Evolutionary impact of size-selective harvesting on shoaling behavior: Individual-level mechanisms and possible consequences for natural and fishing mortality

Abstract

Many fisheries around the globe preferentially capture large individuals with implications for the evolution of exploited populations. Fisheries-induced evolution may alter collective behavioral phenotypes through individual-level adaptations that affect boldness, swimming speed and tendency to follow social vs. environmental cues. Studying the behavioural mechanisms that give rise to possible changes in shoaling and other collective outputs is challenging in the wild, but first insights into whether intensive and size-selective harvesting could alter collective phenotypes and shoaling can be gathered through experiment of size-selective harvesting conducted in the laboratory. We present a multi-generation harvest selection experiment with zebrafish (Danio rerio) as a model species and demonstrate that large size-selective harvesting typical of global fisheries decreases risk-taking behavior of individuals, and surprisingly also decreases shoal cohesion. This counter-intuitive effect at the collective level is mechanistically caused by risk-averse individuals favored under large size-selective harvest paying more attention to environmental instead of social cues. Agent-based model simulations further reveal that fisheries-induced evolution of shoaling behavior is adaptive under fishing scenarios by decreasing exploitation rate. By contrast, the same collective behavior favored by size-selective harvesting is maladaptive in the presence of natural predation and increases natural mortality. The evolutionary adaptations we document may slowly, but steadily erode the natural fitness benefits offered by shoaling in many species targeted by global fisheries. Erosion of shoal cohesion can also negatively affect catchability with consequences for human well-being. boldness | cohesion | swimming | catchability | collective | fishing

Impact of Variable Speed on Collective Movement of Animal Groups

“…A particularly prominent simplification often encountered in models of collective behavior is the assumption of constant speed of individual agents [13,[21][22][23]; for exceptions see [24][25][26][27][28]. However, although animals may generally tend to move at a certain, often preferred, speed, they are also able to flexibly modify their speed, ranging from non-moving to the maximum of their movement capacity.…”

“…These feedbacks incorporate both, the physics and behavioral side of collective behavior. Due to this combination, they have not been explored, to our best knowledge, in the field of 1) active aligning particle models [16,18,33,34], which are often variants of the Vicsek model that either lack inertia, repulsion and/or speed variability (none of those is present in the Vicsek model), 2) active Brownian particles [35] which consider speed variablility and repulsion but operate normally in the over-damped limit (no inertia) and rarely take alignment into account, 3) burst-coast models [26][27][28]36] which model swimming behavior in greater detail (distinct phases of de-and acceleration) but either speeds are picked randomly independent of social interactions and current state [27,36] or the focus was to resemble experimentally observed individual behavior in detail without investigating emergent effects on the collective level [26,28].…”

Size Selective Harvesting Does Not Result in Reproductive Isolation among Experimental Lines of Zebrafish, Danio rerio: Implications for Managing Harvest-Induced Evolution

“…This is evidence that five generations of selection left a genetic legacy in our zebrafish population [19], while maintaining basic genetic variability (Uusi-Heikkilä et al, unpublished data). Moreover, recent studies with these lines (using F 13 ) showed differences in behavioural traits related to biological rhythms, feeding and mating [16,59,60]. Associated with the substantial molecular and phenotypic differences among the size-selected lines, we expected the evolution of line-assortative mating preferences and reproductive success.…”

“…Females could also exert a preference for bolder males with higher risk-taking tendencies [81,95,96]. Previous studies with the zebrafish lines have indicated that control line fish are bolder than the large-harvested line fish [60,61], and this difference in personality could explain why the former were preferred. Large males have higher reproductive success [39,63] and are more often chosen as mating partners in zebrafish [65,70].…”

“…We used experimental selection lines of zebrafish (Danio rerio) subjected to positive (Large-harvested, LH), negative (Small-harvested, SH) and random (Control, RH) size-selective mortality for five consecutive generations [19] and tested the potential for prezygotic reproductive isolation based on line-assortative association preferences. Previous studies with these experimental lines have shown that the three lines differ in body size, reproductive effort [19] and composition of behavioural phenotypes [19,[59][60][61]. The selection lines significantly differed in broad scale gene expression and Single Nucleotide Polymorphism (SNP) allele frequencies [19,61,62], while the global genetic diversity among generations at the onset and after five generation of selection was maintained (Uusi-Heikkilä et al, unpublished data).…”