Rapid, broad‐scale gene expression evolution in experimentally harvested fish populations

Abstract

Gene expression changes potentially play an important role in adaptive evolution under human-induced selection pressures, but this has been challenging to demonstrate in natural populations. Fishing exhibits strong selection pressure against large body size, thus potentially inducing evolutionary changes in life history and other traits that may be slowly reversible once fishing ceases. However, there is a lack of convincing examples regarding the speed and magnitude of fisheries-induced evolution, and thus, the relevant underlying molecular-level effects remain elusive. We use wild-origin zebrafish (Danio rerio) as a model for harvest-induced evolution. We experimentally demonstrate broad-scale gene expression changes induced by just five generations of size-selective harvesting, and limited genetic convergence following the cessation of harvesting. We also demonstrate significant allele frequency changes in genes that were differentially expressed after five generations of size-selective harvesting. We further show that nine generations of captive breeding induced substantial gene expression changes in control stocks likely due to inadvertent selection in the captive environment. The large extent and rapid pace of the gene expression changes caused by both harvest-induced selection and captive breeding emphasizes the need for evolutionary enlightened management towards sustainable fisheries.

Among‐family variation in survival and gene expression uncovers adaptive genetic variation in a threatened fish

“…Differential responses to thiamine deficiency among families comprise 1,446 putatively adaptive genes. The large number of putatively adaptive genes with expression patterns that may be subject to selection is consistent with previous findings describing major roles for regulatory changes in adaptation (Jones et al, ; Schoville, Barreto, Moy, Wolff, & Burton, ; Uusi‐Heikkilä et al, ). A total of 812 genes were significantly upregulated in untreated individuals from high‐survival families (Figure a,c).…”

“…One alternative to these approaches is experimental transcriptomics. By carefully designing treatments, rearing F 1 offspring in a common environment and deeply sequencing mRNA, it is possible to uncover an adaptive, genetic response to selection (Christie, Marine, Fox, French, & Blouin, ; Passow et al, ; Uusi‐Heikkilä, Sävilammi, Leder, Arlinghaus, & Primmer, ). Coupling family‐level replication and formal survival analyses allows for the disentanglement of treatment effects, required for understanding how individuals plastically respond to environmental stressors, and among‐family variation in survival and gene expression.…”

Implications of fisheries‐induced evolution for population recovery: Refocusing the science and refining its communication

“…Although laboratory selection experiments (e.g. Conover & Munch, ; Edley & Law, ; Uusi‐Heikkilä, Savilammi, Leder, Arlinghaus, & Primmer, ; Uusi‐Heikkilä et al, ) and theoretical modelling (e.g. Dunlop, Heino, & Dieckmann, ; Ernande, Dieckmann, & Heino, ; Stokes et al, ) make a strong case for the existence of FIE, there are considerably more reviews of FIE (more than ten; cf.…”

“…There is considerable evidence that fisheries-like selection in a laboratory setting can effect genetic change (e.g. Conover & Munch, 2002;Uusi-Heikkilä et al, 2017;Uusi-Heikkilä et al, 2015), but empirical evidence of such change in wild populations is, at best, not nearly as strong as it is for HIE resulting from hatcheries and aquaculture.…”

Size‐selective harvesting fosters adaptations in mating behaviour and reproductive allocation, affecting sexual selection in fish

“…In earlier studies, the zebrafish selection lines have been found to differ phenotypically in reproductive allocation (defined as the amount of energy allocated to reproduction; Lester, Shuter, & Abrams, ), post‐maturation growth and adult body size (Uusi‐Heikkilä et al, ). Moreover, the selection lines differ genetically, in gene expression profiles and in personality traits (Sbragaglia, Alós, et al, ; Uusi‐Heikkilä, Savilammi, Leder, Arlinghaus, & Primmer, ; Uusi‐Heikkilä et al, ). In particular, the line in which large individuals were harvested (simulated trawl‐like selectivity patterns or harvest regulations mimicking minimum‐landing sizes) evolved a smaller body length, earlier age at maturity, higher relative fecundity and a smaller maximum length compared to the control, suggesting evolution towards a fast life history (Uusi‐Heikkilä et al, ).…”