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.     

Maladaptive changes in multiple traits caused by fishing: impediments to population recovery

Some overharvested fish populations fail to recover even after considerable reductions in fishing pressure. The reasons are unclear but may involve genetic changes in life history traits that are detrimental to population growth when natural environmental factors prevail. We empirically modelled this process by subjecting populations of a harvested marine fish, the Atlantic silverside, to experimental size-biased fishing regimes over five generations and then measured correlated responses across multiple traits. Populations where large fish were selectively harvested (as in most fisheries) displayed substantial declines in fecundity, egg volume, larval size at hatch, larval viability, larval growth rates, food consumption rate and conversion efficiency, vertebral number, and willingness to forage. These genetically based changes in numerous traits generally reduce the capacity for population recovery.     

Evolutionary response to size-selective mortality in an exploited fish population

Many collapsed fish populations have failed to recover after a decade or more with little fishing. This may reflect evolutionary change in response to the highly selective mortality imposed by fisheries. Recent experimental work has demonstrated a rapid genetic change in growth rate in response to size-selective harvesting of laboratory fish populations. Here, we use a 30-year time-series of back-calculated lengths-at-age to test for a genetic response to size-selective mortality in the wild in a heavily exploited population of Atlantic cod (Gadus morhua). Controlling for the effects of density- and temperature-dependent growth, the change in mean length of 4-year-old cod between offspring and their parental cohorts was positively correlated with the estimated selection differential experienced by the parental cohorts between this age and spawning. This result supports the hypothesis that there have been genetic changes in growth in this population in response to size-selective fishing. Such changes may account for the continued small size-at-age in this population despite good conditions for growth and little fishing for over a decade. This study highlights the need for management regimes that take into account the evolutionary consequences of fishing.     

Size‐selective fishing affects sex ratios and the opportunity for sexual selection in Alaskan sockeye salmon Oncorhynchus nerka

Selective exploitation can cause adverse ecological and evolutionary changes in wild populations and also affect sex ratios but few studies have empirically documented skewed sex ratios in exploited fishes (other than species with extreme sexual size dimorphism, SSD). To investigate the possibility of sex‐selective fishing on Alaskan sockeye salmon Oncorhynchus nerka, we assessed sex ratios in fish at two spatial scales: within each of five fishing districts and among 13 breeding populations in one of these districts. We predicted that populations’ sex ratios would vary based on the average size of fish and SSD because size affects vulnerability to fishing. At the larger scale, we found a small but significant bias in fish returning to four of the five fishing districts (average = 52% females), and in four of the five districts males were caught at significantly higher rates than females. At the finer scale there was marked variation in sex ratio on the breeding grounds, ranging from 36% to 47% males. Populations with fish of intermediate sizes experienced the greatest sex ratio biases; the greater vulnerability of males than females to fishing resulted from a combination of larger SSD and different harvest rates between the sexes associated with the fishery size‐selectivity curve shape. Skewed sex ratios may change competition and behavior on the breeding grounds, relaxing selection on male traits associated with mate choice by females or intra‐sexual competition and altering demographic and evolutionary pressures on the fish. Assessment of the size selectivity of fishing gear and the population's SSD can help to illuminate if and how exploitation can affect sex ratios. Future studies examining size‐selective fishing should also evaluate the consequences for sex ratios, as this might help explain changes in harvested population structure and sustainability.     

Assessing evolutionary consequences of size-selective recreational fishing on multiple life-history traits,with an application to northern pike (<Emphasis Type="Italic">Esox lucius</Emphasis>)

Despite mounting recognition of the importance of fishing-induced evolution, methods for quantifying selection pressures on multiple adaptive traits affected by size-selective harvesting are still scarce. We study selection differentials on three life-history traits—reproductive investment, size at maturation, and growth capacity—under size-selective exploitation of northern pike (Esox lucius L.) with recreational-fishing gear. An age-structured population model is presented that accounts for the eco-evolutionary feedback arising from density-dependent and frequency-dependent selection. By introducing minimum-length limits, maximum-length limits, and combinations of such limits (resulting in harvestable-slot length limits) into the model, we examine the potential of simple management tools for mitigating selection pressures induced by recreational fishing. With regard to annual reproductive investment, we find that size-selective fishing mortality exerts relatively small positive selection differentials. By contrast, selection differentials on size at maturation are large and consistently negative. Selection differentials on growth capacity are often large and positive, but become negative when a certain range of minimum-length limits are applied. In general, the strength of selection is reduced by implementing more stringent management policies, but each life-history trait responds differently to the introduction of specific harvest regulations. Based on a simple genetic inheritance model, we examine mid- and long-term evolutionary changes of the three life-history traits and their impacts on the size spectrum and yield of pike. Fishing-induced evolution often reduces sizes and yields, but details depend on a variety of factors such as the specific regulation in place. We find no regulation that is successful in reducing to zero all selection pressures on life-history traits induced by recreational fishing. Accordingly, we must expect that inducing some degree of evolution through recreational fishing is inevitable.     

Rapid,nonparallel genomic evolution of Brassica rapa (field mustard) under experimental drought

While we know that climate change can potentially cause rapid phenotypic evolution, our understanding of the genetic basis and degree of genetic parallelism of rapid evolutionary responses to climate change is limited. In this study, we combined the resurrection approach with an evolve-and-resequence design to examine genome-wide evolutionary changes following drought. We exposed genetically similar replicate populations of the annual plant Brassica rapa derived from a field population in southern California to four generations of experimental drought or watered conditions in a greenhouse. Genome-wide sequencing of ancestral and descendant population pools identified hundreds of SNPs that showed evidence of rapidly evolving in response to drought. Several of these were in stress response genes, and two were identified in a prior study of drought response in this species. However, almost all genetic changes were unique among experimental populations, indicating that the evolutionary changes were largely nonparallel, despite the fact that genetically similar replicates of the same founder population had experienced controlled and consistent selection regimes. This nonparallelism of evolution at the genetic level is potentially because of polygenetic adaptation allowing for multiple different genetic routes to similar phenotypic outcomes. Our findings help to elucidate the relationship between rapid phenotypic and genomic evolution and shed light on the degree of parallelism and predictability of genomic evolution to environmental change.     

Consequences of fisheries-induced evolution for population productivity and recovery potential

Fisheries-induced evolution has become a major branch of the research on anthropogenic and contemporary evolution. Within the conservation context, fisheries-induced evolution has been hypothesized to negatively affect the persistence and recovery potential of depleted populations, but this has not been explicitly investigated. Here, we investigate how fisheries-induced evolution of Atlantic cod (Gadus morhua L.) life histories affects per capita population growth rate, a parameter negatively correlated with extinction risk. We simulate the evolutionary and ecological dynamics of a cod population for a 100 year period of size-selective harvesting, followed thereafter by 300 years of recovery. To evaluate the relative importance of harvest-induced evolution, we either allowed life histories to evolve during and after the fishing period, or we assumed that fisheries-induced evolution was absent. Population growth rates did not differ appreciably between the evolutionary and non-evolutionary simulation scenarios, despite the emergence of rather pronounced differences in life histories. The underlying reason was that in the absence of fishing the cumulative lifetime reproductive outputs were very similar among differing life histories. The results suggest that fisheries-induced evolution might not always have as clear-cut an effect on population growth rate as previously anticipated.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF THE MAMMALIAN BACULUM BY SEXUAL SELECTION

Male genitalia exhibit a taxonomically widespread pattern of rapid and divergent evolution. Sexual selection is generally believed to be responsible for these patterns of evolutionary divergence, although empirical support for the sexual selection hypothesis comes mainly from studies of insects. Here we show that sexual selection is responsible for an evolutionary divergence in baculum morphology among populations of house mice Mus domesticus. We sourced mice from three isolated populations known to be subject to differing strengths of postcopulatory sexual selection and bred them under common‐garden conditions. Mice from populations with strong postcopulatory sexual selection had bacula that were relatively thicker compared with mice from populations with weak selection. We used experimental evolution to determine whether these patterns of divergence could be ascribed to postcopulatory sexual selection. After 27 generations of experimental evolution, populations of mice subjected to postcopulatory sexual selection evolved bacula that were relatively thicker than populations subjected to enforced monogamy. Our data thereby provide evidence that postcopulatory sexual selection underlies an evolutionary divergence in the mammalian baculum and supports the hypothesis that sexual selection plays a general role in the evolution of male genital morphology across evolutionary diverse taxonomic groups.     

Exploitation and recovery of a sea urchin predator has implications for the resilience of southern California kelp forests

Size-structured predator–prey interactions can be altered by the history of exploitation, if that exploitation is itself size-selective. For example, selective harvesting of larger sized predators can release prey populations in cases where only large individuals are capable of consuming a particular prey species. In this study, we examined how the history of exploitation and recovery (inside marine reserves and due to fisheries management) of California sheephead (Semicossyphus pulcher) has affected size-structured interactions with sea urchin prey in southern California. We show that fishing changes size structure by reducing sizes and alters life histories of sheephead, while management measures that lessen or remove fishing impacts (e.g. marine reserves, effort restrictions) reverse these effects and result in increases in density, size and biomass. We show that predation on sea urchins is size-dependent, such that the diet of larger sheephead is composed of more and larger sized urchins than the diet of smaller fish. These results have implications for kelp forest resilience, because urchins can overgraze kelp in the absence of top-down control. From surveys in a network of marine reserves, we report negative relationships between the abundance of sheephead and urchins and the abundance of urchins and fleshy macroalgae (including giant kelp), indicating the potential for cascading indirect positive effects of top predators on the abundance of primary producers. Management measures such as increased minimum size limits and marine reserves may serve to restore historical trophic roles of key predators and thereby enhance the resilience of marine ecosystems.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

Fishing directly selects on growth rate via behaviour: implications of growth-selection that is independent of size

Size-selective harvest of fish and crustacean populations has reduced stock numbers, and led to reduced growth rates and earlier maturation. In contrast to the focus on size-selective effects of harvest, here, we test the hypothesis that fishing may select on life-history traits (here, growth rate) via behaviour, even in the absence of size selection. If true, then traditional size-limits used to protect segments of a population cannot fully protect fast growers, because at any given size, fast-growers will be more vulnerable owing to bolder behaviour. We repeatedly measured individual behaviour and growth of 86 crayfish and found that fast-growing individuals were consistently bold and voracious over time, and were subsequently more likely to be harvested in single- and group-trapping trials. In addition, there was some indication that sex had independent effects on behaviour and trappability, whereby females tended to be less active, shyer, slower-growing and less likely to be harvested, but not all these effects were significant. This study represents, to our knowledge, the first across-individual support for this hypothesis, and suggests that behaviour is an important mechanism for fishing selectivity that could potentially lead to evolution of reduced intrinsic growth rates.     

Harvest-induced maturation evolution under different life-history trade-offs and harvesting regimes

The potential of harvesting to induce adaptive changes in exploited populations is now increasingly recognized. While early studies predicted that elevated mortalities among larger individuals select for reduced maturation size, recent theoretical studies have shown conditions under which other, more complex evolutionary responses to size-selective mortality are expected. These new predictions are based on the assumption that, owing to the trade-off between growth and reproduction, early maturation implies reduced growth. Here we extend these findings by analyzing a model of a harvested size-structured population in continuous time, and by systematically exploring maturation evolution under all three traditionally acknowledged costs of early maturation: reduced fecundity, reduced growth, and/or increased natural mortality. We further extend this analysis to the two main types of harvest selectivity, with an individual's chance of getting harvested depending on its size and/or maturity stage. Surprisingly, we find that harvesting mature individuals not only favors late maturation when the costs of early maturation are low, but promotes early maturation when the costs of early maturation are high. To our knowledge, this study therefore is the first to show that harvesting mature individuals can induce early maturation.     

From nature to the laboratory: the impact of founder effects on adaptation

Most founding events entail a reduction in population size, which in turn leads to genetic drift effects that can deplete alleles. Besides reducing neutral genetic variability, founder effects can in principle shift additive genetic variance for phenotypes that underlie fitness. This could then lead to different rates of adaptation among populations that have undergone a population size bottleneck as well as an environmental change, even when these populations have a common evolutionary history. Thus, theory suggests that there should be an association between observable genetic variability for both neutral markers and phenotypes related to fitness. Here, we test this scenario by monitoring the early evolutionary dynamics of six laboratory foundations derived from founders taken from the same source natural population of Drosophila subobscura. Each foundation was in turn three‐fold replicated. During their first few generations, these six foundations showed an abrupt increase in their genetic differentiation, within and between foundations. The eighteen populations that were monitored also differed in their patterns of phenotypic adaptation according to their immediately ancestral founding sample. Differences in early genetic variability and in effective population size were found to predict differences in the rate of adaptation during the first 21 generations of laboratory evolution. We show that evolution in a novel environment is strongly contingent not only on the initial composition of a newly founded population but also on the stochastic changes that occur during the first generations of colonization. Such effects make laboratory populations poor guides to the evolutionary genetic properties of their ancestral wild populations.     

Effect of size-selective mortality on growth of coastal cod illustrated by tagging data and an individual-based growth and mortality model

In a release experiment with cod in Norway, the apparent mean growth rates of 3+ cod, calculated by sampling the released cohorts at different ages, were very slow (<0·08 mm day⁻¹). However, when individual growth rates of individual tagged cod of the same size range were measured, the mean growth rates were much faster (0·24 mm day⁻¹). These observations were attributed to size-selective fishing mortality and were illustrated by an individual based simulation model of a cohort of cod with variable individual growth rates. The effects on mean length at age of the surviving cohort of increasing fishing intensity were demonstrated. The model showed that size-selective fishing with the observed individual growth variation, removed the fastest-growing individuals at proportionally higher rates than the slower-growing ones, leading to decreased apparent mean growth rate. The fishing pattern which gave the optimum yield, changed when individual variation was included, and when the apparent growth rate was used in the model the yield per recruit reduced dramatically. This study has shown that individual growth heterogeneity and size-selective mortality are factors which should be considered in future fisheries management models.     

A century of life-history evolution in grayling

Synchronic and allochronic data sets consisting of phenotypic values of various life-history traits from five grayling Thymallus thymallus populations with common ancestors were analysed for the purpose of estimating evolution and divergence rates. The synchronic data contained both juvenile and adult traits from populations that have been segregated for 44–88 years (9–22 generations). The allochronic time series contained growth- and maturation data spanning 95 years (16 generations). Estimated evolution and divergence rates were high compared with other life-history studies on the same temporal scale (0.002–1.008 haldanes, 10–30, 500 darwins). The divergence of adult traits were most probably caused by differential mortalities induced by variation in fishing intensity. For the population with allochronic data, 48 years (eight generations) of intense and consistent size-selective gill-net fishing resulted in a constant reduction in age (–0.33 years pr 10 year) and length (–18mm pr 10 year) at maturity. Length-at-age for ages one to five also decreased during the same period. When gill-net fishing was relaxed, age and length at maturity and length-at-age increased. Divergence rates for juvenile traits derived from a common-garden experiment were high, and standardized selection differentials (s) were high, especially for yolk-sac volume (s=2.6). We also document that low divergence rates for juvenile traits were lower between populations having similar spawning/nursery habitats (running water) than populations having relatively different habitats (running water v.s. still water). We suggest that the major part of the observed phenotypic divergence is mostly due to adaptive evolution, although microsatellite data indicate that genetic drift also has occurred.     

Influence of population decline, fishing, and spawner variability on the recovery of marine fishes

Based on an analysis of 90 marine fish populations, collapses (the greatest proportional reduction in spawner biomass over 15 years) are predicated typically by dramatic increases in fishing mortality and recoveries are more likely to occur when exploitation is reduced. However, among populations for which fishing mortality declined after collapse, recovery was independent of exploitation rate, even when fishing mortality (F) post-collapse was expressed as a function of each population's maximum growth rate (r). After a period of 15 years, many populations that experienced 15 year declines >60% exhibited little or no recovery, despite considerable reductions in fishing mortality. This suggests that factors other than fishing may be considerably more important to recovery, and fishing less important, than previously thought. Furthermore, among populations for which fishing mortality decreased post-collapse, rate of population decline was a reliable predictor of recovery. With the possible exception of clupeids, variation in marine fish breeding population size was found to differ little from that of other vertebrates, and such variability appears to have no effect on rate of recovery. In addition to providing an empirical framework for the study of population collapse and recovery, the analyses presented here provide a means of assessing the precautionary nature of various population-decline thresholds used to assign extinction risks to marine fish.     

Evolution in ecological field experiments: implications for effect size

Rapid evolution in response to strong selection, much of which is human-induced, has been indisputably documented. In this perspective, we suggest that adaptation may influence the effect size of treatments in ecological field experiments and alter our predictions of future dynamics in ecological systems. Field experiments often impose very strong and consistent selection over multiple generations. Focal populations may adapt to these treatments and, in the process, increase or decrease the magnitude of the treatment effect through time. We argue that how effect size changes through time will depend on the evolutionary history of the experimental population, the type of experimental manipulation, and the traits involved in adaptive responses. While no field study has conclusively demonstrated evolution in response to treatments with concomitant changes in ecological effect size, we present several examples that provide strong circumstantial evidence that such effects occur. We conclude with a consideration of the differences between plastic and genetic responses to treatments and discuss future research directions linking adaptation to ecological effect size.     

How phenotypic convergence arises in experimental evolution

Evolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a “real‐time” or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short‐term (～20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short‐ and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long‐established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.     

A Systematic Overview of Harvesting-Induced Maturation Evolution in Predator–Prey Systems with Three Different Life-History Tradeoffs

There are concerns that anthropogenic harvesting may cause phenotypic adaptive changes in exploited wild populations, in particular maturation at a smaller size and younger age. In this paper, we study the evolutionarily stable size at maturation of prey subjected to size-selective harvesting in a simple predator?Cprey model, taking into account three recognized life-history costs of early maturation, namely reduced fecundity, reduced growth, and increased mortality. Our analysis shows that harvesting large individuals favors maturation at smaller size compared to the unharvested system, independent of life-history tradeoff and the predator??s prey-size preference. In general, however, the evolutionarily stable maturation size can either increase or decrease relative to the unharvested system, depending on the harvesting regime, the life-history tradeoff, and the predator??s preferred size of prey. Furthermore, we examine how the predator population size changes in response to adaptive change in size at maturation of the prey. Surprisingly, in some situations, we find that the evolutionarily stable maturation size under harvesting is associated with an increased predator population size. This occurs, in particular, when early maturation trades off with growth rate. In total, we determine the evolutionarily stable size at maturation and associated predator population size for a total of forty-five different combinations of tradeoff, harvest regime, and predated size class.     

Harvest-induced disruptive selection increases variance in fitness-related traits

The form of Darwinian selection has important ecological and management implications. Negative effects of harvesting are often ascribed to size truncation (i.e. strictly directional selection against large individuals) and resultant decrease in trait variability, which depresses capacity to buffer environmental change, hinders evolutionary rebound and ultimately impairs population recovery. However, the exact form of harvest-induced selection is generally unknown and the effects of harvest on trait variability remain unexplored. Here we use unique data from the Windermere (UK) long-term ecological experiment to show in a top predator (pike, Esox lucius) that the fishery does not induce size truncation but disruptive (diversifying) selection, and does not decrease but rather increases variability in pike somatic growth rate and size at age. This result is supported by complementary modelling approaches removing the effects of catch selectivity, selection prior to the catch and environmental variation. Therefore, fishing most likely increased genetic variability for somatic growth in pike and presumably favoured an observed rapid evolutionary rebound after fishery relaxation. Inference about the mechanisms through which harvesting negatively affects population numbers and recovery should systematically be based on a measure of the exact form of selection. From a management perspective, disruptive harvesting necessitates combining a preservation of large individuals with moderate exploitation rates, and thus provides a comprehensive tool for sustainable exploitation of natural resources.