Size-selective harvesting drives genomic shifts in a harvested population.

Overfishing not only drastically reduces the number of fish in an exploited population but is also often selective for body size by removing the largest individuals from a population. Here, we study experimentally the evolutionary effects of size-selective harvesting using whole-genome sequencing on a model organism, the zebrafish (Danio rerio). We demonstrate genomic shifts in the populations exposed to size-selective harvesting for five generations and show reduced genetic diversity in all harvested lines, including the control line (non-size-selected). We also determine differences in groups of genes related to certain gene ontology annotations between size-selectively harvested lines, with enrichment in nervous system related genes in the large-selected lines. Our results illuminate the biological processes underlying fisheries-induced genetic changes and hence contribute toward the understanding of the changes potentially associated with the vulnerability of an exploited population to future stressors.

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

The role of sexual selection in the context of harvest-induced evolution is poorly understood. However, elevated and trait-selective harvesting of wild populations may change sexually selected traits, which in turn can affect mate choice and reproduction. We experimentally evaluated the potential for fisheries-induced evolution of mating behaviour and reproductive allocation in fish. We used an experimental system of zebrafish (Danio rerio) lines exposed to large, small or random (i.e. control) size-selective mortality. The large-harvested line represented a treatment simulating the typical case in fisheries where the largest individuals are preferentially harvested. We used a full factorial design of spawning trials with size-matched individuals to control for the systematic impact of body size during reproduction, thereby singling out possible changes in mating behaviour and reproductive allocation. Both small size-selective mortality and large size-selective mortality left a legacy on male mating behaviour by elevating intersexual aggression. However, there was no evidence for line-assortative reproductive allocation. Females of all lines preferentially allocated eggs to the generally less aggressive males of the random-harvested control line. Females of the large-harvested line showed enhanced reproductive performance, and males of the large-harvested line had the highest egg fertilization rate among all males. These findings can be explained as an evolutionary adaptation by which individuals of the large-harvested line display an enhanced reproductive performance early in life to offset the increased probability of adult mortality due to harvest. Our results suggest that the large-harvested line evolved behaviourally mediated reproductive adaptations that could increase the rate of recovery when populations adapted to high fishing pressure come into secondary contact with other populations.

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

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.

Altered trait variability in response to size-selective mortality.

Changes in trait variability owing to size-selective harvesting have received little attention in comparison with changes in mean trait values, perhaps because of the expectation that phenotypic variability should generally be eroded by directional selection typical for fishing and hunting. We show, however, that directional selection, in particular for large body size, leads to increased body-size variation in experimentally harvested zebrafish (Danio rerio) populations exposed to two alternative feeding environments: ad libitum and temporarily restricted food availability. Trait variation may influence population adaptivity, stability and resilience. Therefore, rather than exerting selection pressures that favour small individuals, our results stress the importance of protecting large ones, as they can harbour a great amount of variation within a population, to manage fish stocks sustainably.

Food-web complexity, consumer behavior, and diet specialism: impacts on ecosystem stability.

Ecological stability is a fundamental aspect of food web dynamics. In this study, we explore the factors influencing stability in complex ecological networks, characterizing it through biomass oscillations and species persistence. Using an Extended Niche model, we generate diverse food web structures and investigate the effects of intraspecific consumer interference, network size, connectance, and diet specialism on stability. Our findings reveal that intraspecific consumer interference plays a pivotal role in shaping stability. Higher interference results in stable dynamics, reducing oscillations and extinctions. Additionally, differences emerge between food webs comprised of invertebrate consumers and those of ectotherm vertebrates, with the latter showing higher oscillations. Network size and connectance also influence stability, where larger and more connected webs tend to exhibit reduced oscillations. Overall, our study sheds light on the complex interplay of factors affecting ecological stability in food webs. Understanding these dynamics is crucial for biodiversity conservation and ecosystem management. Supplementary Information: The online version contains supplementary material available at 10.1007/s12080-024-00580-w.

Directional selection, not the direction of selection, affects telomere length and copy number at ribosomal RNA loci.

Many fisheries exert directional selection on traits such as body size and growth rate. Whether directional selection impacts regions of the genome associated with traits related to growth is unknown. To address this issue, we characterised copy number variation in three regions of the genome associated with cell division, (1) telomeric DNA, (2) loci transcribed as ribosomal RNA (rDNA), and (3) mitochondrial DNA (mtDNA), in three selection lines of zebrafish reared at three temperatures (22 °C, 28 °C, and 34 °C). Selection lines differed in (1) the direction of selection (two lines experienced directional selection for large or small body size) and (2) whether they experienced any directional selection itself. Lines that had experienced directional selection were smaller, had lower growth rate, shorter telomeres, and lower rDNA copy number than the line that experiencing no directional selection. Neither telomere length nor rDNA copy number were affected by temperature. In contrast, mtDNA content increased at elevated temperature but did not differ among selection lines. Though directional selection impacts rDNA and telomere length, direction of such selection did not matter, whereas mtDNA acts as a stress marker for temperature. Future work should examine the consequences of these genomic changes in natural fish stocks.

Gut Microbiota Profiling as a Promising Tool to Detect Equine Inflammatory Bowel Disease (IBD).

Gastrointestinal disorders are common and debilitating in horses, but their diagnosis is often difficult and invasive. Fecal samples offer a non-invasive alternative to assessing the gastrointestinal health of horses by providing information about the gut microbiota and inflammation. In this study, we used 16S sequencing to compare the fecal bacterial diversity and composition of 27 healthy horses and 49 horses diagnosed with inflammatory bowel disease (IBD). We also measured fecal calprotectin concentration, a marker of intestinal inflammation, in healthy horses and horses with IBD. We found that microbiota composition differed between healthy horses and horses with IBD, although less than five percent of the variation in microbiota composition was explained by individual health status and age. Several differentially abundant bacterial taxa associated with IBD, age, or body condition were depleted from the most dominant Firmicutes phylum and enriched with the Bacteroidota phylum. An artificial neural network model predicted the probability of IBD among the test samples with 100% accuracy. Our study is the first to demonstrate the association between gut microbiota composition and chronic forms of IBD in horses and highlights the potential of using fecal samples as a non-invasive source of biomarkers for equine IBD.

Fish with slow life-history cope better with chronic manganese exposure than fish with fast life-history.

Animals with different life-history types vary in their stress-coping styles, which can affect their fitness and survival in changing environments. We studied how chronic exposure to manganese sulfate (MnSO4), a common aquatic pollutant, affects life-history traits, physiology, and behavior of zebrafish (Danio rerio) with two life-history types: fast (previously selected for fast juvenile growth, early maturation, and small adult body size) and slow life histories (selected for slow juvenile growth, late maturation, and large adult body size). We found that MnSO4 had negative effects on growth and condition factors, but the magnitude of these effects depended on the life-history type. Individuals with fast life histories were more susceptible to MnSO4 than fish with slow life histories as they had lower growth rate, condition factor and feeding probability in high MnSO4 concentrations. Our results demonstrate that MnSO4 can impair fish performance, and life-history variation can modulate the stress-coping ability of individuals.

Does size-selective harvesting erode adaptive potential to thermal stress?

Overharvesting is a serious threat to many fish populations. High mortality and directional selection on body size can cause evolutionary change in exploited populations via selection for a specific phenotype and a potential reduction in phenotypic diversity. Whether the loss of phenotypic diversity that accompanies directional selection impairs response to environmental stress is not known. To address this question, we exposed three zebrafish selection lines to thermal stress. Two lines had experienced directional selection for (1) large and (2) small body size, and one was (3) subject to random removal of individuals with respect to body size (i.e. line with no directional selection). Selection lines were exposed to three temperatures (elevated, 34°C; ambient, 28°C; low, 22°C) to determine the response to an environmental stressor (thermal stress). We assessed differences among selection lines in their life history (growth and reproduction), physiological traits (metabolic rate and critical thermal max) and behaviour (activity and feeding behaviour) when reared at different temperatures. Lines experiencing directional selection (i.e. size selected) showed reduced growth rate and a shift in average phenotype in response to lower or elevated thermal stress compared with fish from the random-selected line. Our data indicate that populations exposed to directional selection can have a more limited capacity to respond to thermal stress compared with fish that experience a comparable reduction in population size (but without directional selection). Future studies should aim to understand the impacts of environmental stressors on natural fish stocks.

Chemical composition and particle size influence the toxicity of nanoscale plastic debris and their co-occurring benzo(α)pyrene in the model aquatic organisms Daphnia magna and Danio rerio.

Little is known about how particle chemical composition and size might influence the toxicity of nanoscale plastic debris (NPD) and their co-occurring chemicals. Herein, we investigate the toxicity of 3 × 1010 particles/L polyethylene (PE, 50 nm), polypropylene (PP, 50 nm), polystyrene (PS, 200 and 600 nm), and polyvinyl chloride (PVC, 200 nm) NPD and their co-occurring benzo(a)pyrene (BaP) to Daphnia magna and Danio rerio. During the 21 days of exposure to PE 50 nm and PS 200 nm, the number of broods produced by D. magna decreased compared to other treatments. Exposure to BaP alone did not produce any effects on the reproduction of the daphnids, however, the mixture of BaP with PS (200 or 600 nm) or with PE (50 nm) reduced the number of broods. Exposure of D. rerio embryos to PE 50 nm, PS 200 nm, and PS 600 nm led to a delay in the hatching. The presence of PS 200 nm and PVC 200 nm eliminated the effects of BaP on the hatching rate of zebrafish. Our findings suggest that data generated for the toxicity of one type of NPD, e.g. PVC or PS may not be extrapolated to other types of NPD.

Population genomics of wild and laboratory zebrafish (Danio rerio).

Understanding a wider range of genotype-phenotype associations can be achieved through ecological and evolutionary studies of traditional laboratory models. Here, we conducted the first large-scale geographic analysis of genetic variation within and among wild zebrafish (Danio rerio) populations occurring in Nepal, India, and Bangladesh, and we genetically compared wild populations to several commonly used lab strains. We examined genetic variation at 1832 polymorphic EST-based single nucleotide polymorphisms (SNPs) and the cytb mitochondrial gene in 13 wild populations and three lab strains. Natural populations were subdivided into three major mitochondrial DNA clades with an average among-clade sequence divergence of 5.8%. SNPs revealed five major evolutionarily and genetically distinct groups with an overall FST of 0.170 (95% CI 0.105-0.254). These genetic groups corresponded to discrete geographic regions and appear to reflect isolation in refugia during past climate cycles. We detected 71 significantly divergent outlier loci (3.4%) and nine loci (0.5%) with significantly low FST values. Valleys of reduced heterozygosity, consistent with selective sweeps, surrounded six of the 71 outliers (8.5%). The lab strains formed two additional groups that were genetically distinct from all wild populations. An additional subset of outlier loci was consistent with domestication selection within lab strains. Substantial genetic variation that exists in zebrafish as a whole is missing from lab strains that we analysed. A combination of laboratory and field studies that incorporates genetic variation from divergent wild populations along with the wealth of molecular information available for this model organism provides an opportunity to advance our understanding of genetic influences on phenotypic variation for a vertebrate species.

Age is not just a number-Mathematical model suggests senescence affects how fish populations respond to different fishing regimes.

Senescence is often described as an age-dependent increase in natural mortality (known as actuarial senescence) and an age-dependent decrease in fecundity (known as reproductive senescence), and its role in nature is still poorly understood. Based on empirical estimates of reproductive and actuarial senescence, we used mathematical simulations to explore how senescence affects the population dynamics of Coregonus albula, a small, schooling salmonid fish. Using an empirically based eco-evolutionary model, we investigated how the presence or absence of senescence affects the eco-evolutionary dynamics of a fish population during pristine, intensive harvest, and recovery phases. Our simulation results showed that the presence or absence of senescence affected how the population responded to the selection regime. At an individual level, gillnetting caused a larger decline in asymptotic length when senescence was present, compared to the nonsenescent population, and the opposite occurred when fishing was done by trawling. This change was accompanied by evolution toward younger age at maturity. At the population level, the change in biomass and number of fish in response to different fishery size-selection patterns depended on the presence or absence of senescence. Since most life-history and fisheries models ignore senescence, they may be over-estimating reproductive capacity and under-estimating natural mortality. Our results highlight the need to understand the combined effects of life-history characters such as senescence and fisheries selection regime to ensure the successful management of our natural resources.

Implications of size-selective fisheries on sexual selection.

Fisheries often combine high mortality with intensive size selectivity and can, thus, be expected to reduce body size and size variability in exploited populations. In many fish species, body size is a sexually selected trait and plays an important role in mate choice and mate competition. Large individuals are often preferred as mates due to the high fecundity and resources they can provide to developing offspring. Large fish are also successful in competition for mates. Fisheries-induced reductions in size and size variability can potentially disrupt mating systems and lower average reproductive success by decreasing opportunities for sexual selection. By reducing population sizes, fisheries can also lead to an increased level of inbreeding. Some fish species avoid reproducing with kin, and a high level of relatedness in a population can further disrupt mating systems. Reduced body size and size variability can force fish to change their mate preferences or reduce their choosiness. If mate preference is genetically determined, the adaptive response to fisheries-induced changes in size and size variability might not occur rapidly. However, much evidence exists for plastic adjustments of mate choice, suggesting that fish might respond flexibly to changes in their social environment. Here, I first discuss how reduced average body size and size variability in exploited populations might affect mate choice and mate competition. I then consider the effects of sex-biased fisheries on mating systems. Finally, I contemplate the possible effects of inbreeding on mate choice and reproductive success and discuss how mate choice might evolve in exploited populations. Currently, little is known about the mating systems of nonmodel species and about the interplay between size-selective fisheries and sexual selection. Future studies should focus on how reduced size and size variability and increased inbreeding affect fish mating systems, how persistent these effects are, and how this might in turn affect population demography.

Association Mapping Based on a Common-Garden Migration Experiment Reveals Candidate Genes for Migration Tendency in Brown Trout.

A better understanding of the environmental and genetic contribution to migratory behavior and the evolution of traits linked to migration is crucial for fish conservation and fisheries management. Up to date, a few genes with unequivocal influence on the adoption of alternative migration strategies have been identified in salmonids. Here, we used a common garden set-up to measure individual migration distances of generally highly polymorphic brown trout Salmo trutta from two populations. Fish from the assumedly resident population showed clearly shorter migration distances than the fish from the assumed migratory population at the ages of 2 and 3 years. By using two alternative analytical pipelines with 22186 and 18264 SNPs obtained through RAD-sequencing, we searched for associations between individual migration distance, and both called genotypes and genotype probabilities. None of the SNPs showed statistically significant individual effects on migration after correction for multiple testing. By choosing a less stringent threshold, defined as an overlap of the top 0.1% SNPs identified by the analytical pipelines, GAPIT and Angsd, we identified eight candidate genes that are potentially linked to individual migration distance. While our results demonstrate large individual and population level differences in migration distances, the detected genetic associations were weak suggesting that migration traits likely have multigenic control.

Comparing RADseq and microsatellites for estimating genetic diversity and relatedness - Implications for brown trout conservation.

The conservation and management of endangered species requires information on their genetic diversity, relatedness and population structure. The main genetic markers applied for these questions are microsatellites and single nucleotide polymorphisms (SNPs), the latter of which remain the more resource demanding approach in most cases. Here, we compare the performance of two approaches, SNPs obtained by restriction-site-associated DNA sequencing (RADseq) and 16 DNA microsatellite loci, for estimating genetic diversity, relatedness and genetic differentiation of three, small, geographically close wild brown trout (Salmo trutta) populations and a regionally used hatchery strain. The genetic differentiation, quantified as F ST, was similar when measured using 16 microsatellites and 4,876 SNPs. Based on both marker types, each brown trout population represented a distinct gene pool with a low level of interbreeding. Analysis of SNPs identified half- and full-siblings with a higher probability than the analysis based on microsatellites, and SNPs outperformed microsatellites in estimating individual-level multilocus heterozygosity. Overall, the results indicated that moderately polymorphic microsatellites and SNPs from RADseq agreed on estimates of population genetic structure in moderately diverged, small populations, but RADseq outperformed microsatellites for applications that required individual-level genotype information, such as quantifying relatedness and individual-level heterozygosity. The results can be applied to other small populations with low or moderate levels of genetic diversity.

Species' ecological functionality alters the outcome of fish stocking success predicted by a food-web model.

Fish stocking is used worldwide in conservation and management, but its effects on food-web dynamics and ecosystem stability are poorly known. To better understand these effects and predict the outcomes of stocking, we used an empirically validated network model of a well-studied lake ecosystem. We simulate two stocking scenarios with two native fish species valuable for fishing. In the first scenario, we stock planktivorous fish (whitefish) larvae in the ecosystem. This leads to a 1% increase in adult whitefish biomasses and decreases the biomasses of the top predator (perch). In the second scenario, we also stock perch larvae in the ecosystem. This decreases the planktivorous whitefish and the oldest top predator age class biomasses, and destabilizes the ecosystem. Our results demonstrate that the effects of stocking depend on the species' position in the food web and thus cannot be assessed without considering interacting species. We further show that stocking can lead to undesired outcomes from both management and conservation perspectives. The gains of stocking can remain minor and have adverse effects on the entire ecosystem.

Comparison of Migratory and Resident Populations of Brown Trout Reveals Candidate Genes for Migration Tendency.

Candidate genes associated with migration have been identified in multiple taxa: including salmonids, many of whom perform migrations requiring a series of physiological changes associated with the freshwater-saltwater transition. We screened over 5,500 SNPs for signatures of selection related to migratory behavior of brown trout Salmo trutta by focusing on ten differentially migrating freshwater populations from two watersheds (the Koutajoki and the Oulujoki). We found eight outlier SNPs potentially associated with migratory versus resident life history using multiple (≥3) outlier detection approaches. Comparison of three migratory versus resident population pairs in the Koutajoki watershed revealed seven outlier SNPs, of which three mapped close to genes ZNF665-like, GRM4-like, and PCDH8-like that have been previously associated with migration and smoltification in salmonids. Two outlier SNPs mapped to genes involved in mucus secretion (ST3GAL1-like) and osmoregulation (C14orf37-like). The last two strongly supported outlier SNPs mapped to thermally induced genes (FNTA1-like, FAM134C-like). Within the Oulujoki, the only consistent outlier SNP mapped close to a gene (EZH2) that is associated with compensatory growth in fasted trout. Our results suggest that a relatively small yet common set of genes responsible for physiological functions associated with resident and migratory life histories is evolutionarily conserved.

The evolutionary legacy of size-selective harvesting extends from genes to populations.

Size-selective harvesting is assumed to alter life histories of exploited fish populations, thereby negatively affecting population productivity, recovery, and yield. However, demonstrating that fisheries-induced phenotypic changes in the wild are at least partly genetically determined has proved notoriously difficult. Moreover, the population-level consequences of fisheries-induced evolution are still being controversially discussed. Using an experimental approach, we found that five generations of size-selective harvesting altered the life histories and behavior, but not the metabolic rate, of wild-origin zebrafish (Danio rerio). Fish adapted to high positively size selective fishing pressure invested more in reproduction, reached a smaller adult body size, and were less explorative and bold. Phenotypic changes seemed subtle but were accompanied by genetic changes in functional loci. Thus, our results provided unambiguous evidence for rapid, harvest-induced phenotypic and evolutionary change when harvesting is intensive and size selective. According to a life-history model, the observed life-history changes elevated population growth rate in harvested conditions, but slowed population recovery under a simulated moratorium. Hence, the evolutionary legacy of size-selective harvesting includes populations that are productive under exploited conditions, but selectively disadvantaged to cope with natural selection pressures that often favor large body size.

Evolutionary impact assessment: accounting for evolutionary consequences of fishing in an ecosystem approach to fisheries management.

Managing fisheries resources to maintain healthy ecosystems is one of the main goals of the ecosystem approach to fisheries (EAF). While a number of international treaties call for the implementation of EAF, there are still gaps in the underlying methodology. One aspect that has received substantial scientific attention recently is fisheries-induced evolution (FIE). Increasing evidence indicates that intensive fishing has the potential to exert strong directional selection on life-history traits, behaviour, physiology, and morphology of exploited fish. Of particular concern is that reversing evolutionary responses to fishing can be much more difficult than reversing demographic or phenotypically plastic responses. Furthermore, like climate change, multiple agents cause FIE, with effects accumulating over time. Consequently, FIE may alter the utility derived from fish stocks, which in turn can modify the monetary value living aquatic resources provide to society. Quantifying and predicting the evolutionary effects of fishing is therefore important for both ecological and economic reasons. An important reason this is not happening is the lack of an appropriate assessment framework. We therefore describe the evolutionary impact assessment (EvoIA) as a structured approach for assessing the evolutionary consequences of fishing and evaluating the predicted evolutionary outcomes of alternative management options. EvoIA can contribute to EAF by clarifying how evolution may alter stock properties and ecological relations, support the precautionary approach to fisheries management by addressing a previously overlooked source of uncertainty and risk, and thus contribute to sustainable fisheries.