Harvesting-induced evolution of collective risk-taking behavior and changes to the circadian system in a fish

Abstract

16The circadian system is phylogenetically conserved across a wide range of taxa. It 17 orchestrates organismal biological processes and is linked to life history and risk-taking 18 behavior. Fisheries-induced evolution affects life history and may also alter behavioral 19 traits in exploited populations. Thus, intensive and selective harvesting may lead to the 20 evolution of the circadian system and thereby affect temporal organization of 21 physiological processes. We present experimental results based on zebrafish (Danio 22 rerio) selection lines exposed to either large or small size-selective mortality relative to 23 a control, simulating evolutionary responses to intensive fishing. We show that size-24 selective harvest leads to evolution of life-history, risk-taking and shoaling behaviors, 25 and importantly, also shifts the molecular circadian clockwork. Evolutionary effects of 26 size-selective harvesting on risk-taking and shoaling were linked to daily activity 27 rhythms in the small, but not in the large, size-selective mortality scenario. Both small 28 and large size-selective mortality induced an evolutionary shift of the molecular 29 circadian clockwork in the same direction in the brain and liver. Interestingly, the shifts 30 in the molecular circadian clockwork disappeared in the clock output pathway, 31 resulting in similar transcription profile among size-selective scenarios. We reveal that 32 size-selective harvesting not only alters life-histories, but also leaves an evolutionary 33 legacy in the behavioral and physiological machinery of exploited fish populations. 34 These changes can affect catchability, yield, recovery and the way exploited fish 35 population use space and time and maybe difficult to be reversed even when 36 harvesting is halted. 37 38 39 40 Significance statement: 41 Harvesting constitutes a strong driver of life history evolution in wild populations, but 42 there is limited knowledge whether harvesting also leads to adaptive changes in the 43 underlying physiology and behavior of exploited populations. We use a multi-44 generation zebrafish (Danio rerio) harvesting experiment simulating two different 45 fisheries scenarios and we show that size-selective mortality affect the circadian 46 system and collective fish personality traits. Such adaptations were present eight 47 65 syndrome proposes that life-history traits, such as growth rate or maturation size, are 66 systematically and genetically related to behavioural and physiological traits (11). 67 Accordingly, life-history adaptations caused by fisheries can also be expected to 68 indirectly affect the physiology and behavior of exploited fishes (5, 6, 9). Secondly, 69 fisheries can also directly select on physiological and behavioural traits, e.g., because 70 bold, aggressive, social or stress-resilient fishes are preferentially harvested with 71 certain gears (12-16). Theory (6, 9) and experimental harvesting with model fish 72 species (17)(18)(19) have indeed shown that both elevat...

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

“…1D). This confirms a fixed evolutionary change in body length and hence growth rate in response to size-selective harvest at F13 that is eight generations after the experimental harvest stopped (34). To control possible confounding effects of body size on the evolutionary effect of size-selective harvesting on behavior (see methods for more details) we composed a subsample of the dataset with size-matched individuals without significant (χ 2…”

“…We firstly characterized risk-taking and cohesion of the shoals to confirm previously documented preliminary patterns at the collective level (34). To fully understand the mechanistic process driving the resulting collective phenomena, we developed an individual-based model that related…”

“…Overall, the size-selection triggered changes in energy allocation patterns, with the large-harvested line investing early and intensively into reproduction, and the small-harvested line investing early but at low intensity into gonad production and more intensively in somatic growth. Moreover, the selection lines differed significantly in their behavioural traits, size variability, allele frequency and gene expression profiles (6,29,34,(40)(41)(42) B. Experimental design.…”

“…This is due to the selfish herd effect, which proposes that predation mortality risk decreases in more cohesive shoals (18), and the confusion effect, which assumes that attack rate of predators decreases with higher prey densities (33). Hence, a decrease of risktaking behavior should be accompanied with an increase of shoal cohesion, but preliminary studies with the zebrafish selection lines suggested the opposite (34).…”

“…The zebrafish lines that we studied were subjected to two treatments together with a control: large-harvested line (largest individuals preferentially harvested, the typical case in most fisheries), small-harvested line (smallest individuals preferentially harvested, a possible case in fisheries managed with a maximumsize limit or where dome-shaped selectivity is prevalent) and random-harvested line (control; individuals randomly harvested with respect to size). Previous results revealed substantial changes in life history, size variation, gene expression, allele frequencies as well as individual and collective behavioral traits (6,29,34,(40)(41)(42), but the mechanistic underpinning of the collective behavioral changes observed in the cited studies remained untackled.…”