Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon

Abstract

Understanding the mechanisms by which populations adapt to their environments is a fundamental aim in biology. However, it remains challenging to identify the genetic basis of traits, provide evidence of genetic changes and quantify phenotypic responses. Age at maturity in Atlantic salmon represents an ideal trait to study contemporary adaptive evolution as it has been associated with a single locus in the vgll3 region and has also strongly changed in recent decades. Here, we provide an empirical example of contemporary adaptive evolution of a large-effect locus driving contrasting sex-specific evolutionary responses at the phenotypic level. We identified an 18% decrease in the vgll3 allele associated with late maturity in a large and diverse salmon population over 36 years, induced by sex-specific selection during sea migration. Those genetic changes resulted in a significant evolutionary response only in males, due to sex-specific dominance patterns and vgll3 allelic effects. The vgll3 allelic and dominance effects differed greatly in a second population and were likely to generate different selection and evolutionary patterns. Our study highlights the importance of knowledge of genetic architecture to better understand fitness trait evolution and phenotypic diversity. It also emphasizes the potential role of adaptive evolution in the trend towards earlier maturation observed in numerous Atlantic salmon populations worldwide.

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Fig. 1: Change in mean age at maturity.
Fig. 2: Mean age at maturity as a function of the vgll3 genotype.
Fig. 3: Temporal changes in vgll3*L allele frequency associated with late maturation.
Fig. 4: Model-predicted mean vgll3*L allele frequency as a function of the sex and reproductive status in Tenojoki and Inarijoki populations.

Data availability

The data supporting the findings of this study are available in the Dryad Digital Repository with the identifier doi:10.5061/dryad.7hm4708.

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Acknowledgements

We thank numerous fishers who participated in the collection of scales and phenotypic information over the 40-year study period, E. Niemelä for starting the programme and looking after contacts with fishers, J. Kuusela for organizing the collection of samples from the archive, and several scale readers—especially J. Haantie. This project received funding from the Academy of Finland (projects numbers 284941, 286334, 307593, 302873 and 318939) as well as the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement number 742312) and the University of Helsinki.

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J.E. and P.O. coordinated the collection of samples. C.R.P., Y.C., T.A. and J.E. designed the study. Y.C. analysed the data. Y.C., C.R.P. and T.A. wrote the manuscript. All authors contributed to revision of the manuscript.

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Correspondence to Craig Robert Primmer.

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Czorlich, Y., Aykanat, T., Erkinaro, J. et al. Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon. Nat Ecol Evol 2, 1800–1807 (2018). https://doi.org/10.1038/s41559-018-0681-5

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