Genomic basis of fishing-associated selection varies with population density

Crespel, Amélie; Schneider, Kevin; Miller, Toby; Rácz, Anita; Jacobs, Arne; Lindström, Jan; Elmer, Kathryn R.; Killen, Shaun S.

doi:10.1073/pnas.2020833118

Cited by 17 publications

(14 citation statements)

References 67 publications

(79 reference statements)

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“…Our results showed that intensive size-selective mortality leads to complex, multivariate, and asymmetric responses that vary with the type of size-selection operating on fish, a pattern also reported in other recent studies (Claireaux et al 2018;Le Rouzic et al 2020;Renneville et al 2020;Crespel et al 2021b;Bartuseviciute et al 2022). However, we can conclude that size-selective mortality left an evolutionary impact on the ontogentic changes of shoal cohesion and also impacted the physiological basis of behavior.…”

Section: Discussionsupporting

confidence: 87%

Evolutionary implications of size-selective mortality on the ontogenetic development of shoal cohesion: a neurochemical approach using a zebrafish, Danio rerio, harvest selection experiment

Sbragaglia

Roy

Thörnqvist

et al. 2022

Behav Ecol Sociobiol

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Size-selective mortality may evolutionarily alter life-history as well as individual behavioral and physiological traits. Moreover, size-selective mortality can affect group behavioral traits, such as shoaling and collective properties (e.g., shoal cohesion), which are relevant for finding food and reducing risk of predation. Here, we present experimental evidence using selection lines of zebrafish (Danio rerio) that were exposed to positive (large-harvested), negative (small-harvested), and random (control) size-selective mortality for five generations, followed by eight generations during which harvesting was halted to remove maternal effects and to study evolutionarily fixed outcomes. We investigated changes in shoal cohesion and turnover in monoamines in zebrafish through ontogeny. To that end, we repeatedly measured inter-individual distance in groups of eight fish and the turnovers of dopamine and serotonin in brains of fish from juvenile to the adult stage at 40-day intervals. We, firstly, found that shoal cohesion was overall consistent through ontogeny at group levels suggesting the presence of collective personality. Secondly, we found a decrease in shoal cohesion through ontogeny in the small-harvested and control lines, while the large-harvested line did not show any ontogenetic change. Thirdly, the selection lines did not differ among each other in shoal cohesion at any ontogenetic stage. Fourthly, dopamine turnover increased through ontogeny in a similar way for all lines while the serotonin turnover decreased in the large-harvested and control lines, but not in the small-harvested line. The large-harvested line also had higher serotonin turnover than controls at specific time periods. In conclusion, intensive size-selective mortality left an evolutionary legacy of asymmetric selection responses in the ontogeny of shoal cohesion and the underlying physiological mechanisms in experimentally harvested zebrafish in the laboratory. Significant statement The evolution of animal behavior can be affected by human activities both at behavioral and physiological levels, but causal evidence is scarce and mostly focusing on single life-stages. We studied whether and to what extent size-selective harvesting, a common selection pattern in fisheries, can be an evolutionary driver of the development of shoal cohesion during ontogeny. We used a multi-generation experiment with zebrafish to study cause-and-effects of opposing size-selection patterns. We quantified shoal cohesion, and serotonin and dopamine turnover in the brain. We found that shoal cohesion emerged as a collective personality trait and that behavioral and physiological responses were asymmetrical with respect to the opposing selection patterns.

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Section: Discussionsupporting

confidence: 87%

Evolutionary implications of size-selective mortality on the ontogenetic development of shoal cohesion: a neurochemical approach using a zebrafish, Danio rerio, harvest selection experiment

Sbragaglia

Roy

Thörnqvist

et al. 2022

Behav Ecol Sociobiol

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“…This offers support for our results and indicates that stopping selection might not have hampered feeding behaviour. That said, it is possible that the observed variations among selection lines are due to other factors like density (Bouffet‐Halle et al 2021 ; Crespel et al 2021a , b ) and genetic drift (Therkildsen et al 2019 ). A recent study in medaka showed that life-history divergence may not be caused by direct harvest selection but by natural density-dependent selection for a larger body-size (Bouffet‐Halle et al 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Size-selective mortality fosters ontogenetic changes in collective risk-taking behaviour in zebrafish, Danio rerio

Roy

Arlinghaus

2022

Oecologia

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Size-selective mortality is common in fish populations and can operate either in a positive size-selective fashion by harvesting larger-than-average fish or be negatively size-selective by harvesting smaller-than-average fish. Through various mechanisms (like genetic correlations among behaviour and life-history traits or direct selection on behaviour co-varying with growth rate or size-at-maturation), size-selection can result in evolutionary changes in behavioural traits. Theory suggests that both positive and negative size-selection without additional selection on behaviour favours boldness, while evolution of shyness is possible if the largest fish are harvested. Here we examined the impact of size-selective mortality on collective boldness across ontogeny using three experimental lines of zebrafish (Daniorerio) generated through positive (large-harvested), negative (small-harvested) and random (control line) size-selective mortality for five generations and then relaxed selection for 10 generations to examine evolutionarily fixed outcomes. We measured collective risk-taking during feeding (boldness) under simulated aerial predation threat, and across four contexts in presence/absence of a cichlid. Boldness decreased across ontogeny under aerial predation threat, and the small-harvested line was consistently bolder than controls. The large and small-harvested lines showed higher behavioural plasticity as larvae and developed personality earlier compared to the controls. The large-harvested line showed increased variability and plasticity in boldness throughout ontogeny. In the presence of a live predator, fish did not differ in boldness in three contexts compared to the controls, but the large-harvested line showed reduced behavioural plasticity across contexts than controls. Our results confirmed theory by demonstrating that size-selective harvesting evolutionarily alters collective boldness and its variability and plasticity.

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“…The rate of evolution in an exploited population depends on the size groups that are removed by fishing, which are ultimately determined by the size selectivity of gears and the intensity of harvest (Therkildsen et al, 2019;Crespel et al, 2021). In order to control the negative effects of FIE, low fishing mortalities have been suggested as a general remedy (Heino, 1998;Law, 2000;Laugen et al, 2014).…”

Section: Management Implications For Japanese Spanish Mackerel In Res...mentioning

confidence: 99%

The Effects of Selective Harvest on Japanese Spanish Mackerel (Scomberomorus niphonius) Phenotypic Evolution

et al. 2022

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Japanese Spanish mackerel (Scomberomorus niphonius) is an important fish species in the China Seas with wide distribution, extensive migration, and high economic value. This species has been yielding high fisheries production despite experiencing continuously high fishing pressure and the conversion from gillnet to trawl harvesting. Meanwhile, changes in life-history traits have been observed, including earlier maturation and smaller size at age. Here, we build an individual-based eco-genetic model parameterized for Japanese Spanish mackerel to investigate the population’s response to different fishing scenarios (fishing by trawl or by gillnet). The model allows evolution of life-history processes including maturation, reproduction and growth. It also incorporates environmental variability, phenotypic plasticity, and density-dependent feedbacks. Our results show that different gear types can result in different responses of life-history traits and altered population dynamics. The population harvested by gillnet shows weaker response to fishing than that by trawl. When fishing ceases, gillnet-harvested population can recover to the pre-harvest level more easily than that harvested by trawl. The different responses of population growth rate and evolution to different fishing gears demonstrated in this study shed light on the sustainable management and utilization of Japanese Spanish mackerel in the over-exploited China Seas.

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Genomic basis of fishing-associated selection varies with population density

Cited by 17 publications

References 67 publications

Evolutionary implications of size-selective mortality on the ontogenetic development of shoal cohesion: a neurochemical approach using a zebrafish, Danio rerio, harvest selection experiment

Evolutionary implications of size-selective mortality on the ontogenetic development of shoal cohesion: a neurochemical approach using a zebrafish, Danio rerio, harvest selection experiment

Size-selective mortality fosters ontogenetic changes in collective risk-taking behaviour in zebrafish, Danio rerio

The Effects of Selective Harvest on Japanese Spanish Mackerel (Scomberomorus niphonius) Phenotypic Evolution

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