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"Palumbi, Stephen R"
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Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries
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 geno-type 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.
Journal Article
Bacterial community dynamics are linked to patterns of coral heat tolerance
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.
Coral-associated microbes could enhance the capacity of their host organism to respond to environmental change. Ziegler and colleagues use a reciprocal transplant experiment to show that microbiomes of heat-tolerant corals are more resilient to change than those of heat-sensitive corals.
Journal Article
Genetic Structure Among 50 Species of the Northeastern Pacific Rocky Intertidal Community
Comparing many species' population genetic patterns across the same seascape can identify species with different levels of structure, and suggest hypotheses about the processes that cause such variation for species in the same ecosystem. This comparative approach helps focus on geographic barriers and selective or demographic processes that define genetic connectivity on an ecosystem scale, the understanding of which is particularly important for large-scale management efforts. Moreover, a multispecies dataset has great statistical advantages over single-species studies, lending explanatory power in an effort to uncover the mechanisms driving population structure. Here, we analyze a 50-species dataset of Pacific nearshore invertebrates with the aim of discovering the most influential structuring factors along the Pacific coast of North America. We collected cytochrome c oxidase I (COI) mtDNA data from populations of 34 species of marine invertebrates sampled coarsely at four coastal locations in California, Oregon, and Alaska, and added published data from 16 additional species. All nine species with non-pelagic development have strong genetic structure. For the 41 species with pelagic development, 13 show significant genetic differentiation, nine of which show striking FST levels of 0.1-0.6. Finer scale geographic investigations show unexpected regional patterns of genetic change near Cape Mendocino in northern California for five of the six species tested. The region between Oregon and Alaska is a second focus of intraspecific genetic change, showing differentiation in half the species tested. Across regions, strong genetic subdivision occurs more often than expected in mid-to-high intertidal species, a result that may reflect reduced gene flow due to natural selection along coastal environmental gradients. Finally, the results highlight the importance of making primary research accessible to policymakers, as unexpected barriers to marine dispersal break the coast into separate demographic zones that may require their own management plans.
Journal Article
Mechanisms of reef coral resistance to future climate change
Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
Journal Article
Marine defaunation: Animal loss in the global ocean
The loss of animal species in terrestrial environments has been well documented and is continuing. Loss of species in marine environments has been slower than in terrestrial systems, but appears to be increasing rapidly. McCauley et al. review the recent patterns of species decline and loss in marine environments. Though they note many worrying declines, they also highlight approaches that might allow us to prevent the type of massive defaunation that has occurred on land. Science , this issue 10.1126/science.1255641 Marine defaunation, or human-caused animal loss in the oceans, emerged forcefully only hundreds of years ago, whereas terrestrial defaunation has been occurring far longer. Though humans have caused few global marine extinctions, we have profoundly affected marine wildlife, altering the functioning and provisioning of services in every ocean. Current ocean trends, coupled with terrestrial defaunation lessons, suggest that marine defaunation rates will rapidly intensify as human use of the oceans industrializes. Though protected areas are a powerful tool to harness ocean productivity, especially when designed with future climate in mind, additional management strategies will be required. Overall, habitat degradation is likely to intensify as a major driver of marine wildlife loss. Proactive intervention can avert a marine defaunation disaster of the magnitude observed on land.
Journal Article
The genomics of recovery from coral bleaching
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.
Journal Article
Genomic basis for coral resilience to climate change
Recent advances in DNA-sequencing technologies now allow for in-depth characterization of the genomic stress responses of many organisms beyond model taxa. They are especially appropriate for organisms such as reef-building corals, for which dramatic declines in abundance are expected to worsen as anthropogenic climate change intensifies. Different corals differ substantially in physiological resilience to environmental stress, but the molecular mechanisms behind enhanced coral resilience remain unclear. Here, we compare transcriptome-wide gene expression (via RNA-Seq using Illumina sequencing) among conspecific thermally sensitive and thermally resilient corals to identify the molecular pathways contributing to coral resilience. Under simulated bleaching stress, sensitive and resilient corals change expression of hundreds of genes, but the resilient corals had higher expression under control conditions across 60 of these genes. These “frontloaded” transcripts were less up-regulated in resilient corals during heat stress and included thermal tolerance genes such as heat shock proteins and antioxidant enzymes, as well as a broad array of genes involved in apoptosis regulation, tumor suppression, innate immune response, and cell adhesion. We propose that constitutive frontloading enables an individual to maintain physiological resilience during frequently encountered environmental stress, an idea that has strong parallels in model systems such as yeast. Our study provides broad insight into the fundamental cellular processes responsible for enhanced stress tolerances that may enable some organisms to better persist into the future in an era of global climate change.
Journal Article
Designing marine reserve networks for both conservation and fisheries management
Marine protected areas (MPAs) that exclude fishing have been shown repeatedly to enhance the abundance, size, and diversity of species. These benefits, however, mean little to most marine species, because individual protected areas typically are small. To meet the larger-scale conservation challenges facing ocean ecosystems, several nations are expanding the benefits of individual protected areas by building networks of protected areas. Doing so successfully requires a detailed understanding of the ecological and physical characteristics of ocean ecosystems and the responses of humans to spatial closures. There has been enormous scientific interest in these topics, and frameworks for the design of MPA networks for meeting conservation and fishery management goals are emerging. Persistent in the literature is the perception of an inherent tradeoff between achieving conservation and fishery goals. Through a synthetic analysis across these conservation and bioeconomic studies, we construct guidelines for MPA network design that reduce or eliminate this tradeoff. We present size, spacing, location, and configuration guidelines for designing networks that simultaneously can enhance biological conservation and reduce fishery costs or even increase fishery yields and profits. Indeed, in some settings, a well-designed MPA network is critical to the optimal harvest strategy. When reserves benefit fisheries, the optimal area in reserves is moderately large (mode ≈30%). Assessing network design principals is limited currently by the absence of empirical data from large-scale networks. Emerging networks will soon rectify this constraint.
Journal Article
Genomic analysis of distinct bleaching tolerances among cryptic coral species
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.
Journal Article