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.

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.

Greater vulnerability to warming of marine versus terrestrial ectotherms.

Understanding which species and ecosystems will be most severely affected by warming as climate change advances is important for guiding conservation and management. Both marine and terrestrial fauna have been affected by warming1,2 but an explicit comparison of physiological sensitivity between the marine and terrestrial realms has been lacking. Assessing how close populations live to their upper thermal limits has been challenging, in part because extreme temperatures frequently drive demographic responses3,4 and yet fauna can use local thermal refugia to avoid extremes5-7. Here we show that marine ectotherms experience hourly body temperatures that are closer to their upper thermal limits than do terrestrial ectotherms across all latitudes-but that this is the case only if terrestrial species can access thermal refugia. Although not a direct prediction of population decline, this thermal safety margin provides an index of the physiological stress caused by warming. On land, the smallest thermal safety margins were found for species at mid-latitudes where the hottest hourly body temperatures occurred; by contrast, the marine species with the smallest thermal safety margins were found near the equator. We also found that local extirpations related to warming have been twice as common in the ocean as on land, which is consistent with the smaller thermal safety margins at sea. Our results suggest that different processes will exacerbate thermal vulnerability across these two realms. Higher sensitivities to warming and faster rates of colonization in the marine realm suggest that extirpations will be more frequent and species turnover faster in the ocean. By contrast, terrestrial species appear to be more vulnerable to loss of access to thermal refugia, which would make habitat fragmentation and changes in land use critical drivers of species loss on land.

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.

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.

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic.

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.

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.

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.

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.

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.

Path-dependent institutions drive alternative stable states in conservation.

Understanding why some renewable resources are overharvested while others are conserved remains an important challenge. Most explanations focus on institutional or ecological differences among resources. Here, we provide theoretical and empirical evidence that conservation and overharvest can be alternative stable states within the same exclusive-resource management system because of path-dependent processes, including slow institutional adaptation. Surprisingly, this theory predicts that the alternative states of strong conservation or overharvest are most likely for resources that were previously thought to be easily conserved under optimal management or even open access. Quantitative analyses of harvest rates from 217 intensely managed fisheries supports the predictions. Fisheries' harvest rates also showed transient dynamics characteristic of path dependence, as well as convergence to the alternative stable state after unexpected transitions. This statistical evidence for path dependence differs from previous empirical support that was based largely on case studies, experiments, and distributional analyses. Alternative stable states in conservation appear likely outcomes for many cooperatively managed renewable resources, which implies that achieving conservation outcomes hinges on harnessing existing policy tools to navigate transitions.

Shape of species climate response curves affects community response to climate change.

Understanding how community composition is reshaped by changing climate is important for interpreting and predicting patterns of community assembly through time or across space. Community composition often does not perfectly correspond to expectations from current environmental conditions, leading to community-climate mismatches. Here, we combine data analysis and theory development to explore how species climate response curves affect the community response to climate change. We show that strong mismatches between community and climate can appear in the absence of demographic delays or limited species pools. Communities simulated using species response curves showed temporal changes of similar magnitude to those observed in natural communities of fishes and plankton, suggesting no overall delays in community change despite substantial unexplained variation from community assembly and other processes. Our approach can be considered as a null model that will be important to use when interpreting observed community responses to climate change and variability.

Persistence of a reef fish metapopulation via network connectivity: theory and data.

Determining metapopulation persistence requires understanding both demographic rates and patch connectivity. Persistence is well understood in theory but has proved challenging to test empirically for marine and other species with high connectivity that precludes classic colonisation-extinction dynamics. Here, we assessed persistence for a yellowtail anemonefish (Amphiprion clarkii) metapopulation using 7 years of annual sampling data along 30 km of coastline. We carefully accounted for uncertainty in demographic rates. Despite stable population abundances through time and sufficient production of surviving offspring for replacement, the pattern of connectivity made the metapopulation unlikely to persist in isolation and reliant on immigrants from outside habitat. To persist in isolation, the metapopulation would need higher fecundity or to retain essentially all recruits produced. This assessment of persistence in a marine metapopulation shows that stable abundance alone does not indicate persistence, emphasising the necessity of assessing both demographic and connectivity processes to understand metapopulation dynamics.

Resource availability and heterogeneity shape the self-organisation of regular spatial patterning.

Explaining large-scale ordered patterns and their effects on ecosystem functioning is a fundamental and controversial challenge in ecology. Here, we coupled empirical and theoretical approaches to explore how competition and spatial heterogeneity govern the regularity of colony dispersion in fungus-farming termites. Individuals from different colonies fought fiercely, and inter-nest distances were greater when nests were large and resources scarce-as expected if competition is strong, large colonies require more resources and foraging area scales with resource availability. Building these principles into a model of inter-colony competition showed that highly ordered patterns emerged under high resource availability and low resource heterogeneity. Analysis of this dynamical model provided novel insights into the mechanisms that modulate pattern regularity and the emergent effects of these patterns on system-wide productivity. Our results show how environmental context shapes pattern formation by social-insect ecosystem engineers, which offers one explanation for the marked variability observed across ecosystems.

Genomic signatures of spatially divergent selection at clownfish range margins.

Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, Amphiprion clarkii, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations.

Host gene expression in wildlife disease: making sense of species-level responses.

Emerging infectious diseases are significant threats to wildlife conservation, yet the impacts of pathogen exposure and infection can vary widely among host species. As such, conservation biologists and disease ecologists have increasingly aimed to understand species-specific host susceptibility using molecular methods. In particular, comparative gene expression assays have been used to contrast the transcriptomic responses of disease-resistant and disease-susceptible hosts to pathogen exposure. This work usually assumes that the gene expression responses of disease-resistant species will reveal the activation of molecular pathways contributing to host defence. However, results often show that disease-resistant hosts undergo little gene expression change following pathogen challenge. Here, we discuss the mechanistic implications of these "null" findings and offer methodological suggestions for future molecular studies of wildlife disease. First, we highlight that muted transcriptomic responses with minimal immune system recruitment may indeed be protective for nonsusceptible hosts if they limit immunopathology and promote pathogen tolerance in systems where susceptible hosts suffer from genetic dysregulation. Second, we argue that overly narrow investigation of responses to pathogen exposure may overlook important, constitutively active molecular pathways that underlie species-specific defences. Finally, we outline alternative study designs and approaches that complement interspecific transcriptomic comparisons, including intraspecific gene expression studies and genomic methods to detect signatures of selection. Collectively, these insights will help ecologists extract maximal information from conservation-relevant transcriptomic data sets, leading to a deeper understanding of host defences and, ultimately, the implementation of successful conservation interventions.

Genomic signatures of selection in bats surviving white-nose syndrome.

Rapid evolution of advantageous traits following abrupt environmental change can help populations recover from demographic decline. However, for many introduced diseases affecting longer-lived, slower reproducing hosts, mortality is likely to outpace the acquisition of adaptive de novo mutations. Adaptive alleles must therefore be selected from standing genetic variation, a process that leaves few detectable genomic signatures. Here, we present whole genome evidence for selection in bat populations that are recovering from white-nose syndrome (WNS). We collected samples both during and after a WNS-induced mass mortality event in two little brown bat populations that are beginning to show signs of recovery and found signatures of soft sweeps from standing genetic variation at multiple loci throughout the genome. We identified one locus putatively under selection in a gene associated with the immune system. Multiple loci putatively under selection were located within genes previously linked to host response to WNS as well as to changes in metabolism during hibernation. Results from two additional populations suggested that loci under selection may differ somewhat among populations. Through these findings, we suggest that WNS-induced selection may contribute to genetic resistance in this slowly reproducing species threatened with extinction.

Quantifying dispersal variability among nearshore marine populations.

Dispersal drives diverse processes from population persistence to community dynamics. However, the amount of temporal variation in dispersal and its consequences for metapopulation dynamics is largely unknown for organisms with environmentally driven dispersal (e.g., many marine larvae, arthropods and plant seeds). Here, we used genetic parentage analysis to detect larval dispersal events in a common coral reef fish, Amphiprion clarkii, along 30 km of coastline consisting of 19 reef patches in Ormoc Bay, Leyte, Philippines. We quantified variation in the dispersal kernel across seven years (2012-2018) and monsoon seasons with 71 parentage assignments from 791 recruits and 1,729 adults. Connectivity patterns differed significantly among years and seasons in the scale and shape but not in the direction of dispersal. This interannual variation in dispersal kernels introduced positive temporal covariance among dispersal routes that theory predicts is likely to reduce stochastic metapopulation growth rates below the growth rates expected from only a single or a time-averaged connectivity estimate. The extent of variation in mean dispersal distance observed here among years is comparable in magnitude to the differences across reef fish species. Considering dispersal variation will be an important avenue for further metapopulation and metacommunity research across diverse taxa.

Evolution and connectivity influence the persistence and recovery of coral reefs under climate change in the Caribbean, Southwest Pacific, and Coral Triangle.

Corals are experiencing unprecedented decline from climate change-induced mass bleaching events. Dispersal not only contributes to coral reef persistence through demographic rescue but can also hinder or facilitate evolutionary adaptation. Locations of reefs that are likely to survive future warming therefore remain largely unknown, particularly within the context of both ecological and evolutionary processes across complex seascapes that differ in temperature range, strength of connectivity, network size, and other characteristics. Here, we used eco-evolutionary simulations to examine coral adaptation to warming across reef networks in the Caribbean, the Southwest Pacific, and the Coral Triangle. We assessed the factors associated with coral persistence in multiple reef systems to understand which results are general and which are sensitive to particular geographic contexts. We found that evolution can be critical in preventing extinction and facilitating the long-term recovery of coral communities in all regions. Furthermore, the strength of immigration to a reef (destination strength) and current sea surface temperature robustly predicted reef persistence across all reef networks and across temperature projections. However, we found higher initial coral cover, slower recovery, and more evolutionary lag in the Coral Triangle, which has a greater number of reefs and more larval settlement than the other regions. We also found the lowest projected future coral cover in the Caribbean. These findings suggest that coral reef persistence depends on ecology, evolution, and habitat network characteristics, and that, under an emissions stabilization scenario (RCP 4.5), recovery may be possible over multiple centuries.