Fishery-induced Evolution Research Articles

Simulated reproductive allocation to fisheries-induced evolution among small yellow croaker populations in the Yellow and Bohai Seas

Fishery-induced evolution (FIE) affects the body size and reproduction of offspring, resulting in feedback regulation of fish survival and stock recruitment. Small yellow croaker (Larimichthys polyactis) is a species of high ecological and commercial importance in the Yellow and Bohai Seas, with large fluctuations in abundance linked to overfishing and environmental changes in recent decades. To better understand the maturation size and age, threshold reproduction cost, and energy trade-offs of small yellow croaker under environmental changes (e.g. conditions) and human impacts (e.g. fishing) in the Yellow and Bohai Seas, we utilised a two-pool uncertain growth model containing the growth threshold of reproductive energy and reproductive energy cost. The results showed that for growth, maturation age, and reproduction under the baseline scenario based on field survey data from the 1950 s, when resources for small yellow croaker were underexploited, the average age was 5–6 years old and the average body length was approximately 220 mm. As the model parameters for fishing pressure and condition mortality increased, small yellow croaker tended to mature earlier, had a smaller body size, and allocated more energy to reproduction, resulting in higher population fecundity but shorter lifespan. Higher reproductive costs led to a greater proportion of reproductive energy being allocated during the spawning period, resulting in an older age of sexual maturity, shorter lifespan for spawning populations, and poor physical conditions, resulting in higher post-reproductive mortality and a limited capacity for stock recruitment. The key life-history traits of small yellow croaker, including maturity age, mean age of the population, age-specific body weight, and spawn production at different age stages, can change under different conditions. The model represents the main life history strategies and energy allocation characteristics of small yellow croaker. The simulated age and body size were within the observed range and the predicted fecundity aligned with the observed values. This study provides a prediction tool for protecting the spawning and recruitment of small yellow croaker and establishes a biological reference for sustainable management of small yellow croaker populations in the Yellow and Bohai Seas in the future.

Reduction in size-at-maturity in unprecedentedly strong cohorts of redfish (Sebastes mentella and S. fasciatus) in the Gulf of St. Lawrence and Laurentian Channel.

Life-history traits, such as size-at-maturity, are key parameters to model population dynamics used to inform fisheries management. Fishery-induced evolution, density-dependent effects, and global warming have been shown to affect size- and age-at-maturity, and resulting spawning stock biomass (SSB) in a wide range of commercial fish stocks. Marked changes in redfish biomass and environmental conditions in the Gulf of St. Lawrence and Laurentian Channel over the past decade called for a review and update of size-at-maturity for commercially important deepwater redfish Sebastes mentella and Acadian redfish Sebastes fasciatus stocks. Following a 25-year moratorium, local redfish biomass has recently reached unprecedented levels, co-occurring with an overall warming of bottom water temperatures. Our objectives were (1) to perform a histological assessment of redfish reproduction stages, including the validation and fine-tuning of a robust visual chart to facilitate monitoring of size-at-maturity and SSB in a transforming environment, and (2) to evaluate changes in size-at-maturity in unprecedentedly strong cohorts of redfish, and consequences for stock status assessment and fisheries management. Each specimen was genetically identified to species, and gonad reproduction stages were determined by histology and macroscopic appearances. The present study enabled a robust visual chart for continued and cost-effective monitoring of redfish reproduction stages to be refined and validated, and has shown a large decrease in redfish length when 50% of the individuals are considered mature that led to an increase in estimates of SSB during the 2011-2021 period for S. mentella and S. fasciatus. These changes modified the perception of stock status, thus having significant implications for fisheries management. Given that fishery-induced evolution and community structure changes along with global warming are affecting numerous stocks worldwide, the present study outlines a major and global challenge for scientists and resources managers. As shown by our results, the monitoring and frequent updates of life-history traits in transforming environments are needed to provide reliable science advice for sustainable fisheries.

Decline in Size-at-Maturity of European Hake in Relation to Environmental Regimes: A Case in the Eastern Ionian Sea.

European hake, Merluccius merluccius L. 1758, is a highly valuable demersal fish species exploited in both the east Atlantic and the Mediterranean Sea. Changes in the size-at-maturity of this species have been reported in various geographic areas. Size-at-maturity is a key parameter in fishery management. Our main goal was to study the trend of the size-at-maturity of European hake in the eastern Ionian Sea (Central Mediterranean) over the last five decades. Utilizing a multi-decadal series of data for various environmental variables, we employed multivariate analyses and non-additive modeling in an attempt to identify shifts in the climatic environment of the eastern Ionian Sea and whether the maturation of the hake population could be affected by these changes. The analyses used suggest a plausible environmental regime shift in the study area in the late 1990s/early 2000s. The decrease in size-at-maturity that was detected in the last two decades may, thus, be associated with environmental changes. However, as many fish stocks already experience fishery-induced evolution, further investigation is necessary to determine whether this environmental effect is an additional stressor on a possibly already fishery-impacted population. The outcomes of this study highlight the importance of investigating the relationship between fish reproductive traits and altered environmental conditions, as the latter are generally ignored during assessments, affecting the robustness of fishery management.

Species Composition, Growth, and Trophic Traits of Hairtail (Trichiuridae), the Most Productive Fish in Chinese Marine Fishery.

Hairtail (Scombriformes: Trichiuridae) have always ranked first in single-species production in Chinese marine fishery. However, due to the confusion of species identification, in official statistics, data on hairtail production and economic value are a combination of all the different species of Trichiuridae. In this study, based on sampling along China's coastal areas, the composition and distribution of common hairtail species, as well as their age, growth, and trophic traits, are discussed. Six species of four genera and two subfamilies were identified, and largehead hairtail (Trichiurus japonicus) and Savalai hairtail (Lepturacanthus savala) were the most important populations that constituted catch production. The growth parameter b could be divided into two groups, with values in species mostly inhabiting northern parts of Chinese seas higher than those in southern parts. Most individuals were 1-2 years of age, suggesting species sexual precocity and individual miniaturization under multiple stresses. Species of Trichiuridae are at the top of the food web and play a bottom-up role in regulating the trophic dynamics of marine food webs. Largehead hairtail showed the highest stability and the greatest impact on the stability of the trophic structure. Despite temporary resource maintenance under fishery-induced evolution, the effective recovery and reasonable utilization of hairtail resources are still the main focuses of attention for Chinese marine fishery.

Reproductive environment of the decreasing Indian river shad in Asian inland waters: disentangling the climate change and indiscriminative fishing threats.

The regional climate has significantly warmed with erratically declining annual rainfall and intensified downpour within a narrower span of monsoon months, which led to an increased trophic state (≈algae) in most inland waters. Freshwater clupeids vitally control the aquatic food chain by grazing on algae. Despite increasing food availability, IUCN Red List® revealed 16 freshwater clupeids with a decreasing population trend. We investigated one such species' reproductive dependencies, Gudusia chapra (Indian river shad), in the lower Gangetic drainage (India) under a mixed context of climate change and overfishing. Monthly rainfall (≥ 60-100 mm) and water temperature (≥ 31-32 °C) are key breeding cues for females. The regional climate seems inclined to fulfill these through the significant part of the breeding season, and indeed the species has maintained consistent breeding phenology over 20 years. Other breeding thresholds relevant to fishing include size at first maturity (≥ 6.8 cm; reduced by ~ 25-36%) and pre-spawning girth (Girthspawn50 ≥ 7 cm; first record). Girthspawn50 is a proxy of the minimum mesh size requirement of fishing nets to allow safe passage of "gravid" females (+ 22% bulged abdomen) and breed. The operational fishing nets (3-10 cm mesh) probably have been indulged in indiscriminative fishing of gravid females for generations. Under a favorably changing climate and food availability, existing evidence suggests a fishery-induced evolution in regional females (to circumvent such mesh sizes) through earlier maturation/puberty at smaller sizes. It could be an early warning sign of population collapse (smaller females → lessening fecundity → fewer offspring). Overfishing seemed to be a bigger threat than climate change.

Fisheries-induced selection against schooling behaviour in marine fishes.

Group living is a common strategy used by fishes to improve their fitness. While sociality is associated with many benefits in natural environments, including predator avoidance, this behaviour may be maladaptive in the Anthropocene. Humans have become the dominant predator in many marine systems, with modern fishing gear developed to specifically target groups of schooling species. Therefore, ironically, behavioural strategies which evolved to avoid non-human predators may now actually make certain fish more vulnerable to predation by humans. Here, we use an individual-based model to explore the evolution of fish schooling behaviour in a range of environments, including natural and human-dominated predation conditions. In our model, individual fish may leave or join groups depending on their group-size preferences, but their experienced group size is also a function of the preferences of others in the population. Our model predicts that industrial fishing selects against individual-level behaviours that produce large groups. However, the relationship between fishing pressure and sociality is nonlinear, and we observe discontinuities and hysteresis as fishing pressure is increased or decreased. Our results suggest that industrial fishing practices could be altering fishes' tendency to school, and that social behaviour should be added to the list of traits subject to fishery-induced evolution.

Could we consider a single stock when spatial sub-units present lasting patterns in growth and asynchrony in cohort densities? A flatfish case study

An accurate representation of the spatial structure of marine fish populations is a prerequisite for unbiased stock assessment, to build appropriate management measures. The common sole (Solea solea, L.) of the Eastern English Channel (EEC) is a commercial flatfish species, whose stock is currently assessed as a single homogeneous population and has been overexploited over the last decade. Previous studies have highlighted the stock's low connectivity and the lack of understanding in sub-adults and adults mixing between putative subunits, raising the issue of a potential spatial structure of this stock. Here, we examined evidence of spatial structure by analyzing spatiotemporal patterns of length and density-at-age using time series (1989–2015) obtained from a scientific survey (UK-BTS). We tested for various hypotheses of spatial structure, based on both scientific and expert knowledge, including three isolated subunits, their combination, and no spatial structure. We combined two sets of analyses: (1) a selection of the von Bertalanffy growth model with spatial effects capturing the most accurate spatial structure of the stock and the analysis of long-term spatial patterns (gradients, trends, synchrony) in growth parameters; and (2) an analysis of the synchrony among density-at-age time series between spatial subunits. Growth analysis revealed a spatial structure in three subunits (i.e. the southwestern, northeastern and English parts of the EEC) and an overall decline of length-at-age, suggesting Fishery-Induced Evolution. The synchrony analysis revealed high spatiotemporal integrity at the level of the southwestern subunit of the EEC. Our two analyses thus detected a lasting signal of spatial stock structure with a probable isolation of the southwestern subunit from the rest of the EEC. Future research should build on our study by investigating the connectivity of sole throughout its entire life cycle, to improve stock assessment and fishery management.

Fishery‐induced evolution provides insights into adaptive responses of marine species to climate change

Climate change challenges marine species with seawater that is warmer, with less oxygen and lowerpH. To date, most climate‐change studies have focused on organisms' acclimation or shifts in distribution; relatively little is known about the capacity of marine species to respond through evolution. We propose that important insights can be gained from recent studies of fishery‐induced evolution (FIE), which show that increased adult mortality from fishing leads to rapid changes in growth and reproduction schedules. These changes consistently involve evolution of “faster” life histories: earlier maturation at smaller sizes and shorter life spans. In the ocean, coupled effects of higher temperatures and reduced oxygen also differentially affect larger or older individuals, so expected evolutionary consequences of climate change are qualitatively similar to those ofFIE. This general pattern will apply to large numbers of marine species and has important implications for conservation and management.

Harvest-induced evolution and effective population size.

Much has been written about fishery‐induced evolution (FIE) in exploited species, but relatively little attention has been paid to the consequences for one of the most important parameters in evolutionary biology—effective population size (N e). We use a combination of simulations of Atlantic cod populations experiencing harvest, artificial manipulation of cod life tables, and analytical methods to explore how adding harvest to natural mortality affects N e, census size (N), and the ratio N e/N. We show that harvest‐mediated reductions in N e are due entirely to reductions in recruitment, because increasing adult mortality actually increases the N e/N ratio. This means that proportional reductions in abundance caused by harvest represent an upper limit to the proportional reductions in N e, and that in some cases N e can even increase with increased harvest. This result is a quite general consequence of increased adult mortality and does not depend on harvest selectivity or FIE, although both of these influence the results in a quantitative way. In scenarios that allowed evolution, N e recovered quickly after harvest ended and remained higher than in the preharvest population for well over a century, which indicates that evolution can help provide a long‐term buffer against loss of genetic variability.

The fittest fish escape trawling

![Graphic][1] Humans have used trawling nets to catch fish for hundreds of years, making us one of the most effective predators for certain fish species. It is well known that we can shape characteristics of fish populations through ‘fishery-induced evolution’, where we catch the most

Circulating levels of plasma IGF-I during recovery from size-selective harvesting in Menidia menidia

Selection for growth-related traits in domesticated fishes often results in predictable changes within the growth hormone-insulin-like growth factor (GH-IGF-1) axis. Little is known about the mechanisms controlling changes in growth capacity resulting from fishery-induced evolution. We took advantage of a long-term study where Menidia menidia were selected for size at age over multiple generations to mimic fisheries-induced selection. This selection regime produced three populations with significant differences in intrinsic growth rate. These growth differences partially rebounded, but persisted even after selection was relaxed, resulting in fast, intermediate, and slow-growing lines. Plasma IGF-1 was measured in these populations as a potential target of selection on growth. IGF-1 was significantly correlated with current length and mass, and was positively correlated with growth rate (g d−1) in two lines, indicating it may be an appropriate indicator of growth capacity. The slow-growing line exhibited higher overall IGF-1 levels relative to the depressed IGF-1 seen in the fast-growing line, contrary to our prediction. We offer possible explanations for this unusual pattern and argue that somatic growth is likely to be under control of mechanism(s) downstream to IGF-1. IGF-1 provides an interesting basis for understanding endocrine control of growth in response to artificial selection and recovery.

The response of correlated traits following cessation of fishery‐induced selection

The application of evolutionary principles to the management of fisheries has gained considerable attention recently. Harvesting of fish may apply directional or disruptive selection to key life-history traits, and evidence for fishery-induced evolution is growing. The traits that are directly selected upon are often correlated (genetically or phenotypically) with a suite of interrelated physiological, behavioral, and morphological characters. A question that has received comparatively little attention is whether or not, after cessation of fishery-induced selection, these correlated traits revert back to previous states. Here, we empirically examine this question. In experiments with the Atlantic silverside, Menidia menidia, we applied size-selective culling for five generations and then maintained the lines a further five generations under random harvesting. We found that some traits do return to preharvesting levels (e.g., larval viability), some partially recover (e.g., egg volume, size-at-hatch), and others show no sign of change (e.g., food consumption rate, vertebral number). Such correlations among characters could, in theory, greatly accelerate or decelerate the recovery of fish populations. These results may explain why some fish stocks fail to recover after fishing pressure is relaxed.

Genetic correlations between adults and larvae in a marine fish: potential effects of fishery selection on population replenishment.

Correlated genetic responses have been hypothesized as important components of fishery-induced evolution, although predictive data from wild populations have been difficult to obtain. Here, we demonstrate substantial genetic correlations between a trait often subjected to fishery selection (adult body length) and traits that affect survival of larvae (length and swimming performance) in a wild population of a marine fish (bicolor damselfish, Stegastes partitus). Through both genetic covariance and size-dependent maternal effects, selection on adult size may cause a considerable, correlated response in larval traits. To quantify how variation in larval traits may affect survival, we introduce a flexible method that uses information from selection measurements to account for frequency dependence and estimate the relationship between phenotype and relative survival across a broad range of phenotypic values. Using this method, we synthesize studies of selective mortality on larval size for eight species of fish and show that variation in larval size may result in considerable variation in larval survival. We predict that observed rates of fishery selection on adult marine fishes may substantially reduce larval size and survival. The evolution of smaller larvae in response to fishery selection may therefore have substantial consequences for the viability of fished populations.

EDITORIAL: Toward Darwinian fisheries management

There is increasing evidence that fishing may cause rapid contemporary evolution in freshwater and marine fish populations. This has led to growing concern about the possible consequences such evolutionary change might have for aquatic ecosystems and the utility of those ecosystems to society. This special issue contains contributions from a symposium on fisheries-induced evolution held at the American Fisheries Society Annual Meeting in August 2008. Contributions include primary studies and reviews of field-based and experimental evidence, and several theoretical modeling studies advancing life-history theory and investigating potential management options. In this introduction we review the state of research in the field, discuss current controversies, and identify contributions made by the papers in this issue to the knowledge of fisheries-induced evolution. We end by suggesting directions for future research.

The role of experiments in understanding fishery-induced evolution.

Evidence of fishery-induced evolution has been accumulating rapidly from various avenues of investigation. Here we review the knowledge gained from experimental approaches. The strength of experiments is in their ability to disentangle genetic from environmental differences. Common garden experiments have provided direct evidence of adaptive divergence in the wild and therefore the evolvability of various traits that influence production in numerous species. Most of these cases involve countergradient variation in physiological, life history, and behavioral traits. Selection experiments have provided examples of rapid life history evolution and, more importantly, that fishery-induced selection pressures cause simultaneous divergence of not one but a cluster of genetically and phenotypically correlated traits that include physiology, behavior, reproduction, and other life history characters. The drawbacks of experiments are uncertainties in the scale-up from small, simple environments to larger and more complex systems; the concern that taxons with short life cycles used for experimental research are atypical of those of harvested species; and the difficulty of adequately simulating selection due to fishing. Despite these limitations, experiments have contributed greatly to our understanding of fishery-induced evolution on both empirical and theoretical levels. Future advances will depend on integrating knowledge from experiments with those from modeling, field studies, and molecular genetic approaches.

Fishery-induced selection on an Alpine whitefish: quantifying genetic and environmental effects on individual growth rate.

Size-selective fishing, environmental changes and reproductive strategies are expected to affect life-history traits such as the individual growth rate. The relative contribution of these factors is not clear, particularly whether size-selective fishing can have a substantial impact on the genetics and hence on the evolution of individual growth rates in wild populations. We analysed a 25-year monitoring survey of an isolated population of the Alpine whitefish Coregonus palaea. We determined the selection differentials on growth rate, the actual change of growth rate over time and indicators of reproductive strategies that may potentially change over time. The selection differential can be reliably estimated in our study population because almost all the fish are harvested within their first years of life, i.e. few fish escape fishing mortality. We found a marked decline in average adult growth rate over the 25 years and a significant selection differential for adult growth, but no evidence for any linear change in reproductive strategies over time. Assuming that the heritability of growth in this whitefish corresponds to what was found in other salmonids, about a third of the observed decline in growth rate would be linked to fishery-induced evolution. Size-selective fishing seems to affect substantially the genetics of individual growth in our study population.

Increase in maturation size after the closure of a high seas gillnet fishery on hatchery-reared chum salmon Oncorhynchus keta.

Gillnet fisheries are strongly size-selective and seem to produce changes in size at maturity for exploited fishes. After Word War II, large-scale gillnet fisheries targeted Pacific salmon (Oncorhynchus spp.) in the high seas area of the North Pacific and the Bering Sea, but these fisheries were closed in 1993. To assess the effects of this high seas gillnet fishery (and its closing) on size at maturity, we examined long-term trends in size at 50% probability of maturing (L50) for chum salmon (O. keta) from three populations in Hokkaido, Japan. The L50 trends were statistically different among rivers, but showed similar temporal patterns with decreases in the 1970s and early 1980s and increases after the 1985 brood year. While fishery-induced evolution seemed largely responsible for this temporal change in L50 during the fishing period, natural selection and phenotypic plasticity induced by environmental changes could contribute to the increases in L50 after the relaxation of fishing pressure.

Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations

The possibility for fishery-induced evolution of life history traits is an important but unresolved issue for exploited fish populations. Because fisheries tend to select and remove the largest individuals, there is the evolutionary potential for lasting effects on fish production and productivity. Size selection represents an indirect mechanism of selection against rapid growth rate, because individual fish may be large because of rapid growth or because of slow growth but old age. The possibility for direct selection on growth rate, whereby fast-growing genotypes are more vulnerable to fishing irrespective of their size, is unexplored. In this scenario, faster-growing genotypes may be more vulnerable to fishing because of greater appetite and correspondingly greater feeding-related activity rates and boldness that could increase encounter with fishing gear and vulnerability to it. In a realistic whole-lake experiment, we show that fast-growing fish genotypes are harvested at three times the rate of the slow-growing genotypes within two replicate lake populations. Overall, 50% of fast-growing individuals were harvested compared with 30% of slow-growing individuals, independent of body size. Greater harvest of fast-growing genotypes was attributable to their greater behavioral vulnerability, being more active and bold. Given that growth is heritable in fishes, we speculate that evolution of slower growth rates attributable to behavioral vulnerability may be widespread in harvested fish populations. Our results indicate that commonly used minimum size-limits will not prevent overexploitation of fast-growing genotypes and individuals because of size-independent growth-rate selection by fishing.