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Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon.


ABSTRACT: A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report a cis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factor vestigial-like 3 (vgll3) associate with variation in a key life history trait, age at maturity, in Atlantic salmon (Salmo salar). Using a common-garden experiment, we first show that vgll3 genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling of vgll3 expression in ten tissues across the first year of salmon development, we identify a pubertal transition in vgll3 expression where maturation coincided with a 66% reduction in testicular vgll3 expression. The late maturation allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform of vgll3 pre-puberty. By comparing absolute vgll3 mRNA copies in heterozygotes we show that the expression difference between the early and late maturity alleles is largely cis-regulatory. We propose a model whereby expression of a rare isoform from the late allele shifts the liability of its carriers towards delaying puberty. These results exemplify the potential importance of regulatory differences as a mechanism for the evolution of life history traits.

SUBMITTER: Verta JP 

PROVIDER: S-EPMC7549781 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon.

Verta Jukka-Pekka JP   Debes Paul Vincent PV   Piavchenko Nikolai N   Ruokolainen Annukka A   Ovaskainen Outi O   Moustakas-Verho Jacqueline Emmanuel JE   Tillanen Seija S   Parre Noora N   Aykanat Tutku T   Erkinaro Jaakko J   Primmer Craig Robert CR  

PLoS genetics 20200930 9


A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report a cis-regulatory  ...[more]

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