Heterogeneous genetic basis of age at maturity in salmonid fishes

Abstract

Understanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications in conservation and management. However, the extent to which interspecific life‐history trait polymorphisms share evolutionary pathways remains underexplored. Here, we address this gap by studying the genetic basis of a key life‐history trait, age at maturity, in four species of Pacific salmonids (genus Oncorhynchus) that exhibit intra‐ and interspecific variation in this trait—Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome‐wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46 × 10−9 after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life‐history trait, as well as the implications of our findings for conservation and management.

Long distance migration is a major factor driving local adaptation at continental scale in Coho Salmon

“…Rock1 and Greb1L associated with return timing, and Vgll3 and six6, associated with age at maturity). This is similar to recent findings by (Waters et al, 2021), who did not identify any significant associations between the latter two genes and age at maturity in Coho salmon. Moreover, our study did not focus on variation in life history and phenotypic traits among populations, and therefore we did not investigate similar molecular targets of selection.…”

A potential role for restricted intertactical heritability in preventing intralocus conflict

“…The vgll3 gene associated with age at maturity for Atlantic salmon does not appear to influence age at maturity in Chinook, Coho, Sockeye, or Steelhead (Waters et al, 2021 ). The same study showed that the six6 gene is associated with age at maturity in Sockeye and Steelhead, although the effect of the six6 genotype did not differ between sexes in either species (Waters et al, 2021 ). There was no association between the six6 gene and age at maturity in Chinook or Coho.…”

“…In species that are threatened or endangered, such as Coho salmon, reduced population growth rates would be detrimental to conservation efforts. While recent work has begun to address sexual conflict in salmonids by uncovering the genetic architecture of age and length at maturity and ARTs in salmonids (Ayllon et al, 2015 ; Barson et al, 2015 ; Pearse et al, 2019 ; Sinclair‐Waters et al, 2020 ), it is clear that species and populations vary in both genetic architecture for these traits and the degree to which that genetic architecture is sex‐specific (Kusche et al, 2017 ; Waters et al, 2021 ).…”

Genome‐wide analysis reveals demographic and life‐history patterns associated with habitat modification in landlocked, deep‐spawning sockeye salmon (Oncorhynchus nerka)

“…Recent work has further demonstrated significant associations between six6 and age at maturity in both sockeye salmon and steelhead trout (Waters et al, 2021;Willis et al, 2020).…”