Introgressive Hybridization and the Evolution of Lake-Adapted Catostomid Fishes.

Thomas E Dowling,David W Wagman,Douglas F Markle,Greg J Tranah,Evan W Carson,Bernard P May,Filippos A Aravanopoulos

doi:10.1371/journal.pone.0149884

Abstract

Hybridization has been identified as a significant factor in the evolution of plants as groups of interbreeding species retain their phenotypic integrity despite gene exchange among forms. Recent studies have identified similar interactions in animals; however, the role of hybridization in the evolution of animals has been contested. Here we examine patterns of gene flow among four species of catostomid fishes from the Klamath and Rogue rivers using molecular and morphological traits. Catostomus rimiculus from the Rogue and Klamath basins represent a monophyletic group for nuclear and morphological traits; however, the Klamath form shares mtDNA lineages with other Klamath Basin species (C. snyderi, Chasmistes brevirostris, Deltistes luxatus). Within other Klamath Basin taxa, D. luxatus was largely fixed for alternate nuclear alleles relative to C. rimiculus, while Ch. brevirostris and C. snyderi exhibited a mixture of these alleles. Deltistes luxatus was the only Klamath Basin species that exhibited consistent covariation of nuclear and mitochondrial traits and was the primary source of mismatched mtDNA in Ch. brevirostris and C. snyderi, suggesting asymmetrical introgression into the latter species. In Upper Klamath Lake, D. luxatus spawning was more likely to overlap spatially and temporally with C. snyderi and Ch. brevirostris than either of those two with each other. The latter two species could not be distinguished with any molecular markers but were morphologically diagnosable in Upper Klamath Lake, where they were largely spatially and temporally segregated during spawning. We examine parallel evolution and syngameon hypotheses and conclude that observed patterns are most easily explained by introgressive hybridization among Klamath Basin catostomids.

Highlights

While hybridization has generally been viewed as a force that erodes biodiversity, several authors [1,2,3,4] have hypothesized that effects of introgression are not always negative, and that introgressive hybridization can be a creative factor during the evolutionary process [5]
Within other Klamath Basin taxa, D. luxatus was largely fixed for alternate nuclear alleles relative to C. rimiculus, while Ch. brevirostris and C. snyderi exhibited a mixture of these alleles
The third lineage was composed of C. rimiculus (S2 Table) from the Rogue River (RIM1), all with ND4L haplotype “L.” The remaining haplotypes were almost exclusively found in C. rimiculus from the Klamath River and occupied an intermediate position in the consensus tree

Summary

Introduction

While hybridization has generally been viewed as a force that erodes biodiversity, several authors [1,2,3,4] have hypothesized that effects of introgression are not always negative, and that introgressive hybridization can be a creative factor during the evolutionary process [5] This perspective has been especially common in the botanical literature, and plant biologists have noted that there are groups of interbreeding species (termed syngameons) that maintain their ecological, morphological, genetic and evolutionary consistency in spite of extensive hybridization [5,6]. Traits under selection can persist in the face of strong gene flow [10], resulting in a mosaic of introgressed and locally adapted genetic variants within genomes of various species

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Conclusion