Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism

The ecological role of heritable phenotypic variation in free-living populations remains largely unknown. Knowledge of the genetic basis of functional ecological processes can link genomic and phenotypic diversity, providing insight into polymorphism evolution and how populations respond to environm...

Full description

Bibliographic Details
Published in:Molecular Ecology
Main Authors: Aykanat, Tutku, Jacobsen, Jan Arge, Hindar, Kjetil
Format: Article in Journal/Newspaper
Language:English
Published: 2024
Subjects:
Online Access:https://hdl.handle.net/11250/3146011
https://doi.org/10.1111/mec.17465
id ftninstnf:oai:brage.nina.no:11250/3146011
record_format openpolar
spelling ftninstnf:oai:brage.nina.no:11250/3146011 2024-09-15T17:55:55+00:00 Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism Aykanat, Tutku Jacobsen, Jan Arge Hindar, Kjetil Atlantic 2024 application/pdf https://hdl.handle.net/11250/3146011 https://doi.org/10.1111/mec.17465 eng eng Andre: Research Council of Finland, Grant/Award Number: 325964 Andre: Research Council of Finland, Grant/Award Number: 328860 Andre: Research Council of Finland, Grant/Award Number: 353388 Norges forskningsråd: 280308 urn:issn:0962-1083 https://hdl.handle.net/11250/3146011 https://doi.org/10.1111/mec.17465 cristin:2284795 Navngivelse 4.0 Internasjonal http://creativecommons.org/licenses/by/4.0/deed.no © 2024 The Authors 33 Molecular Ecology e17465 Atlantic salmon feeding strategy life history evolution polymorphism six6 vgll3 VDP::Zoologiske og botaniske fag: 480 VDP::Zoology and botany: 480 Peer reviewed Journal article 2024 ftninstnf https://doi.org/10.1111/mec.17465 2024-08-15T23:34:58Z The ecological role of heritable phenotypic variation in free-living populations remains largely unknown. Knowledge of the genetic basis of functional ecological processes can link genomic and phenotypic diversity, providing insight into polymorphism evolution and how populations respond to environmental changes. By quantifying the marine diet of Atlantic salmon, we assessed how foraging behaviour changes along the ontogeny, and in relation to genetic variation in two loci with major effects on age at maturity (six6 and vgll3). We used a two-component, zero-inflated negative binomial model to simultaneously quantify foraging frequency and foraging outcome, separately for fish and crustaceans diets. We found that older salmon forage for both prey types more actively (as evidenced by increased foraging frequency), but with a decreased efficiency (as evidenced by fewer prey in the diet), suggesting an age-dependent shift in foraging dynamics. The vgll3 locus was linked to age-dependent changes in foraging behaviour: Younger salmon with vgll3LL (the genotype associated with late maturation) tended to forage crustaceans more often than those with vgll3EE (the genotype associated with early maturation), whereas the pattern was reversed in older salmon. Vgll3 LL genotype was also linked to a marginal increase in fish acquisition, especially in younger salmon, while six6 was not a factor explaining the diet variation. Our results suggest a functional role for marine feeding behaviour linking genomic diversity at vgll3 with age at maturity among salmon, with potential age-dependent trade-offs maintaining the genetic variation. A shared genetic basis between dietary ecology and age at maturity likely subjects Atlantic salmon populations to evolution induced by bottom-up changes in marine productivity. Atlantic salmon, feeding strategy, life history evolution, polymorphism, six6, vgll3 publishedVersion Article in Journal/Newspaper Atlantic salmon Norwegian Institute for Nature Research: Brage NINA Molecular Ecology 33 16
institution Open Polar
collection Norwegian Institute for Nature Research: Brage NINA
op_collection_id ftninstnf
language English
topic Atlantic salmon
feeding strategy
life history evolution
polymorphism
six6
vgll3
VDP::Zoologiske og botaniske fag: 480
VDP::Zoology and botany: 480
spellingShingle Atlantic salmon
feeding strategy
life history evolution
polymorphism
six6
vgll3
VDP::Zoologiske og botaniske fag: 480
VDP::Zoology and botany: 480
Aykanat, Tutku
Jacobsen, Jan Arge
Hindar, Kjetil
Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism
topic_facet Atlantic salmon
feeding strategy
life history evolution
polymorphism
six6
vgll3
VDP::Zoologiske og botaniske fag: 480
VDP::Zoology and botany: 480
description The ecological role of heritable phenotypic variation in free-living populations remains largely unknown. Knowledge of the genetic basis of functional ecological processes can link genomic and phenotypic diversity, providing insight into polymorphism evolution and how populations respond to environmental changes. By quantifying the marine diet of Atlantic salmon, we assessed how foraging behaviour changes along the ontogeny, and in relation to genetic variation in two loci with major effects on age at maturity (six6 and vgll3). We used a two-component, zero-inflated negative binomial model to simultaneously quantify foraging frequency and foraging outcome, separately for fish and crustaceans diets. We found that older salmon forage for both prey types more actively (as evidenced by increased foraging frequency), but with a decreased efficiency (as evidenced by fewer prey in the diet), suggesting an age-dependent shift in foraging dynamics. The vgll3 locus was linked to age-dependent changes in foraging behaviour: Younger salmon with vgll3LL (the genotype associated with late maturation) tended to forage crustaceans more often than those with vgll3EE (the genotype associated with early maturation), whereas the pattern was reversed in older salmon. Vgll3 LL genotype was also linked to a marginal increase in fish acquisition, especially in younger salmon, while six6 was not a factor explaining the diet variation. Our results suggest a functional role for marine feeding behaviour linking genomic diversity at vgll3 with age at maturity among salmon, with potential age-dependent trade-offs maintaining the genetic variation. A shared genetic basis between dietary ecology and age at maturity likely subjects Atlantic salmon populations to evolution induced by bottom-up changes in marine productivity. Atlantic salmon, feeding strategy, life history evolution, polymorphism, six6, vgll3 publishedVersion
format Article in Journal/Newspaper
author Aykanat, Tutku
Jacobsen, Jan Arge
Hindar, Kjetil
author_facet Aykanat, Tutku
Jacobsen, Jan Arge
Hindar, Kjetil
author_sort Aykanat, Tutku
title Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism
title_short Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism
title_full Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism
title_fullStr Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism
title_full_unstemmed Ontogenetic variation in the marine foraging of Atlantic salmon functionally links genomic diversity with a major life history polymorphism
title_sort ontogenetic variation in the marine foraging of atlantic salmon functionally links genomic diversity with a major life history polymorphism
publishDate 2024
url https://hdl.handle.net/11250/3146011
https://doi.org/10.1111/mec.17465
op_coverage Atlantic
genre Atlantic salmon
genre_facet Atlantic salmon
op_source 33
Molecular Ecology
e17465
op_relation Andre: Research Council of Finland, Grant/Award Number: 325964
Andre: Research Council of Finland, Grant/Award Number: 328860
Andre: Research Council of Finland, Grant/Award Number: 353388
Norges forskningsråd: 280308
urn:issn:0962-1083
https://hdl.handle.net/11250/3146011
https://doi.org/10.1111/mec.17465
cristin:2284795
op_rights Navngivelse 4.0 Internasjonal
http://creativecommons.org/licenses/by/4.0/deed.no
© 2024 The Authors
op_doi https://doi.org/10.1111/mec.17465
container_title Molecular Ecology
container_volume 33
container_issue 16
_version_ 1810432132427808768