Evolutionary regime shifts in age and size at maturation of exploited fish stocks

Worldwide declines of fish stocks raise concerns about deleterious consequences of harvesting for stock abundances and individual life histories, and call for appropriate recovery strategies. Fishes in exploited stocks mature earlier at either larger or smaller sizes due to both genetic and plastic responses. The latter occur commonly when reduced competition for food leads to faster growth. Using a size-structured consumer-resource model, which accounts for both genetic and plastic responses, we show that fisheries-induced evolutionary changes in individual life history and stock properties can easily become irreversible. As a result of annual spawning, early maturation at small sizes and late maturation at large sizes can become alternative, evolutionarily and ecologically stable states under otherwise identical environmental conditions. Exploitation of late-maturing populations can then induce an evolutionary regime shift to smaller maturation sizes associated with stepwise, 1-year decreases in age at first reproduction. Complete and early fishing moratoria slowly reverse this process, but belated or partial closure of fisheries may accelerate or even instigate further evolution to smaller sizes at maturation. We suggest that stepwise decreases in maturation age can be used as early warnings of upcoming evolutionary changes, and should inspire timely restrictions of fisheries.     

Vulnerability of individual fish to capture by trawling is influenced by capacity for anaerobic metabolism

The harvest of animals by humans may constitute one of the strongest evolutionary forces affecting wild populations. Vulnerability to harvest varies among individuals within species according to behavioural phenotypes, but we lack fundamental information regarding the physiological mechanisms underlying harvest-induced selection. It is unknown, for example, what physiological traits make some individual fish more susceptible to capture by commercial fisheries. Active fishing methods such as trawling pursue fish during harvest attempts, causing fish to use both aerobic steady-state swimming and anaerobic burst-type swimming to evade capture. Using simulated trawling procedures with schools of wild minnows Phoxinus phoxinus, we investigate two key questions to the study of fisheries-induced evolution that have been impossible to address using large-scale trawls: (i) are some individuals within a fish shoal consistently more susceptible to capture by trawling than others?; and (ii) if so, is this related to individual differences in swimming performance and metabolism? Results provide the first evidence of repeatable variation in susceptibility to trawling that is strongly related to anaerobic capacity and swimming ability. Maximum aerobic swim speed was also negatively correlated with vulnerability to trawling. Standard metabolic rate was highest among fish that were least vulnerable to trawling, but this relationship probably arose through correlations with anaerobic capacity. These results indicate that vulnerability to trawling is linked to anaerobic swimming performance and metabolic demand, drawing parallels with factors influencing susceptibility to natural predators. Selection on these traits by fisheries could induce shifts in the fundamental physiological makeup and function of descendent populations.     

Does Angling Technique Selectively Target Fishes Based on Their Behavioural Type?

Recently, there has been growing recognition that fish harvesting practices can have important impacts on the phenotypic distributions and diversity of natural populations through a phenomenon known as fisheries-induced evolution. Here we experimentally show that two common recreational angling techniques (active crank baits versus passive soft plastics) differentially target wild largemouth bass (Micropterus salmoides) and rock bass (Ambloplites rupestris) based on variation in their behavioural tendencies. Fish were first angled in the wild using both techniques and then brought back to the laboratory and tested for individual-level differences in common estimates of personality (refuge emergence, flight-initiation-distance, latency-to-recapture and with a net, and general activity) in an in-lake experimental arena. We found that different angling techniques appear to selectively target these species based on their boldness (as characterized by refuge emergence, a standard measure of boldness in fishes) but not other assays of personality. We also observed that body size was independently a significant predictor of personality in both species, though this varied between traits and species. Our results suggest a context-dependency for vulnerability to capture relative to behaviour in these fish species. Ascertaining the selective pressures angling practices exert on natural populations is an important area of fisheries research with significant implications for ecology, evolution, and resource management.     

The anatomy of a shrike bite: bill shape and bite performance in Loggerhead Shrikes

There is evidence that fisheries are altering the phenotypic composition of fish populations, often in ways that may reduce the value of fish stocks for the exploiters. Despite the increasing number of theoretical and field studies, there is still debate as to whether these changes are genetic, can be reversed, and are occurring rapidly enough to be considered in fisheries management. We review the contribution that selection experiments have already provided with respect to the study of the evolutionary effect of fisheries, identify issues that still require more study, and outline future directions for doing so. Selection experiments have already been crucial in showing that harvesting can lead to phenotypic and genetic evolution over relatively short time frames. Furthermore, the experiments have shown the changes involve many other traits than those under direct selection, and that these changes tend to have population‐level consequences, including a decreasing fisheries yield. However, experiments focused on fisheries‐induced evolution that fulfil all our requirements are still lacking. Future studies should have more controlled and realistic set‐ups and assess genetic changes in maturation and growth (i.e. traits most often reported to change) to be more relevant to exploited populations in the wild. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 485–503.     

Intense Habitat-Specific Fisheries-Induced Selection at the Molecular Pan I Locus Predicts Imminent Collapse of a Major Cod Fishery

Predation is a powerful agent in the ecology and evolution of predator and prey. Prey may select multiple habitats whereby different genotypes prefer different habitats. If the predator is also habitat-specific the prey may evolve different habitat occupancy. Drastic changes can occur in the relation of the predator to the evolved prey. Fisheries exert powerful predation and can be a potent evolutionary force. Fisheries-induced selection can lead to phenotypic changes that influence the collapse and recovery of the fishery. However, heritability of the phenotypic traits involved and selection intensities are low suggesting that fisheries-induced evolution occurs at moderate rates at decadal time scales. The Pantophysin I (Pan I) locus in Atlantic cod (Gadus morhua), representing an ancient balanced polymorphism predating the split of cod and its sister species, is under an unusual mix of balancing and directional selection including current selective sweeps. Here we show that Pan I alleles are highly correlated with depth with a gradient of 0.44% allele frequency change per meter. AA fish are shallow-water and BB deep-water adapted in accordance with behavioral studies using data storage tags showing habitat selection by Pan I genotype. AB fish are somewhat intermediate although closer to AA. Furthermore, using a sampling design covering space and time we detect intense habitat-specific fisheries-induced selection against the shallow-water adapted fish with an average 8% allele frequency change per year within year class. Genotypic fitness estimates (0.08, 0.27, 1.00 of AA, AB, and BB respectively) predict rapid disappearance of shallow-water adapted fish. Ecological and evolutionary time scales, therefore, are congruent. We hypothesize a potential collapse of the fishery. We find that probabilistic maturation reaction norms for Atlantic cod at Iceland show declining length and age at maturing comparable to changes that preceded the collapse of northern cod at Newfoundland, further supporting the hypothesis. We speculate that immediate establishment of large no-take reserves may help avert collapse.     

A behavioral perspective on fishing-induced evolution

The potential for excessive and/or selective fishing to act as an evolutionary force has been emphasized recently. However, most studies have focused on evolution of life-history traits in response to size-selective harvesting. Here we draw attention to fishing-induced evolution of behavioral and underlying physiological traits. We contend that fishing-induced selection directly acting on behavioral rather than on life-history traits per se can be expected in all fisheries that operate with passive gears such as trapping, angling and gill-netting. Recent artificial selection experiments in the nest-guarding largemouth bass Micropterus salmoides suggest that fishing-induced evolution of behavioral traits that reduce exposure to fishing gear might be maladaptive, potentially reducing natural recruitment. To improve understanding and management of fisheries-induced evolution, we encourage greater application of methods from behavioral ecology, physiological ecology and behavioral genetics.     

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.     

Conceptual bases for quantifying the role of the environment on gene evolution: the participation of positive selection and neutral evolution

To demonstrate that a given change in the environment has contributed to the emergence of a given genotypic and phenotypic shift during the course of evolution, one should ask to what extent such shifts would have occurred without environmental change. Of course, such tests are rarely practical but phenotypic novelties can still be correlated to genomic shifts in response to environmental changes if enough information is available. We surveyed and re-evaluated the published data in order to estimate the role of environmental changes on the course of species and genomic evolution. Only a few published examples clearly demonstrate a causal link between a given environmental change and the fixation of a genomic variant resulting in functional modification (gain, loss or alteration of function). Many others suggested a link between a given phenotypic shift and a given environmental change but failed to identify the underlying genomic determinant(s) and/or the associated functional consequence(s). The proportion of genotypic and phenotypic variation that is fixed concomitantly with environmental changes is often considered adaptive and hence, the result of positive selection, even though alternative causes, such as genetic drift, are rarely investigated. Therefore, the second aim herein is to review evidence for the mechanisms leading to fixation.     

Climate change impacts on mismatches between phytoplankton blooms and fish spawning phenology

Substantial interannual variability in marine fish recruitment (i.e., the number of young fish entering a fishery each year) has been hypothesized to be related to whether the timing of fish spawning matches that of seasonal plankton blooms. Environmental processes that control the phenology of blooms, such as stratification, may differ from those that influence fish spawning, such as temperature‐linked reproductive maturation. These different controlling mechanisms could cause the timing of these events to diverge under climate change with negative consequences for fisheries. We use an earth system model to examine the impact of a high‐emissions, climate‐warming scenario (RCP8.5) on the future spawning time of two classes of temperate, epipelagic fishes: “geographic spawners” whose spawning grounds are defined by fixed geographic features (e.g., rivers, estuaries, reefs) and “environmental spawners” whose spawning grounds move responding to variations in environmental properties, such as temperature. By the century's end, our results indicate that projections of increased stratification cause spring and summer phytoplankton blooms to start 16 days earlier on average (±0.05 days SE) at latitudes >40°N. The temperature‐linked phenology of geographic spawners changes at a rate twice as fast as phytoplankton, causing these fishes to spawn before the bloom starts across >85% of this region. “Extreme events,” defined here as seasonal mismatches >30 days that could lead to fish recruitment failure, increase 10‐fold for geographic spawners in many areas under the RCP8.5 scenario. Mismatches between environmental spawners and phytoplankton were smaller and less widespread, although sizable mismatches still emerged in some regions. This indicates that range shifts undertaken by environmental spawners may increase the resiliency of fishes to climate change impacts associated with phenological mismatches, potentially buffering against declines in larval fish survival, recruitment, and fisheries. Our model results are supported by empirical evidence from ecosystems with multidecadal observations of both fish and phytoplankton phenology.     

The evolution of dispersal in reserve networks

The fragmentation of an environment into developed and protected areas may influence selection pressure on dispersal by increasing the chance of moving from a favorable to an unfavorable habitat. We theoretically explore this possibility through two cases: (1) marine systems in which reduced predation and/or increased feeding drive the evolution of planktonic larval duration and (2) more generally, where stochasticity in reproductive yield drives the evolution of the proportion of offspring dispersing. Model results indicate that habitat fragmentation generally shifts selection pressure toward reduced dispersal, particularly when areas outside reserves are uninhabitable. However, shifts to increased dispersal may occur when temporal heterogeneity is the primary selective force and constant-quota harvest occurs outside reserves. In addition, model results suggest the potential for changes in the genetic variability in dispersal after habitat fragmentation. The predicted evolutionary changes in dispersal will depend on factors such as the relative genetic and environmental contributions to dispersal-related traits and the extent of anthropogenic impacts outside reserves. If the predicted evolutionary changes are biologically attainable, they may suggest altering current guidelines for the appropriate size and spacing of marine reserves necessary to achieve conservation and fisheries goals.     

Challenges in merging fisheries research and management: the Upper Mississippi River experience

The Upper Mississippi River System (UMRS) is a geographically diverse basin extending 10° north temperate latitude that has produced fishes for humans for millennia. During European colonization through the present, the UMRS has been modified to meet multiple demands such as navigation and flood control. Invasive species, notably the common carp, have dominated fisheries in both positive and negative ways. Through time, environmental decline plus reduced economic incentives have degraded opportunities for fishery production. A renewed focus on fisheries in the UMRS may be dawning. Commercial harvest and corresponding economic value of native and non-native species along the river corridor fluctuates but appears to be increasing. Recreational use will depend on access and societal perceptions of the river. Interactions (e.g., disease and invasive species transmission) among fish assemblages within the UMRS, the Great Lakes, and other lakes and rivers are rising. Data collection for fisheries has varied in intensity and contiguousness through time, although resources for research and management may be growing. As fisheries production likely relies on the interconnectivity of fish populations and associated ecosystem processes among river reaches (e.g., between the pooled and unpooled UMRS), species-level processes such as genetics, life-history interactions, and migratory behavior need to be placed in the context of broad ecosystem- and landscape-scale restoration. Formal communication among a diverse group of researchers, managers, and public stakeholders crossing geographic and disciplinary boundaries is necessary through peer-reviewed publications, moderated interactions, and the embrace of emerging information technologies.     

Reorganization of a large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea

Marine ecosystems such as the Baltic Sea are currently under strong atmospheric and anthropogenic pressure. Besides natural and human-induced changes in climate, major anthropogenic drivers such as overfishing and anthropogenic eutrophication are significantly affecting ecosystem structure and function. Recently, studies demonstrated the existence of alternative stable states in various terrestrial and aquatic ecosystems. These so-called ecosystem regime shifts have been explained mainly as a result of multiple causes, e.g. climatic regime shifts, overexploitation or a combination of both. The occurrence of ecosystem regime shifts has important management implications, as they can cause significant losses of ecological and economic resources. Because of hysteresis in ecosystem responses, restoring regimes considered as favourable may require drastic and expensive management actions. Also the Baltic Sea, the largest brackish water body in the world ocean, and its ecosystems are strongly affected by atmospheric and anthropogenic drivers. Here, we present results of an analysis of the state and development of the Central Baltic Sea ecosystem integrating hydroclimatic, nutrient, phyto- and zooplankton as well as fisheries data. Our analyses of 52 biotic and abiotic variables using multivariate statistics demonstrated a major reorganization of the ecosystem and identified two stable states between 1974 and 2005, separated by a transition period in 1988–1993. We show the change in Baltic ecosystem structure to have the characteristics of a discontinuous regime shift, initiated by climate-induced changes in the abiotic environment and stabilized by fisheries-induced feedback loops in the food web. Our results indicate the importance of maintaining the resilience of an ecosystem to atmospherically induced environmental change by reducing the anthropogenic impact.     

Resurrecting complexity: the interplay of plasticity and rapid evolution in the multiple trait response to strong changes in predation pressure in the water flea Daphnia magna

A resurrection ecology reconstruction of 14 morphological, life history and behavioural traits revealed that a natural Daphnia magna population rapidly tracked changes in fish predation by integrating phenotypic plasticity and widespread evolutionary changes both in mean trait values and in trait plasticity. Increased fish predation mainly generated rapid adaptive evolution of plasticity (especially in the presence of maladaptive ancestral plasticity) resulting in an important change in the magnitude and direction of the multivariate reaction norm. Subsequent relaxation of the fish predation pressure resulted in reversed phenotypic plasticity and mainly caused evolution of the trait means towards the ancestral pre‐fish means. Relaxation from fish predation did, however, not result in a complete reversal to the ancestral fishless multivariate phenotype. Our study emphasises that the study population rapidly tracked environmental changes through a mosaic of plasticity, evolution of trait means and evolution of plasticity to generate integrated phenotypic changes in multiple traits.     

Ecological, environmental and socioeconomic aspects of the Lake Victoria's introduced Nile perch fishery in relation to the native fisheries and the species culture potential: lessons to learn

Inland fishery ecosystems in Africa are characterized by patterns of overexploitation, environmental degradation and exotic species introductions. Ecological complexity and diversity of aquatic habitats dictate that fishes in general are not evenly distributed in a water body. However, fisheries management regimes tend to ignore this basic principle, assume generalized conditions in a water body, and focus more on ‘desired’ objectives such as maximizing catch. The result is to disregard fish habitat boundaries and anthropogenic influences from the catchment that influence fish production. Overexploitation and environmental degradation disrupt sustainable socioeconomic benefits from the fisheries, create uncertainty among investors, but leave some managers calling for more information with the expectation that the fisheries will recover with time. Open access to the fisheries and full control of fishing effort remain challenges for managers. Exotic species introductions and fish farming can increase production, but such interventions require firm commitment to sound ecological principles and strict enforcement of recommended conservation and co‐management measures in capture fisheries. The general tendency to downplay fishing effort issues, other ecosystem values and functions or rely on temperate fisheries models until a new cycle of overexploitation emerges, characterizes many management patterns in inland fisheries. Aquaculture is not an option to challenges in capture fisheries management. Aquaculture should be developed to increase fish production but even this practice may have negative environmental impacts depending on practice and scale. Decades of information on Lake Victoria fisheries trends and aquaculture development did not stop the collapse of native fisheries. The successfully introduced Nile perch (Lates niloticus) has shown signs of overexploitation and aquaculture has again been considered as the option. By reviewing significant trends associated with Nile perch and its feasibility in aquaculture this paper uses Lake Victoria to illustrate ‘special interest management’ targeting selected species of fish rather than the fisheries.     

Shifts in fisheries management: adapting to regime shifts

For many years, fisheries management was based on optimizing yield and maintaining a target biomass, with little regard given to low-frequency environmental forcing. However, this policy was often unsuccessful. In the last two to three decades, fisheries science and management have undergone a shift towards balancing sustainable yield with conservation, with the goal of including ecosystem considerations in decision-making frameworks. Scientific understanding of low-frequency climate–ocean variability, which is manifested as ecosystem regime shifts and states, has led to attempts to incorporate these shifts and states into fisheries assessment and management. To date, operationalizing these attempts to provide tactical advice has met with limited success. We review efforts to incorporate regime shifts and states into the assessment and management of fisheries resources, propose directions for future investigation and outline a potential framework to include regime shifts and changes in ecosystem states into fisheries management.     

Climate change and commercial fishing practices codetermine survival of a long-lived seabird

Understanding the environmental mechanisms that govern population change is a fundamental objective in ecology. Although the determination of how top-down and bottom-up drivers affect demography is important, it is often equally critical to understand the extent to which, environmental conditions that underpin these drivers fluctuate across time. For example, associations between climate and both food availability and predation risk may suggest the presence of trophic interactions that may influence inferences made from patterns in ecological data. Analytical tools have been developed to account for these correlations, while providing opportunities to ask novel questions regarding how populations change across space and time. Here, we combine two modeling disciplines—path analysis and mark-recapture-recovery models—to explore whether shifts in sea-surface temperatures (SSTs) influenced top-down (entanglement in fishing equipment) or bottom-up (forage fish production) population constraints over 60 years, and the extent to which these covarying processes shaped the survival of a long-lived seabird, the Royal tern. We found that hemispheric trends in SST were associated with variation in the amount of fish harvested along the Atlantic coast of North America and in the Caribbean, whereas reductions in forage fish production were mostly driven by shifts in the amount of fish harvested by commercial fisheries throughout the North Atlantic the year prior. Although the indirect (i.e., stock depletion) and direct (i.e., entanglement) impacts of commercial fishing on Royal tern mortality has declined over the last 60 years, increased SSTs during this time period has resulted in a comparable increase in mortality risk, which disproportionately impacted the survival of the youngest age-classes of Royal terns. Given climate projections for the North Atlantic, our results indicate that threats to Royal tern population persistence in the Mid-Atlantic will most likely be driven by failures to recruit juveniles into the breeding population.     

Large but uneven reduction in fish size across species in relation to changing sea temperatures

Ectotherms often attain smaller body sizes when they develop at higher temperatures. This phenomenon, known as the temperature–size rule, has important consequences for global fisheries, whereby ocean warming is predicted to result in smaller fish and reduced biomass. However, the generality of this phenomenon and the mechanisms that drive it in natural populations remain unresolved. In this study, we document the maximal size of 74 fish species along a steep temperature gradient in the Mediterranean Sea and find strong support for the temperature–size rule. Importantly, we additionally find that size reduction in active fish species is dramatically larger than for more sedentary species. As the temperature dependence of oxygen consumption depends on activity levels, these findings are consistent with the hypothesis that oxygen is a limiting factor shaping the temperature–size rule in fishes. These results suggest that ocean warming will result in a sharp, but uneven, reduction in fish size that will cause major shifts in size‐dependent interactions. Moreover, warming will have major implications for fisheries as the main species targeted for harvesting will show the most substantial declines in biomass.     

Using time series analysis to characterize evolutionary and plastic responses to environmental change: a case study of a shift toward earlier migration date in sockeye salmon

Environmental change can shift the phenotype of an organism through either evolutionary or nongenetic processes. Despite abundant evidence of phenotypic change in response to recent climate change, we typically lack sufficient genetic data to identify the role of evolution. We present a method of using phenotypic data to characterize the hypothesized role of natural selection and environmentally driven phenotypic shifts (plasticity). We modeled historical selection and environmental predictors of interannual variation in mean population phenotype using a multivariate state-space model framework. Through model comparisons, we assessed the extent to which an estimated selection differential explained observed variation better than environmental factors alone. We applied the method to a 60-year trend toward earlier migration in Columbia River sockeye salmon Oncorhynchus nerka, producing estimates of annual selection differentials, average realized heritability, and relative cumulative effects of selection and plasticity. We found that an evolutionary response to thermal selection was capable of explaining up to two-thirds of the phenotypic trend. Adaptive plastic responses to June river flow explain most of the remainder. This method is applicable to other populations with time series data if selection differentials are available or can be reconstructed. This method thus augments our toolbox for predicting responses to environmental change.     

Experimental assessment of the probabilistic maturation reaction norm: condition matters

The probabilistic maturation reaction norm (PMRN) describes an individual''s probability of maturing at a given age as a function of size and other relevant phenotypic traits. Population-level shifts in the PMRN are often interpreted to indicate genetic as opposed to phenotypic changes in maturation in fish. Inferences derived from trends in the PMRN have been challenged, warranting an experimental assessment of the method. This was accomplished in a laboratory experiment using zebrafish (Danio rerio). Fish were reared under different food levels to induce variation in growth and maturation. Plasticity in maturation was not entirely captured by the demographic age- and length-based PMRN. Adding condition to the PMRN captured a greater amount of environmental variation in maturation probability. Nevertheless, significant differences in the PMRNs among the food levels remained after accounting for the influences of age, size and condition on maturation probability indicating plasticity of the PMRN. This was particularly pronounced between fish held on low food levels as compared with fish experiencing abundant resources, with the latter experiencing higher size-specific maturation probabilities. Our analysis emphasizes the need for incorporating salient physiological traits influencing maturation, such as condition, to make accurate inferences about documented shifts observed in the position of PMRNs on maturation trends in wild fish stocks.     

Effects of an adaptive zone shift on morphological and ecological diversification in terapontid fishes

A fundamental goal of evolutionary ecology is understanding the processes responsible for contemporary patterns of morphological diversity and species richness. Transitions across the marine–freshwater interface are regarded as key triggers for adaptive radiation of many clades. Using the Australian terapontid fish family as a model system we employed phylogenetic analyses to compare the rates of ecological (dietary) and morphological evolution between marine and freshwater species of the family. Results suggested significantly higher rates of phenotypic evolution in key dietary and morphological characters in freshwater species compared to marine counterparts. Moreover, there was significant correlation between several of these dietary and morphological characters, suggesting an underlying ecomorphological aspect to these greater rates of phenotypic evolution in freshwater clades. Australia’s biogeographic history, which has precluded colonisation by many of the major ostariophysan fish families that make up much global freshwater fish diversity, appears to have provided the requisite ‘ecological opportunity’ to facilitate the radiation of invading marine-derived fish clades.