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

• Published in: PLOS Genetics
• Main Authors: Verta, Jukka-Pekka, Debes, Paul Vincent, Piavchenko, Nikolai, Ruokolainen, Annukka, Ovaskainen, Outi, Moustakas-Verho, Jacqueline Emmanuel, Tillanen, Seija, Parre, Noora, Aykanat, Tutku, Erkinaro, Jaakko, Primmer, Craig Robert
• Format: Text
• Language: English
• Published: Public Library of Science 2020
• Subjects: Research Article; Atlantic salmon; Salmo salar
• Online Access: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7549781/; http://www.ncbi.nlm.nih.gov/pubmed/32997662; https://doi.org/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.