Abstract

BackgroundIntrogressive hybridization is an important evolutionary process that can lead to the creation of novel genome structures and thus potentially new genetic variation for selection to act upon. On the other hand, hybridization with introduced species can threaten native species, such as cutthroat trout (Oncorhynchus clarkii) following the introduction of rainbow trout (O. mykiss). Neither the evolutionary consequences nor conservation implications of rainbow trout introgression in cutthroat trout is well understood. Therefore, we generated a genetic linkage map for rainbow-Yellowstone cutthroat trout (O. clarkii bouvieri) hybrids to evaluate genome processes that may help explain how introgression affects hybrid genome evolution.ResultsThe hybrid map closely aligned with the rainbow trout map (a cutthroat trout map does not exist), sharing all but one linkage group. This linkage group (RYHyb20) represented a fusion between an acrocentric (Omy28) and a metacentric chromosome (Omy20) in rainbow trout. Additional mapping in Yellowstone cutthroat trout indicated the two rainbow trout homologues were fused in the Yellowstone genome. Variation in the number of hybrid linkage groups (28 or 29) likely depended on a Robertsonian rearrangement polymorphism within the rainbow trout stock. Comparison between the female-merged F1 map and a female consensus rainbow trout map revealed that introgression suppressed recombination across large genomic regions in 5 hybrid linkage groups. Two of these linkage groups (RYHyb20 and RYHyb25_29) contained confirmed chromosome rearrangements between rainbow and Yellowstone cutthroat trout indicating that rearrangements may suppress recombination. The frequency of allelic and genotypic segregation distortion varied among parents and families, suggesting few incompatibilities exist between rainbow and Yellowstone cutthroat trout genomes.ConclusionsChromosome rearrangements suppressed recombination in the hybrids. This result supports several previous findings demonstrating that recombination suppression restricts gene flow between chromosomes that differ by arrangement. Conservation of synteny and map order between the hybrid and rainbow trout maps and minimal segregation distortion in the hybrids suggest rainbow and Yellowstone cutthroat trout genomes freely introgress across chromosomes with similar arrangement. Taken together, these results suggest that rearrangements impede introgression. Recombination suppression across rearrangements could enable large portions of non-recombined chromosomes to persist within admixed populations.

Highlights

  • Introgressive hybridization is an important evolutionary process that can lead to the creation of novel genome structures and potentially new genetic variation for selection to act upon

  • Hybrid linkage map After removing markers that were heterozygous for the same alleles in both parents, 310 microsatellite loci, 72 single nucleotide polymorphisms (SNPs), and one species-specific insertion/deletion were mapped in Yellowstone cutthroat trout (YCT)-RBT F1 hybrids using two families (Family, 54 progeny; Family 2, 53 progeny) (Additional file 1, Worksheets 2 – 8; Additional files 2 and 3)

  • We identified a total of 28–29 linkage groups in the sex-merged map for the hybrids (Table 1) and have designated hybrid linkage groups as RYHyb

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Summary

Introduction

Introgressive hybridization is an important evolutionary process that can lead to the creation of novel genome structures and potentially new genetic variation for selection to act upon. Neither the evolutionary consequences nor conservation implications of rainbow trout introgression in cutthroat trout is well understood. We generated a genetic linkage map for rainbow-Yellowstone cutthroat trout (O. clarkii bouvieri) hybrids to evaluate genome processes that may help explain how introgression affects hybrid genome evolution. Introgression breaks down linkage associations and generates novel gene combinations which may have fitness consequences [2]. Hybridization can have significant conservation implications, leading to the formation of hybrid swarms and extinction [6,7]. In these cases, introgression may interfere with epistatic interactions by disrupting local adaptations and breaking down co-adapted gene complexes. Regardless of the consequences, understanding the genome processes that affect introgression is fundamental to understanding hybrid genome evolution

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