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To support conservation practices, societal demand for understanding fundamental coastal ocean ecosystem mechanisms has grown in recent decades. Globally, these regions are among the world’s most productive, but they are highly vulnerable to extractive and non-extractive stresses. In 1999, we established the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO) to perform basic and use-inspired, long-term ecological research at local to large marine ecosystem (LME) scales. Coordinated investigations of ecosystem patterns and dynamics focused on nearshore coastal waters and hard-bottom habitats (rocky intertidal and kelp forests) in the California Current Large Marine Ecosystem. Communicating relevant scientific discoveries to inform decision-making was an integral component, as was commitment to training new generations of interdisciplinary marine scientists, thereby building scientific capacity and expertise in marine conservation science and policy. Issues of climate change and ocean acidification, wildlife disease outbreaks, oil spills, and conservation strategies such as marine protected areas have spotlighted the immense value of long-term monitoring and research at the LME scale. Here, we reflect on PISCO’s approach and progress in linking science, conservation, management, and policy using 20 years of experience in the formation and operation of this research network.

In many animals, the germline differentiates early in embryogenesis, so only mutations that accumulate in germ cells are inherited by offspring. Exceptions to this developmental process may indicate other mechanisms have evolved to limit the effects of deleterious mutation accumulation. Stony corals are animals that can live for hundreds of years and have been thought to produce gametes from somatic tissue. To clarify conflicting evidence about germline-soma distinction in corals, we sequenced high coverage, full genomes with technical replicates for parent coral branches and their sperm pools. We identified post-embryonic single nucleotide variants (SNVs) unique to each parent branch, then checked if each SNV was shared by the respective sperm pool. Twenty-six per cent of post-embryonic SNVs were shared by the sperm and 74% were not. We also identified germline SNVs, those that were present in the sperm but not in the parent. These data suggest that self-renewing stem cells differentiate into germ and soma throughout the adult life of the colony, with SNV rates and patterns differing markedly in stem, soma and germ lineages. In addition to informing the evolution of germlines in metazoans, these insights inform how corals may generate adaptive diversity necessary in the face of global climate change.

The ability of local populations to adapt to future climate conditions is facilitated by a balance between short range dispersal allowing local buildup of adaptively beneficial alleles, and longer dispersal moving these alleles throughout the species range. Reef building corals have relatively low dispersal larvae, but most population genetic studies show differentiation only over 100s of km. Here, we report full mitochondrial genome sequences from 284 tabletop corals ( Acropora hyacinthus ) from 39 patch reefs in Palau, and show two signals of genetic structure across reef scales from 1 to 55 km. First, divergent mitochondrial DNA haplotypes exist in different proportions from reef to reef, causing Phi ST values of 0.02 ( p  = 0.02). Second, closely related sequences of mitochondrial Haplogroups are more likely to be co-located on the same reefs than expected by chance alone. We also compared these sequences to prior data on 155 colonies from American Samoa. In these comparisons, many Haplogroups in Palau were disproportionately represented or absent in American Samoa, and inter-regional Phi ST  = 0.259. However, we saw three instances of identical mitochondrial genomes between locations. Together, these data sets suggest two features of coral dispersal revealed by occurrence patterns in highly similar mitochondrial genomes. First, the Palau-American Samoa data suggest that long distance dispersal in corals is rare, as expected, but that it is common enough to deliver identical mitochondrial genomes across the Pacific. Second, higher than expected co-occurrence of Haplogroups on the same Palau reefs suggests greater retention of coral larvae on local reefs than predicted by many current oceanographic models of larval movement. Increased attention to local scales of coral genetic structure, dispersal, and selection may help increase the accuracy of models of future adaptation of corals and of assisted migration as a reef resilience intervention., Competing Interests: The authors declare no conflict of interests., (© 2023 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.)

The prevalence of global coral bleaching has focused much attention on the possibility of interventions to increase heat resistance. However, if high heat resistance is linked to fitness tradeoffs that may disadvantage corals in other areas, then a more holistic view of heat resilience may be beneficial. In particular, overall resilience of a species to heat stress is likely to be the product of both resistance to heat and recovery from heat stress. Here, we investigate heat resistance and recovery among individual Acropora hyacinthus colonies in Palau. We divided corals into low, moderate, and high heat resistance categories based on the number of days (4-9) needed to reach significant pigmentation loss due to experimental heat stress. Afterward, we deployed corals back onto a reef in a common garden 6-month recovery experiment that monitored chlorophyll a , mortality, and skeletal growth. Heat resistance was negatively correlated with mortality during early recovery (0-1 month) but not late recovery (4-6 months), and chlorophyll a concentration recovered in heat-stressed corals by 1-month postbleaching. However, moderate-resistance corals had significantly greater skeletal growth than high-resistance corals by 4 months of recovery. High- and low-resistance corals on average did not exhibit skeletal growth within the observed recovery period. These data suggest complex tradeoffs may exist between coral heat resistance and recovery and highlight the importance of incorporating multiple aspects of resilience into future reef management programs., Competing Interests: On behalf of all authors, the corresponding author states that there is no conflict of interest., (© 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.)

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., (© 2022 The Authors. Ecological Applications published by Wiley Periodicals LLC on behalf of The Ecological Society of America.)

Widespread mapping of coral thermal resilience is essential for developing effective management strategies and requires replicable and rapid multi-location assays of heat resistance and recovery. One- or two-day short-term heat stress experiments have been previously employed to assess heat resistance, followed by single assays of bleaching condition. We tested the reliability of short-term heat stress resistance, and linked resistance and recovery assays, by monitoring the phenotypic response of fragments from 101 Acropora hyacinthus colonies located in Palau (Micronesia) to short-term heat stress. Following short-term heat stress, bleaching and mortality were recorded after 16 hours, daily for seven days, and after one and two months of recovery. To follow corals over time, we utilized a qualitative, non-destructive visual bleaching score metric that correlated with standard symbiont retention assays. The bleaching state of coral fragments 16 hours post-heat stress was highly indicative of their state over the next 7 days, suggesting that symbiont population sizes within corals may quickly stabilize post-heat stress. Bleaching 16 hours post-heat stress predicted likelihood of mortality over the subsequent 3-5 days, after which there was little additional mortality. Together, bleaching and mortality suggested that rapid assays of the phenotypic response following short-term heat stress were good metrics of the total heat treatment effect. Additionally, our data confirm geographic patterns of intraspecific variation in Palau and show that bleaching severity among colonies was highly correlated with mortality over the first week post-stress. We found high survival (98%) and visible recovery (100%) two months after heat stress among coral fragments that survived the first week post-stress. These findings help simplify rapid, widespread surveys of heat sensitivity in Acropora hyacinthus by showing that standardized short-term experiments can be confidently assayed after 16 hours, and that bleaching sensitivity may be linked to subsequent survival using experimental assessments., Competing Interests: The authors have declared that no competing interests exist.

The pervasive loss of biodiversity in the Anthropocene necessitates rapid assessments of ecosystems to understand how they will respond to anthropogenic environmental change. Many studies have sought to describe the adaptive capacity (AC) of individual species, a measure that encompasses a species' ability to respond and adapt to change. Only those adaptive mechanisms that can be used over the next few decades (e.g. via novel interactions, behavioural changes, hybridization, migration, etc.) are relevant to the timescale set by the rapid changes of the Anthropocene. The impacts of species loss cascade through ecosystems, yet few studies integrate the capacity of ecological networks to adapt to change with the ACs of its species. Here, we discuss three ecosystems and how their ecological networks impact the AC of species and vice versa. A more holistic perspective that considers the AC of species with respect to their ecological interactions and functions will provide more predictive power and a deeper understanding of what factors are most important to a species' survival. We contend that the AC of a species, combined with its role in ecosystem function and stability, must guide decisions in assigning 'risk' and triaging biodiversity loss in the Anthropocene. This article is part of the theme issue 'Ecological complexity and the biosphere: the next 30 years'.

Recent warm temperatures driven by climate change have caused mass coral bleaching and mortality across the world, prompting managers, policymakers, and conservation practitioners to embrace restoration as a strategy to sustain coral reefs. Despite a proliferation of new coral reef restoration efforts globally and increasing scientific recognition and research on interventions aimed at supporting reef resilience to climate impacts, few restoration programs are currently incorporating climate change and resilience in project design. As climate change will continue to degrade coral reefs for decades to come, guidance is needed to support managers and restoration practitioners to conduct restoration that promotes resilience through enhanced coral reef recovery, resistance, and adaptation. Here, we address this critical implementation gap by providing recommendations that integrate resilience principles into restoration design and practice, including for project planning and design, coral selection, site selection, and broader ecosystem context. We also discuss future opportunities to improve restoration methods to support enhanced outcomes for coral reefs in response to climate change. As coral reefs are one of the most vulnerable ecosystems to climate change, interventions that enhance reef resilience will help to ensure restoration efforts have a greater chance of success in a warming world. They are also more likely to provide essential contributions to global targets to protect natural biodiversity and the human communities that rely on reefs., (© 2022 Commonwealth of Australia. Global Change Biology published by John Wiley & Sons Ltd.)

At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterizing the mechanisms of coral resilience to climate change. To explore these mechanisms in the reef coral Acropora tenuis , we collected samples from lagoon and reef slope habitats and combined whole-genome sequencing, ITS2 metabarcoding, experimental heat stress, and transcriptomics. Despite high gene flow across the atoll, we identified clear shifts in allele frequencies between habitats at relatively small linked genomic islands. Common garden heat stress assays showed corals from the lagoon to be more resistant to bleaching, and RNA sequencing revealed marked differences in baseline levels of gene expression between habitats. Our results provide new insight into the complex mechanisms of coral resilience to climate change and highlight the potential for spatially varying selection across complex coral reef seascapes to drive pronounced ecological divergence in climate-related traits.

Reef-building coral species are experiencing an unprecedented decline owing to increasing frequency and intensity of marine heatwaves and associated bleaching-induced mortality. Closely related species from the Acropora hyacinthus species complex differ in heat tolerance and in their association with heat-tolerant symbionts. We used low-coverage full genome sequencing of 114 colonies monitored across the 2015 bleaching event in American Samoa to determine the genetic differences among four cryptic species (termed HA, HC, HD and HE) that have diverged in these species traits. Cryptic species differed strongly at thousands of single nucleotide polymorphisms across the genome which are enriched for amino acid changes in the bleaching-resistant species HE. In addition, HE also showed two particularly divergent regions with strong signals of differentiation. One approximately 220 kb locus, HES1, contained the majority of fixed differences in HE. A second locus, HES2, was fixed in HE but polymorphic in the other cryptic species. Surprisingly, non-HE individuals with HE-like haplotypes at HES2 were more likely to bleach. At both loci, HE showed particular sequence similarity to a congener, Acropora millepora . Overall, resilience to bleaching during the third global bleaching event was strongly structured by host cryptic species, buoyed by differences in symbiont associations between these species.

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., (© 2021 The Authors. Global Change Biology published by John Wiley & Sons Ltd.)

Climate change is dramatically changing ecosystem composition and productivity, leading scientists to consider the best approaches to map natural resistance and foster ecosystem resilience in the face of these changes. Here, we present results from a large-scale experimental assessment of coral bleaching resistance, a critical trait for coral population persistence as oceans warm, in 221 colonies of the coral Acropora hyacinthus across 37 reefs in Palau. We find that bleaching-resistant individuals inhabit most reefs but are found more often in warmer microhabitats. Our survey also found wide variation in symbiont concentration among colonies, and that colonies with lower symbiont load tended to be more bleaching-resistant. By contrast, our data show that low symbiont load comes at the cost of lower growth rate, a tradeoff that may operate widely among corals across environments. Corals with high bleaching resistance have been suggested as a source for habitat restoration or selective breeding in order to increase coral reef resilience to climate change. Our maps show where these resistant corals can be found, but the existence of tradeoffs with heat resistance may suggest caution in unilateral use of this one trait in restoration., Competing Interests: BC, KA, NW, ML, VN, YG, SP none, (© 2021, Cornwell et al.)

DNA metabarcoding has been increasingly used to detail distributions of hundreds of species. Most analyses focus on creating molecular operational taxonomic units (MOTUs) from complex mixtures of DNA sequences, but much less common is use of the sequence diversity within these MOTUs. Here we use the diversity of COI haplotypes within MOTUs from a California kelp forest to infer patterns of population abundance, dispersal and population history from 527 species of animals and algae from 106 samples of benthic habitats in Monterey Bay. Using haplotypes as a unit we show fine-grained differences of abundance across locations for 15 species, and marked aggregation from sample to sample for most of the common species of plants and animals. Previous analyses could not distinguish these patterns from artefacts of amplification or sequence bias. Our haplotype data also reveal strong population genetic differentiation over small spatial scales for 48 species of red algae, sponges and Bryozoa. Last, phylogenetic analysis of mismatch frequencies among haplotypes show a wide variety of demographic histories from recent expansions to long, stable population sizes. These analyses show that abundant, small-bodied marine species that are often overlooked in ecological surveys can have strikingly different patterns of ecological and genetic structure leading to population, ecological and perhaps adaptive differences between habitats. MOTU diversity data from the same sequencing efforts that generate species-level analyses can greatly increase the scope and value of metabarcoding studies., (© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Global environmental change is challenging species with novel conditions, such that demographic and evolutionary trajectories of populations are often shaped by the exchange of organisms and alleles across landscapes. Current ecological theory predicts that random networks with dispersal shortcuts connecting distant sites can promote persistence when there is no capacity for evolution. Here, we show with an eco-evolutionary model that dispersal shortcuts across environmental gradients instead hinder persistence for populations that can evolve because long-distance migrants bring extreme trait values that are often maladaptive, short-circuiting the adaptive response of populations to directional change. Our results demonstrate that incorporating evolution and environmental heterogeneity fundamentally alters theoretical predictions regarding persistence in ecological networks., (© 2021 The Authors. Ecology published by Wiley Periodicals LLC on behalf of Ecological Society of America.)

High pCO 2 habitats and their populations provide an unparalleled opportunity to assess how species may survive under future ocean acidification conditions, and help to reveal the traits that confer tolerance. Here we utilize a unique CO 2 vent system to study the effects of exposure to elevated pCO2 on trait-shifts observed throughout natural populations of Astroides calycularis, an azooxanthellate scleractinian coral endemic to the Mediterranean. Unexpected shifts in skeletal and growth patterns were found. Colonies shifted to a skeletal phenotype characterized by encrusting morphology, smaller size, reduced coenosarc tissue, fewer polyps, and less porous and denser skeletons at low pH. Interestingly, while individual polyps calcified more and extended faster at low pH, whole colonies found at low pH site calcified and extended their skeleton at the same rate as did those at ambient pH sites. Transcriptomic data revealed strong genetic differentiation among local populations of this warm water species whose distribution range is currently expanding northward. We found excess differentiation in the CO 2 vent population for genes central to calcification, including genes for calcium management (calmodulin, calcium-binding proteins), pH regulation (V-type proton ATPase), and inorganic carbon regulation (carbonic anhydrase). Combined, our results demonstrate how coral populations can persist in high pCO 2 environments, making this system a powerful candidate for investigating acclimatization and local adaptation of organisms to global environmental change., (© 2020 John Wiley & Sons Ltd.)

Progress in global shark conservation has been limited by constraints to understanding the species composition and geographic origins of the shark fin trade. Previous assessments that relied on earlier genetic techniques and official trade records focused on abundant pelagic species traded between Europe and Asia. Here, we combine recent advances in DNA barcoding and species distribution modelling to identify the species and source the geographic origin of fins sold at market. Derived models of species environmental niches indicated that shark fishing effort is concentrated within Exclusive Economic Zones, mostly in coastal Australia, Indonesia, the United States, Brazil, Mexico and Japan. By coupling two distinct tools, barcoding and niche modelling, our results provide new insights for monitoring and enforcement. They suggest stronger local controls of coastal fishing may help regulate the unsustainable global trade in shark fins.

The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome-wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides ( Menidia menidia ) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low-coverage, whole-transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome-wide differentiation (median F ST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed ( F ST  > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in these LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change., (© 2020 The Authors. Evolution Letters published by Wiley Periodicals, LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB).)

One challenge for multicellular organisms is maintaining genome stability in the face of mutagens across long life spans. Imperfect genome maintenance leads to mutation accumulation in somatic cells, which is associated with tumors and senescence in vertebrates. Colonial reef-building corals are often large, can live for hundreds of years, rarely develop recognizable tumors, and are thought to convert somatic cells into gamete producers, so they are a pivotal group in which to understand long-term genome maintenance. To measure rates and patterns of somatic mutations, we analyzed transcriptomes from 17 to 22 branches from each of four Acropora hyacinthus colonies, determined putative single nucleotide variants, and verified them with Sanger resequencing. Unlike for human skin carcinomas, there is no signature of mutations caused by UV damage, indicating either higher efficiency of repair than in vertebrates, or strong sunscreen protection in these shallow water tropical animals. The somatic mutation frequency per nucleotide in A. hyacinthus is on the same order of magnitude (10-7) as noncancerous human somatic cells, and accumulation of mutations with age is similar. Loss of heterozygosity variants outnumber gain of heterozygosity mutations ∼2:1. Although the mutation frequency is similar in mammals and corals, the preponderance of loss of heterozygosity changes and potential selection may reduce the frequency of deleterious mutations in colonial animals like corals. This may limit the deleterious effects of somatic mutations on the coral organism as well as potential offspring., (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Kelp forest ecosystems dominate 150,000 km of global temperate coastline, rivalling the coastal occurrence of coral reefs. Despite the astounding biological diversity and productive ecological communities associated with kelp forests, patterns of species richness and composition are difficult to monitor and compare. Crustose coralline algae are a critically important substrate for propagule settlement for a range of kelp forest species. Coralline-covered cobbles are home to hundreds of species of benthic animals and algae and form a replicable unit for ecological assays. Here, we use DNA metabarcoding of bulk DNA extracts sampled from cobbles to explore patterns of species diversity in kelp forests of the central California coast. The data from 97 cobbles within kelp forest ecosystems at three sites in Central California show the presence of 752 molecular operational taxonomic units (MOTUs) and 53 MOTUs assigned up to the species level with >95% similarity to current databases. We are able to detect spatial patterns of important management targets such as abalone recruits, and localized abundance of sea stars in 2012. Comparison of classic ecological surveys of these sites reveals large differences in species targets for these two approaches. In order to make such comparisons more quantitative, we use Presence/Absence Metabarcoding, using the fraction of replicate cobbles showing a species as a measure of its local abundance. This approach provides a fast and repeatable survey method that can be applied for biodiversity assessments across systems to shed light on the impact of different ecological disturbances and the role played by marine protected areas., (© 2019 John Wiley & Sons Ltd.)

Humans cause widespread evolutionary change in nature, but we still know little about the genomic basis of rapid adaptation in the Anthropocene. We tracked genomic changes across all protein-coding genes in experimental fish populations that evolved pronounced shifts in growth rates due to size-selective harvest over only four generations. Comparisons of replicate lines show parallel allele frequency shifts that recapitulate responses to size-selection gradients in the wild across hundreds of unlinked variants concentrated in growth-related genes. However, a supercluster of genes also rose rapidly in frequency and dominated the evolutionary dynamic in one replicate line but not in others. Parallel phenotypic changes thus masked highly divergent genomic responses to selection, illustrating how contingent rapid adaptation can be in the face of strong human-induced selection., (Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

As climate change progresses and extreme temperature events increase in frequency, rates of disturbance may soon outpace the capacity of certain species of reef-building coral to recover from bleaching. This may lead to dramatic shifts in community composition and ecosystem function. Understanding variation in rates of bleaching recovery among species and how that translates to resilience to recurrent bleaching is fundamental to predicting the impacts of increasing disturbances on coral reefs globally. We tracked the response of two heat sensitive species in the genus Acropora to repeated bleaching events during the austral summers of 2015 and 2017. Despite a similar bleaching response, the species Acropora gemmifera recovered faster based on transcriptome-wide gene expression patterns and had a more dynamic algal symbiont community than Acropora hyacinthus growing on the same reef. Moreover, A. gemmifera had higher survival to repeated heat extremes, with six-fold lower mortality than A. hyacinthus. These patterns suggest that speed of recovery from a first round of bleaching, based on multiple mechanisms, contributes strongly to sensitivity to a second round of bleaching. Furthermore, our data uncovered intragenus variation in a group of corals thought generally to be heat-sensitive and therefore paint a more nuanced view of the future health of coral reef ecosystems against a backdrop of increasing thermal disturbances., (© 2019 John Wiley & Sons Ltd.)

Moderate- to high-density genotyping (100 + SNPs) is widely used to determine and measure individual identity, relatedness, fitness, population structure and migration in wild populations.However, these important tools are difficult to apply when high-quality genetic material is unavailable. Most genomic tools are developed for high-quality DNA sources from laboratory or medical settings. As a result, most genetic data from market or field settings is limited to easily amplified mitochondrial DNA or a few microsatellites.To enable genotyping in conservation contexts, we used next-generation sequencing of multiplex PCR products from very low-quality DNA extracted from faeces, hair and cooked samples. We demonstrated utility and wide-ranging potential application in endangered wild tigers and tracking commercial trade in Caribbean queen conch.We genotyped 100 SNPs from degraded tiger samples to identify individuals, discern close relatives and detect population differentiation. Co-occurring carnivores do not amplify (e.g. Indian wild dog/dhole) or are monomorphic (e.g. leopard). Sixty-two SNPs from conch fritters and field-collected samples were used to test relatedness and detect population structure.We provide proof of concept for a rapid, simple, cost-effective and scalable method (for both samples and number of loci), a framework that can be applied to other conservation scenarios previously limited by low-quality DNA samples. These approaches provide a critical advance for wildlife monitoring and forensics, open the door to field-ready testing, and will strengthen the use of science in policy decisions and wildlife trade., Competing Interests: CONFLICT OF INTEREST R.W.T. and End2End Genomics L.L.C. received NIH small business funding (R43HG009482) to develop tools to study non-model species.

Ecological restoration of forests, meadows, reefs, or other foundational ecosystems during climate change depends on the discovery and use of individuals able to withstand future conditions. For coral reefs, climate-tolerant corals might not remain tolerant in different environments because of widespread environmental adjustment of coral physiology and symbionts. Here, we test if parent corals retain their heat tolerance in nursery settings, if simple proxies predict successful colonies, and if heat-tolerant corals suffer lower growth or survival in normal settings. Before the 2015 natural bleaching event in American Samoa, we set out 800 coral fragments from 80 colonies of four species selected by prior tests to have a range of intraspecific natural heat tolerance. After the event, nursery stock from heat-tolerant parents showed two to three times less bleaching across species than nursery stock from less tolerant parents. They also retained higher individual genetic diversity through the bleaching event than did less heat-tolerant corals. The three best proxies for thermal tolerance were response to experimental heat stress, location on the reef, and thermal microclimate. Molecular biomarkers were also predictive but were highly species specific. Colony genotype and symbiont genus played a similarly strong role in predicting bleaching. Combined, our results show that selecting for host and symbiont resilience produced a multispecies coral nursery that withstood multiple bleaching events, that proxies for thermal tolerance in restoration can work across species and be inexpensive, and that different coral clones within species reacted very differently to bleaching., Competing Interests: The authors declare no conflict of interest., (Copyright © 2019 the Author(s). Published by PNAS.)

Closely related species often show substantial differences in ecological traits that allow them to occupy different environmental niches. For few of these systems is it clear what the genomic basis of adaptation is and whether a few loci of major effect or many genome-wide differences drive species divergence. Four cryptic species of the tabletop coral Acropora hyacinthus are broadly sympatric in American Samoa; here we show that two common species have differences in key environmental traits such as microhabitat distributions and thermal stress tolerance. We compared gene expression patterns and genetic polymorphism between these two species using RNA-Seq. The vast majority of polymorphisms are shared between species, but the two species show widespread differences in allele frequencies and gene expression, and tend to host different symbiont types. We find that changes in gene expression are related to changes in the frequencies of many gene regulatory variants, but that many of these differences are consistent with the action of genetic drift. However, we observe greater genetic divergence between species in amino acid replacement polymorphisms compared to synonymous variants. These findings suggest that polygenic evolution plays a major role in driving species differences in ecology and resilience to climate change., (© 2017 The Author(s). Evolution © 2017 The Society for the Study of Evolution.)

Population genomic surveys suggest that climate-associated genetic variation occurs widely across species, but whether it is sufficient to allow population persistence via evolutionary adaptation has seldom been quantified. To ask whether rapid adaptation in reef-building corals can keep pace with future ocean warming, we measured genetic variation at predicted warm-adapted loci and simulated future evolution and persistence in a high-latitude population of corals from Rarotonga, Cook Islands. Alleles associated with thermal tolerance were present but at low frequencies in this cooler, southerly locality. Simulations based on predicted ocean warming in Rarotonga showed rapid evolution of heat tolerance resulting in population persistence under mild warming scenarios consistent with low CO 2 emission plans, RCP2.6 and RCP4.5. Under more severe scenarios, RCP6.0 and RCP8.5, adaptation was not rapid enough to prevent extinction. Population adaptation was faster for models based on smaller numbers of additive loci that determine thermal tolerance and for higher population growth rates. Finally, accelerated migration via transplantation of thermally tolerant individuals (1 to 5%/year) sped adaptation. These results show that cool-water corals can adapt to warmer oceans but only under mild scenarios resulting from international emissions controls. Incorporation of genomic data into models of species response to climate change offers a promising method for estimating future adaptive processes.

Ecological damage from periodic environmental extremes is often repaired in resilient ecosystems, but the rate of return to a non-damaged state is critical. Measures of recovery of communities include biomass, productivity and diversity, while measures of recovery of individuals tend to focus on physiological conditions and the return to normal metabolic functioning. Transcriptomics offers a window into the entire physiology of the organism under stress and can represent a holistic view of organismal recovery. In this study, we track the recovery of seven colonies of Acropora hyacinthus following a natural bleaching event. We identified a large environmental stress response in the field that involved approximately 20% of the host transcriptome. The transcriptome remained largely perturbed for at least six months after temperatures had cooled and four months after symbiont populations had recovered. Moreover, a small set of genes did not recover to previous expression levels even 12 months after the event, about the time that normal growth rates resumed. This study is among the first to incorporate transcriptomics into a longitudinal dataset of recovery from environmental stress. The data demonstrate large and lasting effects on coral physiology long after environmental conditions return to normal and symbiont populations recover., (© 2017 The Author(s).)

Ocean acidification (OA) increasingly threatens marine systems, and is especially harmful to calcifying organisms. One important question is whether OA will alter species interactions. Crustose coralline algae (CCA) provide space and chemical cues for larval settlement. CCA have shown strongly negative responses to OA in previous studies, including disruption of settlement cues to corals. In California, CCA provide cues for seven species of harvested, threatened, and endangered abalone. We exposed four common CCA genera and a crustose calcifying red algae, Peyssonnelia (collectively CCRA) from California to three pCO 2 levels ranging from 419-2,013 µatm for four months. We then evaluated abalone (Haliotis rufescens) settlement under ambient conditions among the CCRA and non-algal controls that had been previously exposed to the pCO 2 treatments. Abalone settlement and metamorphosis increased from 11% in the absence of CCRA to 45-69% when CCRA were present, with minor variation among CCRA genera. Though all CCRA genera reduced growth during exposure to increased pCO 2 , abalone settlement was unaffected by prior CCRA exposure to increased pCO 2 . Thus, we find no impacts of OA exposure history on CCRA provision of settlement cues. Additionally, there appears to be functional redundancy in genera of CCRA providing cues to abalone, which may further buffer OA effects.

Competing Interests: The authors declare no conflict of interest.

Coral reefs support immense biodiversity and provide important ecosystem services to many millions of people. Yet reefs are degrading rapidly in response to numerous anthropogenic drivers. In the coming centuries, reefs will run the gauntlet of climate change, and rising temperatures will transform them into new configurations, unlike anything observed previously by humans. Returning reefs to past configurations is no longer an option. Instead, the global challenge is to steer reefs through the Anthropocene era in a way that maintains their biological functions. Successful navigation of this transition will require radical changes in the science, management and governance of coral reefs.

Concern over rapid environmental shifts associated with climate change has led to a search for molecular markers of environmental tolerance. Climate-associated gene expression profiles exist for a number of systems, but have rarely been tied to fitness outcomes, especially in nonmodel organisms. We reciprocally transplanted corals between two backreef locations with more and less variable temperature regimes to disentangle effects of recent and native environment on survival and growth. Coral growth over 12 months was largely determined by local environment. Survival, however, was impacted by native environment; corals from the more variable environment had 22% higher survivorship. By contrast, corals native to the less variable environment had more variable survival. This might represent a "selective sieve" where poor survivors are filtered from the more stressful environment. We also find a potential fitness trade-off-corals with high survival under stressful conditions grew less in the more benign environment. Transcriptome samples taken a year before transplantation were used to examine gene expression patterns that predicted transplant survival and growth. Two separate clusters of coexpressed genes were predictive of survival in the two locations. Genes from these clusters are candidate biomarkers for predicting persistence of corals under future climate change scenarios.

Previous transcriptional studies in heat-stressed corals have shown that many genes are responsive to generalized heat stress whereas the expression patterns of specific gene networks after heat stress show strong correlations with variation in bleaching outcomes. However, where these specific genes are expressed is unknown. In this study, we employed in situ hybridization to identify patterns of spatial gene expression of genes previously predicted to be involved in general stress response and bleaching. We found that tumor necrosis factor receptors (TNFRs), known to be strong responders to heat stress, were not expressed in gastrodermal symbiont-containing cells but were widely expressed in specific cells of the epidermal layer. The transcription factors AP-1 and FosB, implicated as early signals of heat stress, were widely expressed throughout the oral gastrodermis and epidermis. By contrast, a G protein-coupled receptor gene (GPCR) and a fructose bisphosphate aldolase C gene (aldolase), previously implicated in bleaching, were expressed in symbiont-containing gastrodermal cells and in the epidermal tissue. Finally, chordin-like/kielin (chordin-like), a gene highly correlated to bleaching, was expressed solely in the oral gastrodermis. From this study, we confirm that heat-responsive genes occur widely in coral tissues outside of symbiont-containing cells. Joint information about expression patterns in response to heat and cell specificity will allow greater dissection of the regulatory pathways and specific cell reactions that lead to coral bleaching., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

Rapid environmental change currently presents a major threat to global biodiversity and ecosystem functions, and understanding impacts on individual populations is critical to creating reliable predictions and mitigation plans. One emerging tool for this goal is high-throughput sequencing technology, which can now be used to scan the genome for signs of environmental selection in any species and any system. This explosion of data provides a powerful new window into the molecular mechanisms of adaptation, and although there has been some success in using genomic data to predict responses to selection in fields such as agriculture, thus far genomic data are rarely integrated into predictive frameworks of future adaptation in natural populations. Here, we review both theoretical and empirical studies of adaptation to rapid environmental change, focusing on areas where genomic data are poised to contribute to our ability to estimate species and population persistence and adaptation. We advocate for the need to study and model evolutionary response architectures, which integrate spatial information, fitness estimates, and plasticity with genetic architecture. Understanding how these factors contribute to adaptive responses is essential in efforts to predict the responses of species and ecosystems to future environmental change.

Increasing awareness of spatial and temporal variation in ocean pH suggests some marine populations may be adapted to local pH regimes and will therefore respond differently to present-day pH variation and to long-term ocean acidification. In the Northeast Pacific Ocean, differences in the strength of coastal upwelling cause latitudinal variation in prevailing pH regimes that are hypothesized to promote local adaptation and unequal pH tolerance among resident populations. In this study, responses to experimental seawater acidification were compared among embryos and larvae from six populations of purple sea urchins (Strongylocentrotus purpuratus) inhabiting areas that differ in their frequency of low pH exposure and that prior research suggests are locally adapted to seawater pH. Transcriptomic analyses demonstrate urchin populations most frequently exposed to low pH seawater responded to experimental acidification by expressing genes within major ATP-producing pathways at greater levels than populations encountering low pH less often. Multiple genes within the tricarboxylic acid cycle, electron transport chain and fatty acid beta oxidation pathways were upregulated in urchin populations experiencing low pH conditions most frequently. These same metabolic pathways were significantly over-represented among genes both expressed in a population-specific manner and putatively under selection to enhance low pH tolerance. Collectively, these data suggest natural selection is acting on metabolic gene networks to redirect ATP toward maintaining acid-base homeostasis and enhance tolerance of seawater acidification. As a trade-off, marine populations more tolerant of low pH may have less energy to put towards other aspects of fitness and to respond to additional ocean change., (© 2017 John Wiley & Sons Ltd.)

Corals respond to heat pulses that cause bleaching with massive transcriptional change, but the immediate responses to stress that lead up to these shifts have never been detailed. Understanding these early signals could be important for identifying the regulatory mechanisms responsible for bleaching and how these mechanisms vary between more and less resilient corals. Using RNA sequencing (RNAseq) and sampling every 30 minutes during a short-term heat shock, we found that components of the transcriptome were significantly upregulated within 90 min and after a temperature increase of +2 °C. The developmental transcription factor, Krüppel-like factor 7, was highly expressed within 60 min, and stress-related transcription factors such as Elk-3 were highly expressed starting at 240 min. The sets of genes enriched for early transcriptional response to heat stress included heat shock proteins, small GTPases, and proteasome genes. Retrovirus-related Pol polyproteins from transposons were significantly expressed throughout the whole experiment. Lastly, we propose a model for early transcriptional regulation of protein degradation and cell adhesion response that may ultimately lead to the bleaching and stress response.

Background: Atlantic cod (Gadus morhua), is known to vary genetically across the North Atlantic, Greenland, and Newfoundland. This genetic variation occurs both spatially and temporally through decades of heavy fishing, and is concentrated in three linkage disequilibrium blocks, previously defined by pedigreed linkage mapping analysis. Variation within these genomic regions is correlated with both seawater temperature and behavioral ecotype. The full extent and nature of these linkage groups is important information for interpreting cod genetic structure as a tool for future fisheries management., Results: We conducted whole genome sequencing for 31 individual cod from three sub-populations in the Gulf of Maine. Across the genome, we found 3,390,654 intermediate to high frequency Single Nucleotide Polymorphisms (SNPs). We show that pairwise linkage analysis among these SNPs is a powerful tool to detect linkage disequilibrium clusters by recovering the three previously detected linkage groups and identifying the 1031 genes contained therein. Across these genes, we found significant population differentiation among spawning groups in the Gulf of Maine and between Georges Bank and Gulf of Maine. Coordinated divergence among these genes and their differentiation at both short and long spatial scales suggests that they are acting as linked supergenes in local adaptation of cod populations., Conclusions: Differentiation between SNPs in linkage disequilibrium blocks is the major signal of genetic differentiation between all groups tested within the Gulf of Maine. Our data provide a map of genes contained in these blocks, allowing an enhanced search for neutral genetic structure for demographic inference and fisheries modeling. Patterns of selection and the history of populations may be possible to identify in cod using this description of linkage disequilibrium blocks and future data sets to robustly separate neutral and selected genetic markers.

For reef-building corals, extreme stress exposure can result in loss of endosymbionts, leaving colonies bleached. However, corals in some habitats are commonly exposed to natural cycles of sub-bleaching stress, often leading to higher stress tolerance. We monitored transcription in the tabletop coral Acropora hyacinthus daily for 17 days over a strong tidal cycle that included extreme temperature spikes, and show that increases in temperature above 30.5°C triggered a strong transcriptional response. The transcriptomic time series data allowed us to identify a set of genes with coordinated expression that were activated only on days with strong tides, high temperature, and large diel pH and oxygen changes. The responsive genes are enriched for gene products essential to the unfolded protein response, an ancient cellular response to endoplasmic reticulum stress. After the temporary heat pulses passed, expression of these genes immediately decreased, suggesting that homeostasis was restored to the endoplasmic reticulum. In a laboratory temperature stress experiment, we found that the expression of these environmentally responsive genes increased as corals bleached, showing that the unfolded protein response becomes more intense during more severe stress. Our results point to the unfolded protein response as a first line of defense that acroporid corals use when coping with environmental stress on the reef, thus enhancing our understanding of coral stress physiology during a time of major concern for reefs.

Today most population genomic studies of nonmodel organisms either sequence a subset of the genome deeply in each individual or sequence pools of unlabelled individuals. With a step-by-step workflow, we illustrate how low-coverage whole-genome sequencing of hundreds of individually barcoded samples is now a practical alternative strategy for obtaining genomewide data on a population scale. We used a highly efficient protocol to generate high-quality libraries for ~6.5 USD from each of 876 Atlantic silversides (a teleost fish with a genome size ~730 Mb) that we sequenced to 1-4× genome coverage. In the absence of a reference genome, we developed a bioinformatic pipeline for mapping the genomic reads to a de novo assembled reference transcriptome. This provides an 'in silico' method for exome capture that avoids the complexities and expenses of using wet chemistry for target isolation. Using novel tools for analysis of low-coverage data, we extracted population allele frequencies, individual genotype likelihoods and polymorphism data for 2 504 335 SNPs across the exome for the 876 fish. To illustrate the use of the resulting data, we present a preliminary analysis of geographical patterns in the exome data and a comparison of complete mitochondrial genome sequences for each individual (constructed from the low-coverage data) that show population colonization patterns along the US east coast. With a total cost per sample of less than 50 USD (including sequencing) and ability to prepare 96 libraries in only 5 h, our approach adds a viable new option to the population genomics toolbox., (© 2016 John Wiley & Sons Ltd.)

Ocean warming threatens corals and the coral reef ecosystem. Nevertheless, corals can be adapted to their thermal environment and inherit heat tolerance across generations. In addition, the diverse microbes that associate with corals have the capacity for more rapid change, potentially aiding the adaptation of long-lived corals. Here, we show that the microbiome of reef corals is different across thermally variable habitats and changes over time when corals are reciprocally transplanted. Exposing these corals to thermal bleaching conditions changes the microbiome for heat-sensitive corals, but not for heat-tolerant corals growing in habitats with natural high heat extremes. Importantly, particular bacterial taxa predict the coral host response in a short-term heat stress experiment. Such associations could result from parallel responses of the coral and the microbial community to living at high natural temperatures. A competing hypothesis is that the microbial community and coral heat tolerance are causally linked.

Robert T. Paine, who passed away on 13 June 2016, is among the most influential people in the history of ecology. Paine was an experimentalist, a theoretician, a practitioner, and proponent of the "ecology of place," and a deep believer in the importance of natural history to ecological understanding. His scientific legacy grew from the discovery of a link between top-down forcing and species diversity, a breakthrough that led to the ideas of both keystone species and trophic cascades, and to our early understanding of the mosaic nature of biological communities, causes of zonation across physical gradients, and the intermediate-disturbance hypothesis of species diversity. Paine's influence as a mentor was equally important to the growth of ecological thinking, natural resource conservation, and policy. He served ecology as an Ecological Society of America president, an editor of the Society's journals, a member of and contributor to the National Academy of Sciences and the National Research Council, and an in-demand advisor to various state and federal agencies. Paine's broad interests, enthusiasm, charisma, and humor deeply affected our lives and the lives of so many others., (© 2016 by the Ecological Society of America.)

Organisms respond to environmental variation partly through changes in gene expression, which underlie both homeostatic and acclimatory responses to environmental stress. In some cases, so many genes change in expression in response to different influences that understanding expression patterns for all these individual genes becomes difficult. To reduce this problem, we use a systems genetics approach to show that variation in the expression of thousands of genes of reef-building corals can be explained as variation in the expression of a small number of coexpressed "modules." Modules were often enriched for specific cellular functions and varied predictably among individuals, experimental treatments, and physiological state. We describe two transcriptional modules for which expression levels immediately after heat stress predict bleaching a day later. One of these early "bleaching modules" is enriched for sequence-specific DNA-binding proteins, particularly E26 transformation-specific (ETS)-family transcription factors. The other module is enriched for extracellular matrix proteins. These classes of bleaching response genes are clear in the modular gene expression analysis we conduct but are much more difficult to discern in single gene analyses. Furthermore, the ETS-family module shows repeated differences in expression among coral colonies grown in the same common garden environment, suggesting a heritable genetic or epigenetic basis for these expression polymorphisms. This finding suggests that these corals harbor high levels of gene-network variation, which could facilitate rapid evolution in the face of environmental change., (© The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Species invasions cause significant ecological and economic damage, and genetic information is important to understanding and managing invasive species. In the ocean, many invasive species have high dispersal and gene flow, lowering the discriminatory power of traditional genetic approaches. High-throughput sequencing holds tremendous promise for increasing resolution and illuminating the relative contributions of selection and drift in marine invasion, but has not yet been used to compare the diversity and dynamics of a high-dispersal invader in its native and invaded ranges. We test a transcriptome-based approach in the European green crab (Carcinus maenas), a widespread invasive species with high gene flow and a well-known invasion history, in two native and five invasive populations. A panel of 10 809 transcriptome-derived nuclear SNPs identified significant population structure among highly bottlenecked invasive populations that were previously undifferentiated with traditional markers. Comparing the full data set and a subset of 9246 putatively neutral SNPs strongly suggested that non-neutral processes are the primary driver of population structure within the species' native range, while neutral processes appear to dominate in the invaded range. Non-neutral native range structure coincides with significant differences in intraspecific thermal tolerance, suggesting temperature as a potential selective agent. These results underline the importance of adaptation in shaping intraspecific differences even in high geneflow marine invasive species. They also demonstrate that high-throughput approaches have broad utility in determining neutral structure in recent invasions of such species. Together, neutral and non-neutral data derived from high-throughput approaches may increase the understanding of invasion dynamics in high-dispersal species., (© 2015 John Wiley & Sons Ltd.)

Advances in nucleic acid sequencing technology are removing obstacles that historically prevented use of genomics within ocean change biology. As one of the first marine calcifiers to have its genome sequenced, purple sea urchins (Strongylocentrotus purpuratus) have been the subject of early research exploring genomic responses to ocean acidification, work that points to future experiments and illustrates the value of expanding genomic resources to other marine organisms in this new 'post-genomic' era. This review presents case studies of S. purpuratus demonstrating the ability of genomic experiments to address major knowledge gaps within ocean acidification. Ocean acidification research has focused largely on species vulnerability, and studies exploring mechanistic bases of tolerance toward low pH seawater are comparatively few. Transcriptomic responses to high pCO₂ seawater in a population of urchins already encountering low pH conditions have cast light on traits required for success in future oceans. Secondly, there is relatively little information on whether marine organisms possess the capacity to adapt to oceans progressively decreasing in pH. Genomics offers powerful methods to investigate evolutionary responses to ocean acidification and recent work in S. purpuratus has identified genes under selection in acidified seawater. Finally, relatively few ocean acidification experiments investigate how shifts in seawater pH combine with other environmental factors to influence organism performance. In S. purpuratus, transcriptomics has provided insight into physiological responses of urchins exposed simultaneously to warmer and more acidic seawater. Collectively, these data support that similar breakthroughs will occur as genomic resources are developed for other marine species., (Copyright © 2015 Elsevier Inc. All rights reserved.)