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

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 t...

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Bibliographic Details
Published in:PLOS Genetics
Main Authors: Verta, Jukka-Pekka, Debes, Paul, Piavchenko, Nikolai, Ruokolainen, Annukka, Ovaskainen, Outi Sinikka, Moustakas-Verho, Jacqueline, Tillanen, Seija Iiris, Parre, Noora, Aykanat, Tutku, Erkinaro, Jaakko, Primmer, Craig
Other Authors: Evolution, Conservation, and Genomics, Organismal and Evolutionary Biology Research Programme, Research Services, Genetics, Helsinki Institute of Sustainability Science (HELSUS), Institute of Biotechnology
Format: Article in Journal/Newspaper
Language:English
Published: PUBLIC LIBRARY OF SCIENCE 2020
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Online Access:http://hdl.handle.net/10138/321074
Description
Summary: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 acis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factorvestigial-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 thatvgll3genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling ofvgll3expression in ten tissues across the first year of salmon development, we identify a pubertal transition invgll3expression where maturation coincided with a 66% reduction in testicularvgll3expression. Thelatematuration allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform ofvgll3pre-puberty. By comparing absolutevgll3mRNA copies in heterozygotes we show that the expression difference between theearlyandlatematurity alleles is largelycis-regulatory. We propose a model whereby expression of a rare isoform from thelateallele 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. Author summary Alternative life history strategies are an important source of diversity within populations and promote the maintenance of adaptive capacity and population resilience. However, in many cases the molecular basis of different life history strategies remains elusive. Age at maturity is a key adaptive life history trait in Atlantic salmon and has a relatively simple ...