Polygenic and major-locus contributions to sexual maturation timing in Atlantic salmon.

Paul V Debes,Nikolai Piavchenko,Jaakko Erkinaro,Jacqueline E Moustakas‐Verho,Craig R Primmer,Tutku Aykanat,Noora Parre,Annukka Ruokolainen,Outi Ovaskainen

doi:10.1111/mec.16062

Paul V Debes, Nikolai Piavchenko + Show 7 more

Open Access

https://doi.org/10.1111/mec.16062

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Abstract

Sexual maturation timing is a life-history trait central to the balance between mortality and reproduction. Maturation may be triggered when an underlying compound trait, called liability, exceeds a threshold. In many different species and especially fishes, this liability is approximated by growth and body condition. However, environmental vs. genetic contributions either directly or via growth and body condition to maturation timing remain unclear. Uncertainty exists also because the maturation process can reverse this causality and itself affect growth and body condition. In addition, disentangling the contributions of polygenic and major loci can be important. In many fishes, males mature before females, enabling the study of associations between male maturation and maturation-unbiased female liability traits. Using 40 Atlantic salmon families, longitudinal common-garden experimentation, and quantitative genetic analyses, we disentangled environmental from polygenic and major locus (vgll3) effects on male maturation, and sex-specific growth and condition. We detected polygenic heritabilities for maturation, growth, and body condition, and vgll3 effects on maturation and body condition but not on growth. Longitudinal patterns for sex-specific phenotypic liability, and for genetic variances and correlations between sexes suggested that early growth and condition indeed positively affected maturation initiation. However, towards spawning time, causality appeared reversed for males whereby maturation affected growth negatively and condition positively via both the environmental and genetic effects. Altogether, the results indicate that growth and condition are useful traits to study liability for maturation initiation, but only until maturation alters their expression, and that vgll3 contributes to maturation initiation via condition.

Highlights

Sexual maturation timing is a central life-history trait that contributes to fitness by trading off individual survival and reproductive success, and contributes thereby to per capita population growth rate (Bernardo, 1993; Roff, 1992, 2002; Stearns, 1992; Wells et al, 2017)
In Atlantic salmon, there is a long history of sexual maturation studies (Andersson et al, 2018; Marschall et al, 1998; Meerburg, 1986) and investigations of maturation as a threshold trait (Myers & Hutchings, 1986; Piché et al, 2008)
Mirroring the mechanistic assumptions for how maturation is initiated in many animal species (Dupont et al, 2014; Koyama et al, 2020; Parker & Cheung, 2020; Shalitin & Phillip, 2003), age- or season-specific size, growth rate, or available energy reserves have all been suggested as liability traits determining the sexual maturation timing in fishes

Summary

| INTRODUCTION

Sexual maturation timing is a central life-history trait that contributes to fitness by trading off individual survival and reproductive success, and contributes thereby to per capita population growth rate (Bernardo, 1993; Roff, 1992, 2002; Stearns, 1992; Wells et al, 2017). The maturation process can reduce somatic growth by competing with resources and lower condition by depleting reserves, or affect both growth and condition, for example, via appetite (Andersson et al, 2018; Stearns & Koella, 1986; Taranger et al, 2010) Related to this problem, fundamental knowledge on the presence and relative importance of environmental versus genetic contributions to maturation timing and their link to liability traits remains limited (Dunlop et al, 2009; Enberg et al, 2012; Gjedrem & Baranski, 2005; Law, 2007). In Atlantic salmon, there is a long history of sexual maturation studies (Andersson et al, 2018; Marschall et al, 1998; Meerburg, 1986) and investigations of maturation as a threshold trait (Myers & Hutchings, 1986; Piché et al, 2008) This species offers features allowing for jointly assessing environmental and genetic effects of maturation and the liability traits growth and body condition. The longitudinal study of these families in a common-garden environment, involving a temporary food restriction treatment, enabled estimates of environmental versus genetic contributions to

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Findings

| DISCUSSION