Global patterns of nuclear and mitochondrial genetic diversity in marine fishes.

Genetic diversity is a fundamental component of biodiversity. Examination of global patterns of genetic diversity can help highlight mechanisms underlying species diversity, though a recurring challenge has been that patterns may vary by molecular marker. Here, we compiled 6862 observations of genetic diversity from 492 species of marine fish and tested among hypotheses for diversity gradients: the founder effect hypothesis, the kinetic energy hypothesis, and the productivity-diversity hypothesis. We fit generalized linear mixed effect models (GLMMs) and explored the extent to which various macroecological drivers (latitude, longitude, temperature (SST), and chlorophyll-a concentration) explained variation in genetic diversity. We found that mitochondrial genetic diversity followed geographic gradients similar to those of species diversity, being highest near the Equator, particularly in the Coral Triangle, while nuclear genetic diversity did not follow clear geographic patterns. Despite these differences, all genetic diversity metrics were correlated with chlorophyll-a concentration, while mitochondrial diversity was also positively associated with SST. Our results provide support for the kinetic energy hypothesis, which predicts that elevated mutation rates at higher temperatures increase mitochondrial but not necessarily nuclear diversity, and the productivity-diversity hypothesis, which posits that resource-rich regions support larger populations with greater genetic diversity. Overall, these findings reveal how environmental variables can influence mutation rates and genetic drift in the ocean, caution against using mitochondrial macrogenetic patterns as proxies for whole-genome diversity, and aid in defining global gradients of genetic diversity.

Bringing traits back into the equation: A roadmap to understand species redistribution.

Ecological and evolutionary theories have proposed that species traits should be important in mediating species responses to contemporary climate change; yet, empirical evidence has so far provided mixed evidence for the role of behavioral, life history, or ecological characteristics in facilitating or hindering species range shifts. As such, the utility of trait-based approaches to predict species redistribution under climate change has been called into question. We develop the perspective, supported by evidence, that trait variation, if used carefully can have high potential utility, but that past analyses have in many cases failed to identify an explanatory value for traits by not fully embracing the complexity of species range shifts. First, we discuss the relevant theory linking species traits to range shift processes at the leading (expansion) and trailing (contraction) edges of species distributions and highlight the need to clarify the mechanistic basis of trait-based approaches. Second, we provide a brief overview of range shift-trait studies and identify new opportunities for trait integration that consider range-specific processes and intraspecific variability. Third, we explore the circumstances under which environmental and biotic context dependencies are likely to affect our ability to identify the contribution of species traits to range shift processes. Finally, we propose that revealing the role of traits in shaping species redistribution may likely require accounting for methodological variation arising from the range shift estimation process as well as addressing existing functional, geographical, and phylogenetic biases. We provide a series of considerations for more effectively integrating traits as well as extrinsic and methodological factors into species redistribution research. Together, these analytical approaches promise stronger mechanistic and predictive understanding that can help society mitigate and adapt to the effects of climate change on biodiversity.

FISHGLOB_data: an integrated dataset of fish biodiversity sampled with scientific bottom-trawl surveys.

Scientific bottom-trawl surveys are ecological observation programs conducted along continental shelves and slopes of seas and oceans that sample marine communities associated with the seafloor. These surveys report taxa occurrence, abundance and/or weight in space and time, and contribute to fisheries management as well as population and biodiversity research. Bottom-trawl surveys are conducted all over the world and represent a unique opportunity to understand ocean biogeography, macroecology, and global change. However, combining these data together for cross-ecosystem analyses remains challenging. Here, we present an integrated dataset of 29 publicly available bottom-trawl surveys conducted in national waters of 18 countries that are standardized and pre-processed, covering a total of 2,170 sampled fish taxa and 216,548 hauls collected from 1963 to 2021. We describe the processing steps to create the dataset, flags, and standardization methods that we developed to assist users in conducting spatio-temporal analyses with stable regional survey footprints. The aim of this dataset is to support research, marine conservation, and management in the context of global change.

The importance of oxygen for explaining rapid shifts in a marine fish.

Large-scale shifts in marine species biogeography have been a notable impact of climate change. An effective explanation of what drives these species shifts, as well as accurate predictions of where they might move, is crucial to effectively managing these natural resources and conserving biodiversity. While temperature has been implicated as a major driver of these shifts, physiological processes suggest that oxygen, prey, and other factors should also play important roles. We expanded upon previous temperature-based distribution models by testing whether oxygen, food web productivity, salinity, and scope for metabolic activity (the Metabolic Index) better explained the changing biogeography of Black Sea Bass (Centropristis striata) in the Northeast US. This species has been expanding further north over the past 15 years. We found that oxygen improved model performance beyond a simple consideration of temperature (ΔAIC = 799, ΔTSS = 0.015), with additional contributions from prey and salinity. However, the Metabolic Index did not substantially increase model performance relative to temperature and oxygen (ΔAIC = 0.63, ΔTSS = 0.0002). Marine species are sensitive to oxygen, and we encourage researchers to use ocean biogeochemical hindcast and forecast products to better understand marine biogeographic changes.

Marine heatwaves are not a dominant driver of change in demersal fishes.

Marine heatwaves have been linked to negative ecological effects in recent decades1,2. If marine heatwaves regularly induce community reorganization and biomass collapses in fishes, the consequences could be catastrophic for ecosystems, fisheries and human communities3,4. However, the extent to which marine heatwaves have negative impacts on fish biomass or community composition, or even whether their effects can be distinguished from natural and sampling variability, remains unclear. We investigated the effects of 248 sea-bottom heatwaves from 1993 to 2019 on marine fishes by analysing 82,322 hauls (samples) from long-term scientific surveys of continental shelf ecosystems in North America and Europe spanning the subtropics to the Arctic. Here we show that the effects of marine heatwaves on fish biomass were often minimal and could not be distinguished from natural and sampling variability. Furthermore, marine heatwaves were not consistently associated with tropicalization (gain of warm-affiliated species) or deborealization (loss of cold-affiliated species) in these ecosystems. Although steep declines in biomass occasionally occurred after marine heatwaves, these were the exception, not the rule. Against the highly variable backdrop of ocean ecosystems, marine heatwaves have not driven biomass change or community turnover in fish communities that support many of the world's largest and most productive fisheries.

Coral Reef Population Genomics in an Age of Global Change.

Coral reefs are both exceptionally biodiverse and threatened by climate change and other human activities. Here, we review population genomic processes in coral reef taxa and their importance for understanding responses to global change. Many taxa on coral reefs are characterized by weak genetic drift, extensive gene flow, and strong selection from complex biotic and abiotic environments, which together present a fascinating test of microevolutionary theory. Selection, gene flow, and hybridization have played and will continue to play an important role in the adaptation or extinction of coral reef taxa in the face of rapid environmental change, but research remains exceptionally limited compared to the urgent needs. Critical areas for future investigation include understanding evolutionary potential and the mechanisms of local adaptation, developing historical baselines, and building greater research capacity in the countries where most reef diversity is concentrated.

Detecting parallel polygenic adaptation to novel evolutionary pressure in wild populations: a case study in Atlantic cod (Gadus morhua).

Populations can adapt to novel selection pressures through dramatic frequency changes in a few genes of large effect or subtle shifts in many genes of small effect. The latter (polygenic adaptation) is expected to be the primary mode of evolution for many life-history traits but tends to be more difficult to detect than changes in genes of large effect. Atlantic cod (Gadus morhua) were subjected to intense fishing pressure over the twentieth century, leading to abundance crashes and a phenotypic shift toward earlier maturation across many populations. Here, we use spatially replicated temporal genomic data to test for a shared polygenic adaptive response to fishing using methods previously applied to evolve-and-resequence experiments. Cod populations on either side of the Atlantic show covariance in allele frequency change across the genome that are characteristic of recent polygenic adaptation. Using simulations, we demonstrate that the degree of covariance in allele frequency change observed in cod is unlikely to be explained by neutral processes or background selection. As human pressures on wild populations continue to increase, understanding and attributing modes of adaptation using methods similar to those demonstrated here will be important in identifying the capacity for adaptive responses and evolutionary rescue. This article is part of the theme issue 'Detecting and attributing the causes of biodiversity change: needs, gaps and solutions'.

The practice and promise of temporal genomics for measuring evolutionary responses to global change.

Understanding the evolutionary consequences of anthropogenic change is imperative for estimating long-term species resilience. While contemporary genomic data can provide us with important insights into recent demographic histories, investigating past change using present genomic data alone has limitations. In comparison, temporal genomics studies, defined herein as those that incorporate time series genomic data, utilize museum collections and repeated field sampling to directly examine evolutionary change. As temporal genomics is applied to more systems, species and questions, best practices can be helpful guides to make the most efficient use of limited resources. Here, we conduct a systematic literature review to synthesize the effects of temporal genomics methodology on our ability to detect evolutionary changes. We focus on studies investigating recent change within the past 200 years, highlighting evolutionary processes that have occurred during the past two centuries of accelerated anthropogenic pressure. We first identify the most frequently studied taxa, systems, questions and drivers, before highlighting overlooked areas where further temporal genomic studies may be particularly enlightening. Then, we provide guidelines for future study and sample designs while identifying key considerations that may influence statistical and analytical power. Our aim is to provide recommendations to a broad array of researchers interested in using temporal genomics in their work.

The sizes of life.

Recent research has revealed the diversity and biomass of life across ecosystems, but how that biomass is distributed across body sizes of all living things remains unclear. We compile the present-day global body size-biomass spectra for the terrestrial, marine, and subterranean realms. To achieve this compilation, we pair existing and updated biomass estimates with previously uncatalogued body size ranges across all free-living biological groups. These data show that many biological groups share similar ranges of body sizes, and no single group dominates size ranges where cumulative biomass is highest. We then propagate biomass and size uncertainties and provide statistical descriptions of body size-biomass spectra across and within major habitat realms. Power laws show exponentially decreasing abundance (exponent -0.9±0.02 S.D., R2 = 0.97) and nearly equal biomass (exponent 0.09±0.01, R2 = 0.56) across log size bins, which resemble previous aquatic size spectra results but with greater organismal inclusivity and global coverage. In contrast, a bimodal Gaussian mixture model describes the biomass pattern better (R2 = 0.86) and suggests small (~10-15 g) and large (~107 g) organisms outweigh other sizes by one order magnitude (15 and 65 Gt versus ~1 Gt per log size). The results suggest that the global body size-biomass relationships is bimodal, but substantial one-to-two orders-of-magnitude uncertainty mean that additional data will be needed to clarify whether global-scale universal constraints or local forces shape these patterns.

Isolation-by-distance and isolation-by-oceanography in Maroon Anemonefish (Amphiprion biaculeatus).

Obtaining dispersal estimates for a species is key to understanding local adaptation and population dynamics and to implementing conservation actions. Genetic isolation-by-distance (IBD) patterns can be used for estimating dispersal, and these patterns are especially useful for marine species in which few other methods are available. In this study, we genotyped coral reef fish (Amphiprion biaculeatus) at 16 microsatellite loci across eight sites across 210 km in the central Philippines to generate fine-scale estimates of dispersal. All sites except for one followed IBD patterns. Using IBD theory, we estimated a larval dispersal kernel spread of 8.9 km (95% confidence interval of 2.3-18.4 km). Genetic distance to the remaining site correlated strongly with the inverse probability of larval dispersal from an oceanographic model. Ocean currents were a better explanation for genetic distance at large spatial extents (sites greater than 150 km apart), while geographic distance remained the best explanation for spatial extents less than 150 km. Our study demonstrates the utility of combining IBD patterns with oceanographic simulations to understand connectivity in marine environments and to guide marine conservation strategies.

Simulation-Based Evaluation of Methods, Data Types, and Temporal Sampling Schemes for Detecting Recent Population Declines.

Understanding recent population trends is critical to quantifying species vulnerability and implementing effective management strategies. To evaluate the accuracy of genomic methods for quantifying recent declines (beginning <120 generations ago), we simulated genomic data using forward-time methods (SLiM) coupled with coalescent simulations (msprime) under a number of demographic scenarios. We evaluated both site frequency spectrum (SFS)-based methods (momi2, Stairway Plot) and methods that employ linkage disequilibrium information (NeEstimator, GONE) with a range of sampling schemes (contemporary-only samples, sampling two time points, and serial sampling) and data types (RAD-like data and whole-genome sequencing). GONE and momi2 performed best overall, with >80% power to detect severe declines with large sample sizes. Two-sample and serial sampling schemes could accurately reconstruct changes in population size, and serial sampling was particularly valuable for making accurate inferences when genotyping errors or minor allele frequency cutoffs distort the SFS or under model mis-specification. However, sampling only contemporary individuals provided reliable inferences about contemporary size and size change using either site frequency or linkage-based methods, especially when large sample sizes or whole genomes from contemporary populations were available. These findings provide a guide for researchers designing genomics studies to evaluate recent demographic declines.

Genetic decline and recovery of a demographically rebuilt fishery species.

The demographic history of a population is important for conservation and evolution, but this history is unknown for many populations. Methods that use genomic data have been developed to infer demography, but they can be challenging to implement and interpret, particularly for large populations. Thus, understanding if and when genetic estimates of demography correspond to true population history is important for assessing the performance of these genetic methods. Here, we used double-digest restriction-site associated DNA (ddRAD) sequencing data from archived collections of larval summer flounder (Paralichthys dentatus, n = 279) from three cohorts (1994-1995, 1997-1998 and 2008-2009) along the U.S. East coast to examine how contemporary effective population size and genetic diversity responded to changes in abundance in a natural population. Despite little to no detectable change in genetic diversity, coalescent-based demographic modelling from site frequency spectra revealed that summer flounder effective population size declined dramatically in the early 1980s. The timing and direction of change corresponded well with the observed decline in spawning stock census abundance in the late 1980s from independent fish surveys. Census abundance subsequently recovered and achieved the prebottleneck size. Effective population size also grew following the bottleneck. Our results for summer flounder demonstrate that genetic sampling and site frequency spectra can be useful for detecting population dynamics, even in species with large effective sizes.

The role of continental shelf bathymetry in shaping marine range shifts in the face of climate change.

As a consequence of anthropogenic climate change, marine species on continental shelves around the world are rapidly shifting deeper and poleward. However, whether these shifts deeper and poleward will allow species to access more, less, or equivalent amounts of continental shelf area and associated critical habitats remains unclear. By examining the proportion of seabed area at a range of depths for each large marine ecosystem (LME), we found that shelf area declined monotonically for 19% of LMEs examined. However, the majority exhibited a greater proportion of shelf area in mid-depths or across several depth ranges. By comparing continental shelf area across 2° latitudinal bands, we found that all coastlines exhibit multiple instances of shelf area expansion and contraction, which have the potential to promote or restrict poleward movement of marine species. Along most coastlines, overall shelf habitat increases or exhibits no significant change moving towards the poles. The exception is the Southern West Pacific, which experiences an overall loss of area with increasing latitude. Changes in continental shelf area availability across latitudes and depths are likely to affect the number of species local ecosystems can support. These geometric analyses help identify regions of conservation priority and ecological communities most likely to face attrition or expansion due to variations in available area.

Unifying climate change biology across realms and taxa.

A major challenge in modern biology is to understand extinction risk from climate change across all realms. Recent research has revealed that physiological tolerance, behavioral thermoregulation, and small elevation shifts are dominant coping strategies on land, whereas large-scale latitudinal shifts are more important in the ocean. Freshwater taxa may face the highest global extinction risks. Nevertheless, some species in each realm face similar risks because of shared adaptive, dispersal, or physiological tolerances and abilities. Taking a cross-realm perspective offers unique research opportunities because confounding physical factors in one realm are often disaggregated in another realm. Cross-realm, across taxa, and other forms of climate change biology synthesis are needed to advance our understanding of emergent patterns of risk across all life.

Assessing the potential for demographic restoration and assisted evolution to build climate resilience in coral reefs.

Interest is growing in developing conservation strategies to restore and maintain coral reef ecosystems in the face of mounting anthropogenic stressors, particularly climate warming and associated mass bleaching events. One such approach is to propagate coral colonies ex situ and transplant them to degraded reef areas to augment habitat for reef-dependent fauna, prevent colonization from spatial competitors, and enhance coral reproductive output. In addition to such "demographic restoration" efforts, manipulating the thermal tolerance of outplanted colonies through assisted relocation, selective breeding, or genetic engineering is being considered for enhancing rates of evolutionary adaptation to warming. Although research into such "assisted evolution" strategies has been growing, their expected performance remains unclear. We evaluated the potential outcomes of demographic restoration and assisted evolution in climate change scenarios using an eco-evolutionary simulation model. We found that supplementing reefs with pre-existing genotypes (demographic restoration) offers little climate resilience benefits unless input levels are large and maintained for centuries. Supplementation with thermally resistant colonies was successful at improving coral cover at lower input levels, but only if maintained for at least a century. Overall, we found that, although demographic restoration and assisted evolution have the potential to improve long-term coral cover, both approaches had a limited impact in preventing severe declines under climate change scenarios. Conversely, with sufficient natural genetic variance and time, corals could readily adapt to warming temperatures, suggesting that restoration approaches focused on building genetic variance may outperform those based solely on introducing heat-tolerant genotypes.

A long evolutionary reach for fishing nets.

Earlier maturation of Atlantic salmon is linked to indirect effects of fisheries on its prey.

Body size and food-web interactions mediate species range shifts under warming.

Species ranges are shifting in response to climate change, but most predictions disregard food-web interactions and, in particular, if and how such interactions change through time. Predator-prey interactions could speed up species range shifts through enemy release or create lags through biotic resistance. Here, we developed a spatially explicit model of interacting species, each with a thermal niche and embedded in a size-structured food-web across a temperature gradient that was then exposed to warming. We also created counterfactual single species models to contrast and highlight the effect of trophic interactions on range shifts. We found that dynamic trophic interactions hampered species range shifts across 450 simulated food-webs with up to 200 species each over 200 years of warming. All species experiencing dynamic trophic interactions shifted more slowly than single-species models would predict. In addition, the trailing edges of larger bodied species ranges shifted especially slowly because of ecological subsidies from small shifting prey. Trophic interactions also reduced the numbers of locally novel species, novel interactions and productive species, thus maintaining historical community compositions for longer. Current forecasts ignoring dynamic food-web interactions and allometry may overestimate species' tendency to track climate change.

A stark future for ocean life.

Model predicts a mass extinction event in the oceans if climate change is uncurbed.

Ocean warming alters the distributional range, migratory timing, and spatial protections of an apex predator, the tiger shark (Galeocerdo cuvier).

Given climate change threats to ecosystems, it is critical to understand the responses of species to warming. This is especially important in the case of apex predators since they exhibit relatively high extinction risk, and changes to their distribution could impact predator-prey interactions that can initiate trophic cascades. Here we used a combined analysis of animal tracking, remotely sensed environmental data, habitat modeling, and capture data to evaluate the effects of climate variability and change on the distributional range and migratory phenology of an ectothermic apex predator, the tiger shark (Galeocerdo cuvier). Tiger sharks satellite tracked in the western North Atlantic between 2010 and 2019 revealed significant annual variability in the geographic extent and timing of their migrations to northern latitudes from ocean warming. Specifically, tiger shark migrations have extended farther poleward and arrival times to northern latitudes have occurred earlier in the year during periods with anomalously high sea-surface temperatures. A complementary analysis of nearly 40 years of tiger shark captures in the region revealed decadal-scale changes in the distribution and timing of shark captures in parallel with long-term ocean warming. Specifically, areas of highest catch densities have progressively increased poleward and catches have occurred earlier in the year off the North American shelf. During periods of anomalously high sea-surface temperatures, movements of tracked sharks shifted beyond spatial management zones that had been affording them protection from commercial fishing and bycatch. Taken together, these study results have implications for fisheries management, human-wildlife conflict, and ecosystem functioning.