Abstract

Alternative mating tactics have important ecological and evolutionary implications and are determined by complex interactions between environmental and genetic factors. Here, we study the genetic effect and architecture of the variability in reproductive tactics among Atlantic salmon males which can either mature sexually early in life in freshwater or more commonly only after completing a migration at sea. We applied the latent environmental threshold model (LETM), which provides a conceptual framework linking individual status to a threshold controlling the decision to develop alternative traits, in an innovative experimental design using a semi-natural river which allowed for ecologically relevant phenotypic expression. Early male parr maturation rates varied greatly across families (10 to 93%) which translated into 90% [64–100%] of the phenotypic variation explained by genetic variation. Three significant QTLs were found for the maturation status, however only one collocated with a highly significant QTL explaining 20.6% of the variability of the maturation threshold located on chromosome 25 and encompassing a locus previously shown to be linked to sea age at maturity in anadromous Atlantic salmon. These results provide new empirical illustration of the relevance of the LETM for a better understanding of alternative mating tactics evolution in natural populations.

Highlights

  • Ecologically-relevant context to better understand the genetic basis and the genetic architecture of the components of alternative reproductive tactics

  • We explore for the first time the genomic aspect of the different components of early male parr maturation by performing quantitative trait locus (QTL) analyses of early growth, maturation status and threshold to characterize the genetic architecture of alternative reproductive tactics

  • Our study is a rare empirical application of the environmental threshold model which reports unequivocal evidence for a genetically determined threshold and further characterises the genetic architecture for the components of a threshold trait involved in alternative life histories in a vertebrate

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Summary

Introduction

Ecologically-relevant context to better understand the genetic basis and the genetic architecture of the components of alternative reproductive tactics. Mature male parr take advantage of their small size that can be up to two or three order of magnitude smaller than anadromous males (Fig. 1a) to sneak into female nests and furtively gain paternity[19]. This alternative mating tactic probably evolved among males to escape strong competition for access to females[18]. Evidence from experimental studies including artificial crosses followed by rearing in laboratory conditions and from studies in natural populations has demonstrated a genetic component for early male maturation in S. salar[15,22,23,24,25,26,27]. We explore for the first time the genomic aspect of the different components of early male parr maturation by performing QTL analyses of early growth, maturation status and threshold to characterize the genetic architecture of alternative reproductive tactics

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