Evolutionary drivers of kype size in Atlantic salmon (Salmo salar): Domestication, age and genetics

William Bernard Perry; Monica Favnebøe Solberg; Francois Besnier; Lise Dyrhovden; Ivar Helge Matre; Per Gunnar Fjelldal; Fernando Ayllon; Simon Creer; Martin Llewellyn; Martin I. Taylor; Gary Carvalho; Kevin Alan Glover

doi:10.1098/rsos.190021

Evolutionary drivers of kype size in Atlantic salmon (Salmo salar): Domestication, age and genetics

William Bernard Perry, Monica Favnebøe Solberg, Francois Besnier, Lise Dyrhovden, Ivar Helge Matre, Per Gunnar Fjelldal, Fernando Ayllon, Simon Creer, Martin Llewellyn, Martin I. Taylor, Gary Carvalho, Kevin Alan Glover

Research output: Contribution to journal › Article › peer-review

17 Citations (Scopus)

17 Downloads (Pure)

Abstract

The diversity of reproduction and associated mating patterns in Atlantic salmon (Salmo salar) has long captivated evolutionary biologists. Salmo salar exhibit strategies involving migration, bold mating behaviours and radical morphological and physiological change. One such radical change is the elongation and curvature of the lower jaw in sexually mature males into a hook-like appendage called the kype. The kype is a secondary sexual characteristic used in mating hierarchies and a prime candidate for sexual selection. As one of the core global aquaculture fish species, however, mate choice, and thus sexual selection, has been replaced by industrial artificial fertilization seeking to develop more commercially viable strains. Removal of mate choice provides a unique opportunity to examine the kype over successive generations in the absence of sexual selection. Here we use a large-scale common-garden experiment, incorporating six experimental strains (wild, farmed and wild × farmed hybrids), experiencing one to three sea winters, to assess the impact of age and genetic background. After controlling for allometry, fork length-adjusted kype height (AKH) was significantly reduced in the domesticated strain in comparison to two wild strains. Furthermore, genetic variation at a locus on linkage group SSA1 was associated with kype height, and a locus on linkage group SSA23 was associated with fork length-adjusted kype length (AKL). The reduction in fork length-AKH in domesticated salmon suggests that the kype is of importance in mate choice and that it has decreased due to relaxation of sexual selection. Fork length-AKL showed an increase in domesticated individuals, highlighting that it may not be an important cue in mate choice. These results give us insight into the evolutionary significance of the kype, as well as implications of genetic induced phenotypic change caused by domesticated individuals escaping into the natural environment.

Original language	English
Article number	190021
Journal	Royal Society Open Science
Volume	6
Issue number	4
Early online date	17 Apr 2019
DOIs	https://doi.org/10.1098/rsos.190021
Publication status	Published - Apr 2019

Access to Document

10.1098/rsos.190021Licence: CC BY

Published_VersionFinal published version, 1.23 MBLicence: CC BY

Martin Taylor
- Martin.Tayloruea.acuk
- School of Biological Sciences - Associate Professor in Molecular Ecology
- Centre for Ecology, Evolution and Conservation - Member
- Collaborative Centre for Sustainable Use of the Seas - Member
- Organisms and the Environment - Member
Person: Research Group Member, Research Centre Member, Academic, Teaching & Research

Cite this

@article{910ebf062b81458cb81d1c7725335d6f,

title = "Evolutionary drivers of kype size in Atlantic salmon (Salmo salar): Domestication, age and genetics",

abstract = "The diversity of reproduction and associated mating patterns in Atlantic salmon (Salmo salar) has long captivated evolutionary biologists. Salmo salar exhibit strategies involving migration, bold mating behaviours and radical morphological and physiological change. One such radical change is the elongation and curvature of the lower jaw in sexually mature males into a hook-like appendage called the kype. The kype is a secondary sexual characteristic used in mating hierarchies and a prime candidate for sexual selection. As one of the core global aquaculture fish species, however, mate choice, and thus sexual selection, has been replaced by industrial artificial fertilization seeking to develop more commercially viable strains. Removal of mate choice provides a unique opportunity to examine the kype over successive generations in the absence of sexual selection. Here we use a large-scale common-garden experiment, incorporating six experimental strains (wild, farmed and wild × farmed hybrids), experiencing one to three sea winters, to assess the impact of age and genetic background. After controlling for allometry, fork length-adjusted kype height (AKH) was significantly reduced in the domesticated strain in comparison to two wild strains. Furthermore, genetic variation at a locus on linkage group SSA1 was associated with kype height, and a locus on linkage group SSA23 was associated with fork length-adjusted kype length (AKL). The reduction in fork length-AKH in domesticated salmon suggests that the kype is of importance in mate choice and that it has decreased due to relaxation of sexual selection. Fork length-AKL showed an increase in domesticated individuals, highlighting that it may not be an important cue in mate choice. These results give us insight into the evolutionary significance of the kype, as well as implications of genetic induced phenotypic change caused by domesticated individuals escaping into the natural environment.",

author = "Perry, {William Bernard} and Solberg, {Monica Favneb{\o}e} and Francois Besnier and Lise Dyrhovden and Matre, {Ivar Helge} and Fjelldal, {Per Gunnar} and Fernando Ayllon and Simon Creer and Martin Llewellyn and Taylor, {Martin I.} and Gary Carvalho and Glover, {Kevin Alan}",

note = "Data accessibility statement: You can find all morphometric data used in this study in the electronic supplementary material, along with the R code used for the analyses. Data pertaining to the QTL are available from: Besnier F, Glover KA, Lien S, Kent M, Hansen MM, Shen X, Skaala {\O}. 2015 Identification of quantitative genetic components of fitness variation in farmed, hybrid and native salmon in the wild. Heredity 115, 47-55. (doi:10.1038/hdy.2015.15). Funding information: This work was funded by the Norwegian Research Council project INTERACT (grant no. 200510), and the UK Natural Environment Research Council (NERC) Envision doctoral training programme.",

year = "2019",

month = apr,

doi = "10.1098/rsos.190021",

language = "English",

volume = "6",

journal = "Royal Society Open Science",

issn = "2054-5703",

publisher = "The Royal Society",

number = "4",

}

TY - JOUR

T1 - Evolutionary drivers of kype size in Atlantic salmon (Salmo salar): Domestication, age and genetics

AU - Perry, William Bernard

AU - Solberg, Monica Favnebøe

AU - Besnier, Francois

AU - Dyrhovden, Lise

AU - Matre, Ivar Helge

AU - Fjelldal, Per Gunnar

AU - Ayllon, Fernando

AU - Creer, Simon

AU - Llewellyn, Martin

AU - Taylor, Martin I.

AU - Carvalho, Gary

AU - Glover, Kevin Alan

N1 - Data accessibility statement: You can find all morphometric data used in this study in the electronic supplementary material, along with the R code used for the analyses. Data pertaining to the QTL are available from: Besnier F, Glover KA, Lien S, Kent M, Hansen MM, Shen X, Skaala Ø. 2015 Identification of quantitative genetic components of fitness variation in farmed, hybrid and native salmon in the wild. Heredity 115, 47-55. (doi:10.1038/hdy.2015.15). Funding information: This work was funded by the Norwegian Research Council project INTERACT (grant no. 200510), and the UK Natural Environment Research Council (NERC) Envision doctoral training programme.

PY - 2019/4

Y1 - 2019/4

N2 - The diversity of reproduction and associated mating patterns in Atlantic salmon (Salmo salar) has long captivated evolutionary biologists. Salmo salar exhibit strategies involving migration, bold mating behaviours and radical morphological and physiological change. One such radical change is the elongation and curvature of the lower jaw in sexually mature males into a hook-like appendage called the kype. The kype is a secondary sexual characteristic used in mating hierarchies and a prime candidate for sexual selection. As one of the core global aquaculture fish species, however, mate choice, and thus sexual selection, has been replaced by industrial artificial fertilization seeking to develop more commercially viable strains. Removal of mate choice provides a unique opportunity to examine the kype over successive generations in the absence of sexual selection. Here we use a large-scale common-garden experiment, incorporating six experimental strains (wild, farmed and wild × farmed hybrids), experiencing one to three sea winters, to assess the impact of age and genetic background. After controlling for allometry, fork length-adjusted kype height (AKH) was significantly reduced in the domesticated strain in comparison to two wild strains. Furthermore, genetic variation at a locus on linkage group SSA1 was associated with kype height, and a locus on linkage group SSA23 was associated with fork length-adjusted kype length (AKL). The reduction in fork length-AKH in domesticated salmon suggests that the kype is of importance in mate choice and that it has decreased due to relaxation of sexual selection. Fork length-AKL showed an increase in domesticated individuals, highlighting that it may not be an important cue in mate choice. These results give us insight into the evolutionary significance of the kype, as well as implications of genetic induced phenotypic change caused by domesticated individuals escaping into the natural environment.

AB - The diversity of reproduction and associated mating patterns in Atlantic salmon (Salmo salar) has long captivated evolutionary biologists. Salmo salar exhibit strategies involving migration, bold mating behaviours and radical morphological and physiological change. One such radical change is the elongation and curvature of the lower jaw in sexually mature males into a hook-like appendage called the kype. The kype is a secondary sexual characteristic used in mating hierarchies and a prime candidate for sexual selection. As one of the core global aquaculture fish species, however, mate choice, and thus sexual selection, has been replaced by industrial artificial fertilization seeking to develop more commercially viable strains. Removal of mate choice provides a unique opportunity to examine the kype over successive generations in the absence of sexual selection. Here we use a large-scale common-garden experiment, incorporating six experimental strains (wild, farmed and wild × farmed hybrids), experiencing one to three sea winters, to assess the impact of age and genetic background. After controlling for allometry, fork length-adjusted kype height (AKH) was significantly reduced in the domesticated strain in comparison to two wild strains. Furthermore, genetic variation at a locus on linkage group SSA1 was associated with kype height, and a locus on linkage group SSA23 was associated with fork length-adjusted kype length (AKL). The reduction in fork length-AKH in domesticated salmon suggests that the kype is of importance in mate choice and that it has decreased due to relaxation of sexual selection. Fork length-AKL showed an increase in domesticated individuals, highlighting that it may not be an important cue in mate choice. These results give us insight into the evolutionary significance of the kype, as well as implications of genetic induced phenotypic change caused by domesticated individuals escaping into the natural environment.

U2 - 10.1098/rsos.190021

DO - 10.1098/rsos.190021

M3 - Article

SN - 2054-5703

VL - 6

JO - Royal Society Open Science

JF - Royal Society Open Science

IS - 4

M1 - 190021

ER -

Evolutionary drivers of kype size in Atlantic salmon (Salmo salar): Domestication, age and genetics

Abstract

Access to Document

Profiles

Martin Taylor

Cite this