Implications for introgression: has selection for fast growth altered the size threshold for precocious male maturation in domesticated Atlantic salmon?

Abstract

BackgroundMature male parr (MMP) represent an important alternative life-history strategy in Atlantic salmon populations. Previous studies indicate that the maturation size threshold for male parr varies among wild populations and is influenced by individual growth, environmental conditions, and genetics. More than ten generations of breeding have resulted in domesticated salmon displaying many genetic differences to wild salmon, including greatly increased growth rates. This may have resulted in domesticated fish with the potential to outgrow the size threshold for early maturation, or evolution of the size threshold of the trait itself. To investigate this, we performed a common-garden experiment under farming conditions using 4680 salmon from 39 families representing four wild, two wild-domesticated hybrid, and two domesticated strains.ResultsDomesticated salmon outgrew wild salmon 2–5-fold, and hybrids displayed intermediate growth. Overall, the numbers of MMP varied greatly among families and strains: averaging 4–12% in domesticated, 18–25% in hybrid, and 43–74% in the wild populations. However, when the influence of growth was accounted for, by dividing fish into lower and upper size modes, no difference in the incidence of MMP was detected among domesticated and wild strains in either size mode. In the lower size mode, hybrids displayed significantly lower incidences of mature males than their wild parental strains. No consistent differences in the body size of MMP, connected to domestication, was detected.ConclusionsOur data demonstrate: 1- no evidence for the evolution of the size threshold for MMP in domesticated salmon, 2- the vastly lower incidence of MMP in domesticated strains under aquaculture conditions is primarily due to their genetically increased growth rate causing them to outgrow the size threshold for early maturation, 3- the incidence of MMP is likely to overlap among domesticated and wild salmon in the natural habitat where they typically display overlapping growth, although hybrid offspring may display lower incidences of mature male parr. These results have implications for wild salmon populations that are exposed to introgression from domesticated escapees.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1294-y) contains supplementary material, which is available to authorized users.

Autosomal sdY Pseudogenes Explain Discordances Between Phenotypic Sex and DNA Marker for Sex Identification in Atlantic Salmon

“…Over the past decade, we have conducted a number of pedigree-controlled studies on a multiple-generation experimental population of domesticated and wild Atlantic salmon and their crosses at the aquaculture facility owned by the Institute of Marine Research located in Matre, western Norway ( Solberg et al, 2013 , 2014 ; Ayllon et al, 2015 ; Harvey et al, 2016 , 2018 ; Glover et al, 2018 , 2020 ; Perry et al, 2019 ; Besnier et al, 2020 ). The reader is directed to these publications for full details regarding the standard rearing conditions experienced in this fish farm.…”

“…Following the above-mentioned procedure, 97–99% of the offspring were unambiguously assigned to their family of origin. The laboratory conducting these analyses has extensive experience in DNA parentage testing ( Solberg et al, 2013 , 2014 ; Harvey et al, 2016 , 2018 ; Glover et al, 2018 ), and the full details regarding the markers used and their amplification conditions are available in these previous studies.…”

Sex determining gene transposition as an evolutionary platform for chromosome turnover

“…Over the past decade, we have studied an experimental population of domesticated and wild Atlantic salmon and their crosses at the aquaculture facility owned by the Institute of Marine Research located in Matre, western Norway (Solberg et al 2013;Solberg et al 2014;Ayllon et al 2015;Harvey et al 2016;Glover et al 2018;Harvey et al 2018). The reader is directed to these publications for full details regarding the standard rearing conditions experienced in this fish farm.…”

“…Total DNA from all offspring and parents was purified using the Qiagen DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany) according to the manufacturer´s recommendations Microsatellite DNA parentage testing was used to unambiguously identify the pedigree of all individuals used in this study using the exclusion based method implemented in FAP (Taggart 2007). The laboratory conducting these analyses has extensive experience in DNA parentage testing (Solberg et al 2013;Solberg et al 2014;Harvey et al 2016;Glover et al 2018;Harvey et al 2018), and the full details regarding the markers used and their amplification conditions are available in these previous studies. In addition to microsatellites, a set of 116 genome-wide distributed SNPs were genotyped in all offspring and parents for the purpose of linkage mapping (see below).…”

Regulatory issues for genetically modified animals

“…A theoretical paper suggested that the escape of a growthenhanced fish could lead to the demise of natural salmon stocks [135,136] despite clear indications that this speculative extreme concern would not happen in nature [137] . The theory has been field tested with farmed Norwegian Atlantic salmon where the dire consequences have not occurred despite thousands of growth-enhanced salmon escaping from Norwegian net pens [138][139][140] . In nature only about 1/1000 to 1/10000 fish eggs reach sexual maturity.…”