Coherent long-term body-size responses across all Northwest Atlantic herring populations to warming and environmental change despite contrasting harvest and ecological factors.

Body size is a key component of individual fitness and an important factor in the structure and functioning of populations and ecosystems. Disentangling the effects of environmental change, harvest and intra- and inter-specific trophic effects on body size remains challenging for populations in the wild. Herring in the Northwest Atlantic provide a strong basis for evaluating hypotheses related to these drivers given that they have experienced significant warming and harvest over the past century, while also having been exposed to a wide range of other selective constraints across their range. Using data on mean length-at-age 4 for the sixteen principal populations over a period of 53 cohorts (1962-2014), we fitted a series of empirical models for temporal and between-population variation in the response to changes in sea surface temperature. We find evidence for a unified cross-population response in the form of a parabolic function according to which populations in naturally warmer environments have responded more negatively to increasing temperature compared with those in colder locations. Temporal variation in residuals from this function was highly coherent among populations, further suggesting a common response to a large-scale environmental driver. The synchrony observed in this study system, despite strong differences in harvest and ecological histories among populations and over time, clearly indicates a dominant role of environmental change on size-at-age in wild populations, in contrast to commonly reported effects of fishing. This finding has important implications for the management of fisheries as it indicates that a key trait associated with population productivity may be under considerably less short-term management control than currently assumed. Our study, overall, illustrates the need for a comparative approach within species for inferences concerning the many possible effects on body size of natural and anthropogenic drivers in the wild.

Multiple-batch spawning: a risk-spreading strategy disarmed by highly intensive size-selective fishing rate.

Can the advantage of risk-managing life-history strategies become a disadvantage under human-induced evolution? Organisms have adapted to the variability and uncertainty of environmental conditions with a vast diversity of life-history strategies. One such evolved strategy is multiple-batch spawning, a spawning strategy common to long-lived fishes that 'hedge their bets' by distributing the risk to their offspring on a temporal and spatial scale. The fitness benefits of this spawning strategy increase with female body size, the very trait that size-selective fishing targets. By applying an empirically and theoretically motivated eco-evolutionary mechanistic model that was parameterized for Atlantic cod (Gadus morhua), we explored how fishing intensity may alter the life-history traits and fitness of fishes that are multiple-batch spawners. Our main findings are twofold; first, the risk-spreading strategy of multiple-batch spawning is not effective against fisheries selection, because the fisheries selection favours smaller fish with a lower risk-spreading effect; and second, the ecological recovery in population size does not secure evolutionary recovery in the population size structure. The beneficial risk-spreading mechanism of the batch spawning strategy highlights the importance of recovery in the size structure of overfished stocks, from which a full recovery in the population size can follow.

Differential reproductive plasticity under thermal variability in a freshwater fish (Danio rerio).

Human-driven increases in global mean temperatures are associated with concomitant increases in thermal variability. Yet, few studies have explored the impacts of thermal variability on fitness-related traits, limiting our ability to predict how organisms will respond to dynamic thermal changes. Among the myriad organismal responses to thermal variability, one of the most proximate to fitness-and, thus, a population's ability to persist-is reproduction. Here, we examine how a model freshwater fish (Danio rerio) responds to diel thermal fluctuations that span the species's viable developmental range of temperatures. We specifically investigate reproductive performance metrics including spawning success, fecundity, egg provisioning and sperm concentration. Notably, we apply thermal variability treatments during two ontogenetic timepoints to disentangle the relative effects of developmental plasticity and reversible acclimation. We found evidence of direct, negative effects of thermal variability during later ontogenetic stages on reproductive performance metrics. We also found complex interactive effects of early and late-life exposure to thermal variability, with evidence of beneficial acclimation of spawning success and modification of the relationship between fecundity and egg provisioning. Our findings illuminate the plastic life-history modifications that fish may undergo as their thermal environments become increasingly variable.

Combining population genomics with demographic analyses highlights habitat patchiness and larval dispersal as determinants of connectivity in coastal fish species.

Gene flow shapes spatial genetic structure and the potential for local adaptation. Among marine animals with nonmigratory adults, the presence or absence of a pelagic larval stage is thought to be a key determinant in shaping gene flow and the genetic structure of populations. In addition, the spatial distribution of suitable habitats is expected to influence the distribution of biological populations and their connectivity patterns. We used whole genome sequencing to study demographic history and reduced representation (double-digest restriction associated DNA) sequencing data to analyse spatial genetic structure in broadnosed pipefish (Syngnathus typhle). Its main habitat is eelgrass beds, which are patchily distributed along the study area in southern Norway. Demographic connectivity among populations was inferred from long-term (~30-year) population counts that uncovered a rapid decline in spatial correlations in abundance with distance as short as ~2 km. These findings were contrasted with data for two other fish species that have a pelagic larval stage (corkwing wrasse, Symphodus melops; black goby, Gobius niger). For these latter species, we found wider spatial scales of connectivity and weaker genetic isolation-by-distance patterns, except where both species experienced a strong barrier to gene flow, seemingly due to lack of suitable habitat. Our findings verify expectations that a fragmented habitat and absence of a pelagic larval stage promote genetic structure, while presence of a pelagic larvae stage increases demographic connectivity and gene flow, except perhaps over extensive habitat gaps.

Genomic reaction norms inform predictions of plastic and adaptive responses to climate change.

Genomic reaction norms represent the range of gene expression phenotypes (usually mRNA transcript levels) expressed by a genotype along an environmental gradient. Reaction norms derived from common-garden experiments are powerful approaches for disentangling plastic and adaptive responses to environmental change in natural populations. By treating gene expression as a phenotype in itself, genomic reaction norms represent invaluable tools for exploring causal mechanisms underlying organismal responses to climate change across multiple levels of biodiversity. Our goal is to provide the context, framework and motivation for applying genomic reaction norms to study the responses of natural populations to climate change. Here, we describe the utility of integrating genomics with common-garden-gradient experiments under a reaction norm analytical framework to answer fundamental questions about phenotypic plasticity, local adaptation, their interaction (i.e. genetic variation in plasticity) and future adaptive potential. An experimental and analytical framework for constructing and analysing genomic reaction norms is presented within the context of polygenic climate change responses of structured populations with gene flow. Intended for a broad eco-evo readership, we first briefly review adaptation with gene flow and the importance of understanding the genomic basis and spatial scale of adaptation for conservation and management of structured populations under anthropogenic change. Then, within a high-dimensional reaction norm framework, we illustrate how to distinguish plastic, differentially expressed (difference in reaction norm intercepts) and differentially plastic (difference in reaction norm slopes) genes, highlighting the areas of opportunity for applying these concepts. We conclude by discussing how genomic reaction norms can be incorporated into a holistic framework to understand the eco-evolutionary dynamics of climate change responses from molecules to ecosystems. We aim to inspire researchers to integrate gene expression measurements into common-garden experimental designs to investigate the genomics of climate change responses as sequencing costs become increasingly accessible.

Allee effects and the Allee-effect zone in northwest Atlantic cod.

According to the theory of compensatory dynamics, depleted populations should recover when the threat responsible for their decline is removed because per capita population growth is assumed to be highest when populations are at their smallest viable sizes. Yet, many seriously depleted fish populations have failed to recover despite threat mitigation. Atlantic cod (Gadus morhua) stocks off Newfoundland, despite 30 years of dramatically reduced fishing mortality and numerous fishery closures, have not recovered, suggesting that drivers other than fishing can regulate the growth of collapsed fish populations, inhibiting or preventing their recovery. Here, using Bayesian inference, we show strong evidence of Allee effects in a south Newfoundland cod population, based on data on recruitment and spawning stock biomass. We infer the Allee-effect threshold, below which recovery is impaired. We demonstrate the necessity of data at low population sizes to make inferences about the nature of low-abundance dynamics. Our work indicates that Allee effects are not negligible in commercially exploited fish populations, as commonly projected, and that they represent an inhibitory force that can effectively prevent recovery from overfishing. Our findings contrast with prevailing fisheries management practices that assume compensatory dynamics at low abundances with potential to seriously overestimate the recovery potential of collapsed populations.

Gill area explains deviations from body size-metabolic rate relationship in teleost fishes.

Whether gill area constrains fish metabolism through oxygen limitation is a debated topic. Here, the authors provide insights into this question by analysing mass-specific metabolic rates across 44 teleost fishes extracted from FishBase. They explore whether species deviations from metabolic rates predicted by body mass can be explained by species gill area. They show that the gill area explains c. 26%-28% of species-level deviations from mass-specific metabolic rates. Their findings suggest that gill area might indeed be one of the factors limiting metabolic rate in fishes.

Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change.

Genetic and genomic architectures of traits under selection are key factors influencing evolutionary responses. Yet, knowledge of their impacts has been limited by a widespread assumption that most traits are controlled by unlinked polygenic architectures. Recent advances in genome sequencing and eco-evolutionary modeling are unlocking the potential for integrating genomic information into predictions of population responses to environmental change. Using eco-evolutionary simulations, we demonstrate that hypothetical single-locus control of a life history trait produces highly variable and unpredictable harvesting-induced evolution relative to the classically applied multilocus model. Single-locus control of complex traits is thought to be uncommon, yet blocks of linked genes, such as those associated with some types of structural genomic variation, have emerged as taxonomically widespread phenomena. Inheritance of linked architectures resembles that of single loci, thus enabling single-locus-like modeling of polygenic adaptation. Yet, the number of loci, their effect sizes, and the degree of linkage among them all occur along a continuum. We review how linked architectures are often associated, directly or indirectly, with traits expected to be under selection from anthropogenic stressors and are likely to play a large role in adaptation to environmental disturbance. We suggest using single-locus models to explore evolutionary extremes and uncertainties when the trait architecture is unknown, refining parameters as genomic information becomes available, and explicitly incorporating linkage among loci when possible. By overestimating the complexity (e.g., number of independent loci) of the genomic architecture of traits under selection, we risk underestimating the complexity (e.g., nonlinearity) of their evolutionary dynamics.

Cyclical and stochastic thermal variability affects survival and growth in brook trout.

Directional changes in temperature have well-documented effects on ectotherms, yet few studies have explored how increased thermal variability (a concomitant of climate change) might affect individual fitness. Using a common-garden experimental protocol, we investigated how bidirectional temperature change can affect survival and growth of brook trout (Salvelinus fontinalis) and whether the survival and growth responses differ between two populations, using four thermal-variability treatments (mean: 10 °C; range: 7-13 °C): (i) constancy; (ii) cyclical fluctuations every two days; (iii) low stochasticity (random changes every 2 days); (iv) high stochasticity (random changes daily). Recently hatched individuals were monitored under thermal variability (6 weeks) and a subsequent one-month period of thermal constancy. We found that variability can positively influence survival, relative to thermal constancy, but negatively affect growth. The observations reported here can be interpreted within the context of Jensen's Inequality (performance at average conditions is unequal to average performance across a range of conditions). Projections of future population viability in the context of climate change would be strengthened by increased experimental attention to the fitness consequences of stochastic and non-stochastic thermal variability.

Empirical links between natural mortality and recovery in marine fishes.

Probability of species recovery is thought to be correlated with specific aspects of organismal life history, such as age at maturity and longevity, and how these affect rates of natural mortality (M) and maximum per capita population growth (rmax). Despite strong theoretical underpinnings, these correlates have been based on predicted rather than realized population trajectories following threat mitigation. Here, we examine the level of empirical support for postulated links between a suite of life-history traits (related to maturity, age, size and growth) and recovery in marine fishes. Following threat mitigation (medium time since cessation of overfishing = 20 years), 71% of 55 temperate populations had fully recovered, the remainder exhibiting, on average, negligible change (impaired recovery). Singly, life-history traits did not influence recovery status. In combination, however, those that jointly reflect length-based mortality at maturity, Mα , revealed that recovered populations have higher Mα , which we hypothesize to reflect local adaptations associated with greater rmax But, within populations, the smaller sizes at maturity generated by overfishing are predicted to increase Mα , slowing recovery and increasing its uncertainty. We conclude that recovery potential is greater for populations adapted to high M but that temporal increases in M concomitant with smaller size at maturity will have the opposite effect. The recovery metric documented here (Mα ) has a sound theoretical basis, is significantly correlated with direct estimates of M that directly reflect rmax, is not reliant on data-intensive time series, can be readily estimated, and offers an empirically defensible correlate of recovery, given its clear links to the positive and impaired responses to threat mitigation that have been observed in fish populations over the past three decades.

Thresholds for impaired species recovery.

Studies on small and declining populations dominate research in conservation biology. This emphasis reflects two overarching frameworks: the small-population paradigm focuses on correlates of increased extinction probability; the declining-population paradigm directs attention to the causes and consequences of depletion. Neither, however, particularly informs research on the determinants, rate or uncertainty of population increase. By contrast, Allee effects (positive associations between population size and realized per capita population growth rate, r(realized), a metric of average individual fitness) offer a theoretical and empirical basis for identifying numerical and temporal thresholds at which recovery is unlikely or uncertain. Following a critique of studies on Allee effects, I quantify population-size minima and subsequent trajectories of marine fishes that have and have not recovered following threat mitigation. The data suggest that threat amelioration, albeit necessary, can be insufficient to effect recovery for populations depleted to less than 10% of maximum abundance (N(max)), especially when they remain depleted for lengthy periods of time. Comparing terrestrial and aquatic vertebrates, life-history analyses suggest that population-size thresholds for impaired recovery are likely to be comparatively low for marine fishes but high for marine mammals.Articulation of a 'recovering population paradigm' would seem warranted. It might stimulate concerted efforts to identify generic impaired recovery thresholds across species. It might also serve to reduce the confusion of terminology, and the conflation of causes and consequences with patterns currently evident in the literature on Allee effects, thus strengthening communication among researchers and enhancing the practical utility of recovery-oriented research to conservation practitioners and resource managers.

Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish.

Whether and how habitat fragmentation and population size jointly affect adaptive genetic variation and adaptive population differentiation are largely unexplored. Owing to pronounced genetic drift, small, fragmented populations are thought to exhibit reduced adaptive genetic variation relative to large populations. Yet fragmentation is known to increase variability within and among habitats as population size decreases. Such variability might instead favour the maintenance of adaptive polymorphisms and/or generate more variability in adaptive differentiation at smaller population size. We investigated these alternative hypotheses by analysing coding-gene, single-nucleotide polymorphisms associated with different biological functions in fragmented brook trout populations of variable sizes. Putative adaptive differentiation was greater between small and large populations or among small populations than among large populations. These trends were stronger for genetic population size measures than demographic ones and were present despite pronounced drift in small populations. Our results suggest that fragmentation affects natural selection and that the changes elicited in the adaptive genetic composition and differentiation of fragmented populations vary with population size. By generating more variable evolutionary responses, the alteration of selective pressures during habitat fragmentation may affect future population persistence independently of, and perhaps long before, the effects of demographic and genetic stochasticity are manifest.

Allee effect and the uncertainty of population recovery.

Recovery of depleted populations is fundamentally important for conservation biology and sustainable resource harvesting. At low abundance, population growth rate, a primary determinant of population recovery, is generally assumed to be relatively fast because competition is low (i.e., negative density dependence). But population growth can be limited in small populations by an Allee effect. This is particularly relevant for collapsed populations or species that have not recovered despite large reductions in, or elimination of, threats. We investigated how an Allee effect can influence the dynamics of recovery. We used Atlantic cod (Gadus morhua) as the study organism and an empirically quantified Allee effect for the species to parameterize our simulations. We simulated recovery through an individual-based mechanistic simulation model and then compared recovery among scenarios incorporating an Allee effect, negative density dependence, and an intermediate scenario. Although an Allee effect significantly slowed recovery, such that population increase could be negligible even after 100 years or more, it also made the time required for biomass rebuilding much less predictable. Our finding that an Allee effect greatly increased the uncertainty in recovery time frames provides an empirically based explanation for why the removal of threat does not always result in the recovery of depleted populations or species.

Risk assessment of inbreeding and outbreeding depression in a captive-breeding program.

Captive-breeding programs can be implemented to preserve the genetic diversity of endangered populations such that the controlled release of captive-bred individuals into the wild may promote recovery. A common difficulty, however, is that programs are founded with limited wild broodstock, and inbreeding can become increasingly difficult to avoid with successive generations in captivity. Program managers must choose between maintaining the genetic purity of populations, at the risk of inbreeding depression, or interbreeding populations, at the risk of outbreeding depression. We evaluate these relative risks in a captive-breeding program for 3 endangered populations of Atlantic salmon (Salmo salar). In each of 2 years, we released juvenile F(1) and F(2) interpopulation hybrids, backcrosses, as well as inbred and noninbred within-population crosstypes into 9 wild streams. Juvenile size and survival was quantified in each year. Few crosstype effects were observed, but interestingly, the relative fitness consequences of inbreeding and outbreeding varied from year to year. Temporal variation in environmental quality might have driven some of these annual differences, by exacerbating the importance of maternal effects on juvenile fitness in a year of low environmental quality and by affecting the severity of inbreeding depression differently in different years. Nonetheless, inbreeding was more consistently associated with a negative effect on fitness, whereas the consequences of outbreeding were less predictable. Considering the challenges associated with a sound risk assessment in the wild and given that the effect of inbreeding on fitness is relatively predictable, we suggest that risk can be weighted more strongly in terms of the probable outcome of outbreeding. Factors such as genetic similarities between populations and the number of generations in isolation can sometimes be used to assess outbreeding risk, in lieu of experimentation.

Environmental quality predicts optimal egg size in the wild.

Parents can maximize their reproductive success by balancing the trade-off between investment per offspring and fecundity. According to theory, environmental quality influences the relationship between investment per offspring and offspring fitness, such that well-provisioned offspring fare better when environmental quality is lower. A major prediction of classic theory, then, is that optimal investment per offspring will increase as environmental quality decreases. To test this prediction, we release over 30,000 juvenile Atlantic salmon (Salmo salar) into eight wild stream environments, and we monitor subsequent growth and survival of juveniles. We estimate the shape of the relationship between investment per offspring (egg size) and offspring fitness in each stream. We find that optimal egg size is greater when the quality of the stream environment is lower (as estimated by a composite index of habitat quality). Across streams, the mean size of stream gravel and the mean amount of incident sunlight are the most important individual predictors of optimal egg size. Within streams, juveniles recaptured in stream subsections that featured larger gravels and greater levels of sunlight also grew relatively quickly, an association that complements our cross-stream analyses. This study provides the first empirical verification that environmental quality alters the relationship between investment per offspring and offspring fitness, such that optimal investment per offspring increases as environmental quality decreases.

The relationship between offspring size and fitness: integrating theory and empiricism.

How parents divide the energy available for reproduction between size and number of offspring has a profound effect on parental reproductive success. Theory indicates that the relationship between offspring size and offspring fitness is of fundamental importance to the evolution of parental reproductive strategies: this relationship predicts the optimal division of resources between size and number of offspring, it describes the fitness consequences for parents that deviate from optimality, and its shape can predict the most viable type of investment strategy in a given environment (e.g., conservative vs. diversified bet-hedging). Many previous attempts to estimate this relationship and the corresponding value of optimal offspring size have been frustrated by a lack of integration between theory and empiricism. In the present study, we draw from C. Smith and S. Fretwell's classic model to explain how a sound estimate of the offspring size--fitness relationship can be derived with empirical data. We evaluate what measures of fitness can be used to model the offspring size--fitness curve and optimal size, as well as which statistical models should and should not be used to estimate offspring size--fitness relationships. To construct the fitness curve, we recommend that offspring fitness be measured as survival up to the age at which the instantaneous rate of offspring mortality becomes random with respect to initial investment. Parental fitness is then expressed in ecologically meaningful, theoretically defensible, and broadly comparable units: the number of offspring surviving to independence. Although logistic and asymptotic regression have been widely used to estimate offspring size-fitness relationships, the former provides relatively unreliable estimates of optimal size when offspring survival and sample sizes are low, and the latter is unreliable under all conditions. We recommend that the Weibull-1 model be used to estimate this curve because it provides modest improvements in prediction accuracy under experimentally relevant conditions.

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.

Differences in transcription levels among wild, domesticated, and hybrid Atlantic salmon (Salmo salar) from two environments.

Escaped domesticated individuals can introduce disadvantageous traits into wild populations due to both adaptive differences between population ancestors and human-induced changes during domestication. In contrast to their domesticated counterparts, some endangered wild Atlantic salmon populations encounter during their marine stage large amounts of suspended sediments, which may act as a selective agent. We used microarrays to elucidate quantitative transcriptional differences between a domesticated salmon strain, a wild population and their first-generation hybrids during their marine life stage, to describe transcriptional responses to natural suspended sediments, and to test for adaptive genetic variation in plasticity relating to a history of natural exposure or nonexposure to suspended sediments. We identified 67 genes differing in transcription level among salmon groups. Among these genes, processes related to energy metabolism and ion homoeostasis were over-represented, while genes contributing to immunity and actin-/myosin-related processes were also involved in strain differentiation. Domestic-wild hybrids exhibited intermediate transcription patterns relative to their parents for two-thirds of all genes that differed between their parents; however, genes deviating from additivity tended to have similar levels to those expressed by the wild parent. Sediments induced increases in transcription levels of eight genes, some of which are known to contribute to external or intracellular damage mitigation. Although genetic variation in plasticity did not differ significantly between groups after correcting for multiple comparisons, two genes (metallothionein and glutathione reductase) tended to be more plastic in response to suspended sediments in wild and hybrid salmon, and merit further examination as candidate genes under natural selection.

Life-history correlates of extinction risk and recovery potential.

Extinction risk is inversely associated with maximum per capita population growth rate (r(max)). However, this parameter is not known for most threatened species, underscoring the value in identifying correlates of r(max) that, in the absence of demographic data, would indirectly allow one to identify species and populations at elevated risk of extinction and their associated recovery potential. We undertook a comparative life-history analysis of 199 species from three taxonomic classes: Chondrichthyes (e.g., sharks; n = 82), Actinopterygii (teleost or bony fishes; n = 47), and Mammalia (n = 70, including 16 marine species). Median r(max) was highest for (and similar between) terrestrial mammals (0.71) and teleosts (0.43), significantly lower among chondrichthyans (0.26), and lower still in marine mammals (0.07). Age at maturity was the primary (and negative) correlate of r(max). In contrast, although body size was negatively correlated with r(max) in chondrichthyans and mammals, evidence of an association in teleosts was equivocal, and fecundity was not related to r(max) in fishes, despite recurring assertions to the contrary. Our analyses suggest that age at maturity can serve as a universal predictor of extinction risk in fishes and mammals when r(max) itself is unknown. Moreover, in contrast to what is generally expected, the recovery potential of teleost fishes does not differ from that of terrestrial mammals. Our findings are supportive of the application of extinction-risk criteria that are based on generation time and that are independent of taxonomic affinity.