriers among species. While ddRAD and RADseq represent a huge leap forward in terms of the amount of data generated, these methods often increase the number of loci genotyped at the expense of missing data and low coverage (MacGuigan & Near, 2019). As such, there is currently no published method for reproducibly generating data for a single consistent set of loci distributed across the genome for darters.…”

Rapture-ready darters: choice of reference genome and genotyping method (whole-genome or sequence capture) influence population genomic inference inEtheostoma

“…Most previous phylogenetic work in darters has focused on Sanger sequencing of a small number of mitochondrial and nuclear genes (Near et al 2011), while conservation genetics, landscape genetics, and molecular ecology studies have mainly used microsatellite markers developed for single species but with some applicability across the clade (Tonnis 2006, Khudamrongsawat et al 2007, Switzer et al 2008, Gabel et al 2008, Hudman et al 2008, Saarinen and Austin 2010. Recent work has begun to incorporate HTS methods, employing single-digest RADseq , MacGuigan et al 2019, Moran et al 2020 and double-digest RADseq (ddRAD, Moran et al 2017, George 2018 to investigate phylogeny, phylogeography, and reproductive barriers among species. While ddRAD and RADseq represent a huge leap forward in terms of the amount of data generated, these methods often increase the number of loci genotyped at the expense of missing data and low coverage (MacGuigan et al 2019).…”

“…Recent work has begun to incorporate HTS methods, employing single-digest RADseq , MacGuigan et al 2019, Moran et al 2020 and double-digest RADseq (ddRAD, Moran et al 2017, George 2018 to investigate phylogeny, phylogeography, and reproductive barriers among species. While ddRAD and RADseq represent a huge leap forward in terms of the amount of data generated, these methods often increase the number of loci genotyped at the expense of missing data and low coverage (MacGuigan et al 2019). As such, there is currently no published method for reproducibly generating data for a single consistent set of loci distributed across the genome for darters.…”

Reinforcement in the banded darter Etheostoma zonale: The effect of sex and sympatry on preferences

“…Premating barriers are found to evolve more rapidly than other barriers in darters (Martin & Mendelson, 2016;Mendelson, 2003;Mendelson, Imhoff, & Venditti, 2007;Williams & Mendelson, 2014), and diversification in darters is thought to occur primarily in allopatry, with sister species pairs all having allopatric ranges (Near et al, 2011). However, natural hybrids have been reported involving over 25% of darter species (Keck & Near, 2009), and recent phylogenetic analyses find evidence of ancient hybridization and genome-wide introgression between major darter lineages (MacGuigan & Near, 2018). These data suggest that hybridization between darters, both current and historically, is common enough to support a potential role for reinforcement in this system.…”