NEW YORK (GenomeWeb) – A team of researchers from Norway and Finland has identified a locus that controls the age of maturity in Atlantic salmon.
Through a genome-wide association study, the team homed in on two candidate loci, one of which — VGLL3 — has a large effect size and exhibits sex-dependent dominance that leads to earlier maturation in male and later maturation in female salmon, as the team reported in Nature today.
"The discovery of a major locus affecting age at maturity will have a substantial impact on population management of Atlantic salmon, where a decrease in the frequency of late maturation has been observed in many populations," the University of Turku's Craig Primmer and his colleagues wrote in their paper.
VGLL3 also has been linked to size and age at maturity in humans, suggesting evolutionary conservation across large taxonomic distances, the researchers added.
Primmer and his colleagues conducted their GWAS for age at maturity in two sets of Atlantic salmon, one cohort of 463 salmon from the Tana river system and the other of 941 salmon from the Norwegian coast. In both sets, a 100-kilobase region on chromosome 25 was linked to age at maturity, an association they confirmed in a third cohort of 114 fish from the Baltic Sea. This region, the researchers added, explains nearly 40 percent of the phenotypic variation.
They noted two candidate loci in this region: VGLL3, a transcription cofactor that plays a role in adipogenesis, and AKAP11, which is expressed during spermatogenesis.
Through targeted whole-genome resequencing of 32 individuals from seven populations, the researchers uncovered two missense mutations in VGLL3 that were in strong linkage disequilibrium with a nearby genic SNP as well as with each other, and confirmed a missense SNP in AKAP11. Two of these mutations — VGLL3 Asn323Lys and AKAP11 Val214Met — were predicted to influence phenotype, the researchers added.
Two alleles from the most highly associated VGLL3 locus conferred either early (E) or late (L) maturation, Primmer and his colleagues reported. LL individuals, they added, had higher odds ratios for delayed maturation. For instance, female LL individuals matured an average 0.87 years later and male LL individuals matured an average 0.86 years later than EE individuals.
This is "a remarkable shift," the researchers said, as the average age at maturity for salmon is 1.6 years. They further noted that the locus also influenced size at maturity.
In addition, Primmer and his colleagues reported a difference in dominance patterns between the sexes. In female salmon, the L allele was partly dominant, they said, while in male salmon, the E allele was completely dominant. This, they added, could provide a mechanism that leads to more male fish that mature earlier, as compared to female fish.
Earlier maturation in male fish, they noted, enables them to spawn earlier and avoid the risk of dying before reproducing, while later maturation in female fish enables them to be larger and have greater reproductive success.
Variation at VGLL3, they said, was conserved in 53 of the 54 Norwegian salmon populations studies, with large salmon in each population maintaining intermediate allele frequencies.
This, they added, is consistent with balancing selection, which maintains variation in fitness-related traits, as is the large effect size of the VGLL3 locus. Overall, this is consistent with evolutionary theory, the researchers said, as it posits that beneficial alleles of medium-to-large effects are likely to be maintained through balancing selection, especially when the phenotypic and fitness effect vary by sex.
The researchers also found higher levels of extended homozygosity around the L allele, as compare to the E allele, in salmon populations with an older average age at maturity, and the converse pattern in populations that generally mature at a younger age.
This, they said, is consistent with a systematic shift in selection pressure for early or late maturation alleles, and that shift then leads to divergent evolution among populations, enabling them to reach the local optimum.
As a decline in late maturation has been observed in salmon, the researchers also noted that their findings could inform the population management of Atlantic salmon.