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

Autoři: Jukka-Pekka Verta aff001;  Paul Vincent Debes aff001;  Nikolai Piavchenko aff001;  Annukka Ruokolainen aff001;  Outi Ovaskainen aff001;  Jacqueline Emmanuel Moustakas-Verho aff001;  Seija Tillanen aff001;  Noora Parre aff001;  Tutku Aykanat aff001;  Jaakko Erkinaro aff003;  Craig Robert Primmer aff001
Působiště autorů: Organismal and Evolutionary Biology Research Programme, University of Helsinki, Viikinkaari, Helsinki, Finland aff001;  Organismal and Evolutionary Biology Research Programme, University of Helsinki, Helsinki, Finland aff001;  Institute of Biotechnology, University of Helsinki, Finland aff002;  Natural Resources Institute Finland (LUKE), Oulu, Finland aff003
Vyšlo v časopise: Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009055
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009055


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.

Klíčová slova:

Alleles – Fish – Genetic polymorphism – Gonads – Heterozygosity – Puberty – Testes – 5' UTR


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