Abstract

Admixture in natural populations is a long‐standing management challenge, with population genomic approaches offering means for adjudication. We now more clearly understand the permeability of species boundaries and the potential of admixture for promoting adaptive evolution. These issues particularly resonate in western North America, where tectonism and aridity have fragmented and reshuffled rivers over millennia, in turn promoting reticulation among endemic fishes, a situation compounded by anthropogenic habitat modifications and non‐native introductions. The melding of historic and contemporary admixture has both confused and stymied management. We underscore this situation with a case study that quantifies basin‐wide admixture among a group of native and introduced fishes by employing double‐digest restriction site‐associated DNA (ddRAD) sequencing. Our approach: (a) quantifies the admixed history of 343 suckers (10 species of Catostomidae) across the Colorado River Basin; (b) gauges admixture within the context of phylogenetic distance and “ecological specialization”; and (c) extrapolates potential drivers of introgression across hybrid crosses that involve endemic as well as invasive species. Our study extends across an entire freshwater basin and expands previous studies more limited in scope both geographically and taxonomically. Our results detected admixture involving all 10 species, with habitat alterations not only accelerating the breakdown of reproductive isolation, but also promoting introgression. Hybridization occurred across the genus despite phylogenetic distance, whereas introgression was only detected within subgenera, implicating phylogenetic distance and/or ecological specialization as drivers of reproductive isolation. Understanding the extent of admixture and reproductive isolation across multiple species serves to disentangle their reticulate evolutionary histories and provides a broadscale perspective for basin‐wide conservation and management.

Highlights

  • Reticulated evolution is a product of several, often interacting phenomena, including horizontal gene transfer, polyploidization, and hybridization with introgression (Wendel & Doyle, 1998)

  • Due to minimal rates of introgression found in most locations and the rarity of hybrids with ancestry of more than two species across the basin, as well as in a focused population study in the upper reaches of the Upper Colorado River Basin (Mandeville et al, 2017), the capacity for White Sucker to serve as a “hybrid bridge” between native species is negligible, and the implication that multiple species will potentially collapse into a “mutt sucker” is improbable

  • While hybridization is increasingly recognized as a common evolutionary phenomenon among fishes, our case study of catostomid fishes from the Colorado River basin suggests introgression seemingly decreases with phylogenetic distance and may be driven by ecological specializations that separate subgenera

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Summary

Introduction

Reticulated evolution is a product of several, often interacting phenomena, including horizontal gene transfer, polyploidization, and hybridization with introgression (Wendel & Doyle, 1998). Hybridization, especially when coupled with introgression (i.e., the incorporation of alleles from one species into the gene pool of another), has long been thought to play a beneficial evolutionary role in both plants (Arnold, 1992) and animals (Dowling & Secor, 1997). It can promote evolution by (a) generating new genetic variation, (b) transferring adaptive traits, and (c) producing new lineages that exploit a novel niche within which neither parental taxa could succeed (Darras, Leniaud, & Aron, 2014; Edelman et al, 2019; Seehausen et al, 2014)

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