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.     

Recurrent fruit harvesting reduces seedling density but increases the frequency of clonal reproduction in a tropical tree

Studies on the ecological impacts of non‐timber forest products (NTFP) harvest reveal that plants are often more resilient to fruit and seed harvest than to bark and root harvest. Several studies indicate that sustainable fruit harvesting limits can be set very high (>80% fruit harvesting intensity). For species with clonal and sexual reproduction, understanding how fruit harvest affects clonal reproduction can shed light on the genetic risks and sustainability of NTFP harvest. We studied 18 populations of a gallery forest tree, Pentadesma butyracea (Clusiaceae), to test the impact of fruits harvest, climate and habitat size (gallery forest width) on the frequency of sexual or clonal recruitment in Benin, West Africa. We sampled populations in two ecological regions (Sudanian and Sudano‐Guinean) and in each region, we selected sites with low, moderate and high fruit harvesting intensities. These populations were selected in gallery forests with varying width to sample the natural variation in P. butyracea habitat size. Heavily harvested populations produced significantly less seedlings but had the highest density and proportion of clonal offspring. Our study suggests that for plant species with dual reproductive strategy (via seeds and clonal), fruit harvesting and associated disturbances that come with it can lead to an increase in the proportion of clonal offspring. This raises the issue that excessive fruit harvest by increasing the proportion of clonal offspring to the detriment of seed originated offspring may lead to a reduction in genetic diversity with consequence on harvested species capability to withstand environmental stochasticity.     

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.     

Evolutionary responses to harvesting in ungulates

1. We investigate the evolutionary responses to harvesting in ungulates using a state-dependent, stochastic, density-dependent individual-based model of red deer Cervus elaphus (L.) females subject to different harvesting regimes. 2. The population's mean weight at first reproduction shifts towards light weights as harvesting increases, and its distribution changes from a single peak distribution under very low or high harvest rates, to a bimodal distribution under intermediate harvest rates. 3. These results suggest that, consistent with previous studies on aquatic species, harvesting-induced mortality may drive adaptive responses in ungulates by reducing the fitness benefits from adult survival and growth in favour of early and lightweight reproduction. 4. Selective harvesting for heavy animals has no additional effect on the evolutionarily stable strategy, suggesting that harvest rate is more important than the degree of selectivity in driving adaptive responses. However, selective harvesting of light females is positively associated with maturation weights even higher than those of a nonharvested population, probably due to the reduction in the fitness value of the offspring. 5. The average number of weight at maturation strategies in the population declines but the total number of strategies across all simulations increases with harvest rate, suggesting that harvesting-induced selection on weight at maturity overcomes the increase in strategy diversity expected from density-dependent release. 6. Yield initially increases with harvesting due to enhanced productivity of light females experiencing density-dependent release. However, it crashes under intense harvesting resulting in a population skewed to light, young and, therefore, less reproductive animals.     

Effects of harvesting onAscophyllum nodosum (L.) Le Jol. (Fucales,Phaeophyta): a demographic approach

Although populations ofAscophyllum nodosum are harvested commercially, little is known about the effects on demographic vital rates (growth, reproduction, survival). This study examines the effects of harvesting season and harvesting intensity on growth, reproduction and mortality of intact fronds in four size classes and in fronds truncated by the harvest. Knowledge of size-specific vital rates was used to evaluate the response of the population to harvesting.Harvesting season and harvesting intensity did not exert a significant effect on growth. Growth in plots not subject to harvesting was less than in harvested plots. No major differences in growth, reproduction and survival between intact and severed fronds emerged. The number of fronds attaining reproduction was enhanced by increased harvesting intensity and by cutting in summer. Harvesting did not seem to induce breakage, and breakage appeared higher in the uncut plots. Most harvesting treatments did not influence survivorship and survivorship was similar among all size classes. Growth rates were inversely related to sizes of fronds.Assessment of variation across size classes yielded more accurate estimates of growth rates than those of previously used methods. Accurate size class specific-growth rates will be a useful criterion when regulating intervals between harvests. Furthermore, assessment of size-specific vital rates allows identification of the frond size classes most relevant to the preservation of resources. Because of their fast growth rates and abundance, fronds in class 1, and, to a lesser extent, class 2, are responsible for most of the population regrowth after harvest. In contrast, classes 3 and 4 contribute little to recovery. This finding provides a strong basis for a harvesting strategy that targets the largest fronds.Author for correspondence     

The effect of optimal harvesting on the dynamics of size and genetic composition of a two-age population

The effect of optimal stationary harvesting at a constant harvest rate on the dynamics of a two-age population is considered. It has been shown analytically that harvesting a fixed rate of the population size of only one age cohort is optimal. As has been observed, the maximum of revenue function is unattainable in the case of concurrent harvesting of both age cohorts. It has been demonstrated that the direction of natural selection does not explicitly change when unselectively harvesting individuals; however, the adaptive genetic diversity of an unharvested population can be lost due to harvesting.     

Modeling the Effects of Harvest Alternatives on Mitigating Oak Decline in a Central Hardwood Forest Landscape

Oak decline is a process induced by complex interactions of predisposing factors, inciting factors, and contributing factors operating at tree, stand, and landscape scales. It has greatly altered species composition and stand structure in affected areas. Thinning, clearcutting, and group selection are widely adopted harvest alternatives for reducing forest vulnerability to oak decline by removing susceptible species and declining trees. However, the long-term, landscape-scale effects of these different harvest alternatives are not well studied because of the limited availability of experimental data. In this study, we applied a forest landscape model in combination with field studies to evaluate the effects of the three harvest alternatives on mitigating oak decline in a Central Hardwood Forest landscape. Results showed that the potential oak decline in high risk sites decreased strongly in the next five decades irrespective of harvest alternatives. This is because oak decline is a natural process and forest succession (e.g., high tree mortality resulting from intense competition) would eventually lead to the decrease in oak decline in this area. However, forest harvesting did play a role in mitigating oak decline and the effectiveness varied among the three harvest alternatives. The group selection and clearcutting alternatives were most effective in mitigating oak decline in the short and medium terms, respectively. The long-term effects of the three harvest alternatives on mitigating oak decline became less discernible as the role of succession increased. The thinning alternative had the highest biomass retention over time, followed by the group selection and clearcutting alternatives. The group selection alternative that balanced treatment effects and retaining biomass was the most viable alternative for managing oak decline. Insights from this study may be useful in developing effective and informed forest harvesting plans for managing oak decline.     

On the moulding of senescence by natural selection in sexual and partly sexual populations

Under a wide variety of dynamic environmental conditions, natural selection appears to favor reproductive investment in a sexually produced offspring, carrying only half of the mother’s genes, over the investment in an asexually produced offspring, genetically identical to her. It is maintained that the same environmental conditions must affect the evolutionary cost and benefit of an investment in the prolongation of one’s own life versus an investment in sexual reproduction, in favor of the latter. The effects of different environmental conditions on the division of resources among sexual reproduction, asexual reproduction and prolongation of life are studied.     

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.     

Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids

Sexual reproduction implies binary outcomes of competitive interactions for access to male gametes: lifelong virgin females with null fitness vs. mated females with variable (generally nonzero) fitness. Female mating failure has long remained a dormant concept in sexual selection theory in part because it is acutely maladaptive (lifelong virgins that do not reproduce are strongly selected against) and also due to widespread acceptance of the Bateman–Trivers paradigm (anisogamy and correlated sex roles). Based on recent scientific output on lifelong virginity across multiple taxonomic groups in insects (Coleoptera, Diptera, Hemiptera, Lepidoptera, Odonata, Orthoptera, Strepsiptera), female mating failure has become a mainstay of sexual selection over the last decade. Lifelong virginity and senescence (death) are intertwined processes; old virgin females compensate for increased risk of lifelong virginity by becoming less choosy and increasing investment in mating‐related activities. Low rates of female lifelong virginity (<5%) in most natural populations of insects indicate that sex generally ‘works’ due to selective pressures acting on both males and females to enhance lifetime fitness. Mating failures are most common in insects with female flightlessness; these pressures may lead in evolutionary time to transitionary pathways from sexual reproduction to parthenogenesis. Female mating probability is affected by nonlinear density‐dependent processes dependent upon the scale of observation (mate‐encounter Allee effect at large spatial scales, mating interferences between females at small scales). Mate choice and sex role reversal (females being the active sexual partner) are ubiquitous in insects and arachnids with significant paternal investment, but consequences in terms of female lifelong virginity remain unknown. Logistically, conceptual development of female mating failure in insects is most limited by the lack of broadly applicable methods to assess rates of lifetime virginity among flighted females.     

Harvest‐induced phenotypic selection in an island population of moose,Alces alces

Empirical evidence strongly indicates that human exploitation has frequently led to rapid evolutionary changes in wild populations, yet the mechanisms involved are often poorly understood. Here, we applied a recently developed demographic framework for analyzing selection to data from a 20‐year study of a wild population of moose, Alces alces. In this population, a genetic pedigree has been established all the way back to founders. We demonstrate harvest‐induced directional selection for delayed birth dates in males and reduced body mass as calf in females. During the study period, birth date was delayed by 0.81 days per year for both sexes, whereas no significant changes occurred in calf body mass. Quantitative genetic analyses indicated that both traits harbored significant additive genetic variance. These results show that selective harvesting can induce strong selection that oppose natural selection. This may cause evolution of less favorable phenotypes that become maladaptive once harvesting ceases.     

Hunting Bambi—evaluating the basis for selective harvesting of juveniles

Human harvesting is often a major mortality factor and, hence, an important proximate factor driving the population dynamics of large mammals. Several selective harvesting regimes focus on removing animals with low reproductive value, such as “antlered” harvests in North America and juvenile harvesting in many European countries. Despite its widespread use and assumed impact, the scientific basis of juvenile harvesting is scattered in the literature and not empirically well-documented. We give the first overview of demographic, evolutionary and practical management arguments for selective harvesting of juveniles. Furthermore, we empirically test two demographic arguments based on harvest statistics of Red Deer (Cervus elaphus) in seven European countries. P₁: Harvesting juveniles has little influence on harvest growth compared with harvesting adult females due to the lower reproductive value of juveniles than adult females; P₂: Harvesting of juveniles dampens variance in harvest due to lower and more variable natural survival rates of juveniles compared with adults. We found that harvesting juveniles has little effect on harvest growth rate, while harvesting adult females has a significant negative effect (consistent with P₁), but that increasing the proportion of juveniles in the harvest did not decrease the variability in harvest between years (P₂ not supported). Based on our empirical findings and overview of arguments, we discuss how the merits of juvenile harvesting may vary over time as populations move from a low density to a very high density state.     

Fitness landscape of Atlantic cod shaped by harvest selection and natural selection

Harvesting may lead to evolutionary changes in life histories on a contemporary time scale, changes that could be maladaptive in natural contexts. However, our understanding of the strength and direction of harvest-induced selection versus natural selection is still limited, partly due to the difficulty of tracking the fate of individuals in the wild. Here, we present direct estimates of harvest mortality, natural mortality and site fidelity of coastal Atlantic cod (Gadus morhua) from the Norwegian Skagerrak coast. Furthermore, we present standardised selection differentials for fish body size. Estimates are obtained from acoustic telemetry, where we continuously monitored fish (n = 60) within a semi-sheltered area using a network of 25 listening stations. To obtain additional information about harvested cod, all fish (body size: 30–66 cm) were also tagged with traditional T-bar tags with a printed reward of 500 NOK (60 E). We estimate that 75% of the fish died within the study area during 1 year. Fishing mortality was markedly higher than natural mortality. Together, recreational fishers and commercial fishers caught at least 50% of the tagged fish during 1 year. Standardised selection differentials showed that fisheries targeted larger fish (i.e. favoured the survival of smaller fish), while natural selection favoured the survival of larger fish. Albeit on a small scale, we provide empirical evidence that harvesting can have a dominant influence on the fitness landscape experienced by a marine fish such as the Atlantic cod. We suggest that no-take marine reserves may help to counter evolutionary impacts of harvesting in the ocean.     

Harvesting,census timing and “hidden” hydra effects

Population control in some form of harvesting might be expected to reduce population size, but quite the opposite can happen due to the hydra effect. This phenomenon describes an increase in population size with increased mortality. One mechanism causing hydra effects is the temporal separation of (i) harvesting and (ii) density-dependent reproduction. Here we consider discrete-time models of these two processes. It is commonly believed that harvesting needs to precede reproduction for a hydra effect to occur. We show that, by contrast, hydra effects also take place for harvest after reproduction. Due to the timing of population census, however, the hydra effect will not be measured and thus remains ‘hidden’. As a consequence, managers may miss out on the opportunity to increase both the yield and the remaining stock of renewable resources. If harvesting aims at controlling pest species, management interventions may backfire in the sense that the pest increases rather than decreases—and, to make things even worse, this may actually go unnoticed. To remedy these undesirable consequences, we propose a modelling framework that can reveal hidden hydra effects. Our results are based on rigorous mathematical proofs that the order of two events does not matter for standard harvesting/hunting strategies.     

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.     

Effects of size‐ and sex‐selective harvesting: An integral projection model approach

Harvesting is often size‐selective, and in species with sexual size dimorphism, it may also be sex‐selective. A powerful approach to investigate potential consequences of size‐ and/or sex‐selective harvesting is to simulate it in a demographic population model. We developed a population‐based integral projection model for a size‐ and sex‐structured species, the commonly exploited pike (Esox lucius). The model allows reproductive success to be proportional to body size and potentially limited by both sexes. We ran all harvest simulations with both lower size limits and slot limits, and to quantify the effects of selective harvesting, we calculated sex ratios and the long‐term population growth rate (λ). In addition, we quantified to what degree purely size‐selective harvesting was sex‐selective, and determined when λ shifted from being female to male limited under size‐ and sex‐selective harvesting. We found that purely size‐selective harvest can be sex‐selective, and that it depends on the harvest limits and the size distributions of the sexes. For the size‐ and sex‐selective harvest simulations, λ increased with harvest intensity up to a threshold as females limited reproduction. Beyond this threshold, males became the limiting sex, and λ decreased as more males were harvested. The peak in λ, and the corresponding sex ratio in harvest, varied with both the selectivity and the intensity of the harvest simulation. Our model represents a useful extension of size‐structured population models as it includes both sexes, relaxes the assumption of female dominance, and accounts for size‐dependent fecundity. The consequences of selective harvesting presented here are especially relevant for size‐ and sex‐structured exploited species, such as commercial fisheries. Thus, our model provides a useful contribution toward the development of more sustainable harvesting regimes.     

The Lessonia nigrescens fishery in northern Chile: “how you harvest is more important than how much you harvest”

In Chile, management of natural resources usually starts right before its imminent collapse or after evident declination. In the northern area of the country, the fishery of brown seaweeds has an enormous social, ecological, and economical importance. More than 11,000 people depend directly or indirectly on the collection and harvesting of this resource. Ecologically, kelps constitute areas for food, reproduction, and refuge for hundreds of invertebrates and fish species. Economically, landings up to 300,000 dry tons per year represent close to US $60 million for the industry. Until 2002, the Chilean brown seaweed fishery was mainly sustained by natural mortality, where plants cast ashore were collected by artisanal fishermen. Since then, three brown seaweed species of economic importance (Lessonia nigrescens, Lessonia trabeculata, and Macrocystis pyrifera) have been intensively harvested in coastal areas between 18° and 32° S. To manage kelp populations along the northern Chilean coast, regulations have been based on the principle “how you harvest is more important than how much you harvest”. This exploitation strategy has been adopted in consensus between fishermen, industries, governmental entities, and scientists. Since L. nigrescens represents more than 70% of total brown seaweed landings, this study tests the effects of L. nigrescens harvesting on the following population variables: (1) abundance, (2) distribution, (3) juvenile recruitment, (4) plant morphology, (5) frequency of reproductive plants, and (6) biodiversity of the macroinvertebrate community associated to kelp holdfasts. Our results show that, despite the enormous harvesting pressure on Lessonia density and biomass, the associated macroinvertebrate richness has been maintained, due to normal plant growth and high recruitment all year round.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae

Trade-offs between life-history components are a central concept of evolution and ecology. Sexual and natural selection seem particularly apt to impose antagonistic selective pressures. When sex is not integrated into reproduction, as in Saccharomyces cerevisiae, natural selection can impair or even eliminate it. In this study, a genetic trade-off between the sexual and asexual phases of the yeast life cycle was suggested by sharp declines in the mating and sporulation abilities of unrelated genotypes that were propagated asexually in minimal growth medium and in mice. When sexual selection was applied to populations that had previously evolved asexually, sexual fitness increased but asexual fitness declined. No such negative correlation was observed when sexual selection was applied to an ancestral strain: sexual and asexual fitness both increased. Thus, evolutionary history affected the evolution of genetic correlations, as fitness increases in a population already well adapted to the environment were more likely to come at the expense of sexual functions.     

Determinants of male fitness: disentangling intra- and inter-sexual selection

Both intra- and inter-sexual selection may crucially determine a male's fitness. Their interplay, which has rarely been experimentally investigated, determines a male's optimal reproductive strategy and thus is of fundamental importance to the understanding of a male's behaviour. Here we investigated the relative importance of intra- and inter-sexual selection for male fitness in the common lizard. We investigated which male traits predict a male's access to reproduction allowing for both selective pressures and comparing it with a staged mating experiment excluding all types of intra-sexual selection. We found that qualitatively better males were more likely to reproduce and that sexual selection was two times stronger when allowing for both selective pressures, suggesting that inter- and intra-sexual selection determines male fitness and confirming the existence of multi-factorial sexual selection. Consequently, to optimize fitness, males should trade their investment between the traits, which are important for inter- and intra-sexual selection.