Genomic basis of fishing-associated selection varies with population density

Abstract

Fisheries induce one of the strongest anthropogenic selective pressures on natural populations, but the genetic effects of fishing remain unclear. Crucially, we lack knowledge of how capture-associated selection and its interaction with reductions in population density caused by fishing can potentially shift which genes are under selection. Using experimental fish reared at two densities and repeatedly harvested by simulated trawling, we show consistent phenotypic selection on growth, metabolism, and social behavior regardless of density. However, the specific genes under selection-mainly related to brain function and neurogenesis-varied with the population density. This interaction between direct fishing selection and density could fundamentally alter the genomic responses to harvest. The evolutionary consequences of fishing are therefore likely context dependent, possibly varying as exploited populations decline. These results highlight the need to consider environmental factors when predicting effects of human-induced selection and evolution.

Keywords: anthropogenic effects; density-dependent effects; environmental change; fisheries; sequencing.

Fig. 1.

Physiological and behavioral phenotypic selection in the two density populations. The distribution of the specific growth rate (A), aerobic scope (adjusted to the mean mass of the fish, i.e., 0.30 g) (B), level of aggressiveness (C), and sociability (D) of captured (dark gray) and escaped fish (light gray) after a series of trawling simulations reared either under a baseline or reduced density (n = 75 per group). Different letters indicate significant difference among the conditions (GLM: P < 0.05).

Fig. 2.

Genomic variation and selection in the two density populations. (A) Distribution of the allele frequency difference between captured and escaped fish after a series of trawl simulations, with the complete set of SNPs (5 666 304 SNPs) and the outlier SNPs (480 and 517 SNPs in the baseline and reduced density respectively) in the fish reared under baseline (dark blue) or reduced (light blue) density. The dark line represents the outlier threshold based on the 0.5% quantiles of the Bonferroni-corrected zdAF (4.65 and −4.77, upper and lower cutoff, respectively). (B) Distribution of the genomic PC score of the outliers of captured (dark gray) and escaped fish (light gray) after a series of trawling simulations, reared either under a baseline or reduced density (n = 24 per group). Different letters indicate significant difference among the conditions (GLM: P < 0.05).

Fig. 3.

Outlier GO terms from the genes selected by the fishing simulation in the two density populations. The significance and fold enrichment of the 15 most significant GO terms are represented in the outliers of the fish reared under a baseline (A) or reduced (B) density. The numbers shown in parentheses are the GO identities of each biological process and GO term. Dark blue GO terms represent GO terms only present in the baseline density population, while clear blue GO terms represent GO terms only present in the reduced density population. Orange GO terms represent the GO terms present in the two populations. GO terms with asterisks are the GO terms with significant enrichment (FDR < 0.05). The complete list of the outlier GO terms from each population is available in SI Appendix, Table S1.

Fig. 4.

Summary of the phenotypic and genomic selection by the fishing simulation according to population density. Shown are differences in captured fish relative to those that were never captured, illustrating the selection by fishing on the phenotypes (physiological and behavioral traits) and the genomes (outlier SNPs, annotated genes, GO terms, and enriched GO terms) of fish reared at a baseline (dark blue) or reduced (light blue) density. The overlapping section represents the selection that is shared between the baseline and reduced density. The complete list of the GO terms from each population is available in SI Appendix, Table S1.

Fig. 5.

Significant correlations between genomic and phenotypic variance. The correlations between the genomic PC score of the outliers and mass (A), specific growth rate (B), and aggressiveness (C) of captured (round shape) and escaped (triangle shape) fish after a series of small-scale trawling simulations reared either under a baseline (dark blue) or reduced (light blue) density (n = 24 per group). The black line in C represents the main effect of genomic PC score (there was no interaction with density). The shaded areas around the lines correspond to 95% intervals.