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      Building coral reef resilience through assisted evolution.

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          Abstract

          The genetic enhancement of wild animals and plants for characteristics that benefit human populations has been practiced for thousands of years, resulting in impressive improvements in commercially valuable species. Despite these benefits, genetic manipulations are rarely considered for noncommercial purposes, such as conservation and restoration initiatives. Over the last century, humans have driven global climate change through industrialization and the release of increasing amounts of CO2, resulting in shifts in ocean temperature, ocean chemistry, and sea level, as well as increasing frequency of storms, all of which can profoundly impact marine ecosystems. Coral reefs are highly diverse ecosystems that have suffered massive declines in health and abundance as a result of these and other direct anthropogenic disturbances. There is great concern that the high rates, magnitudes, and complexity of environmental change are overwhelming the intrinsic capacity of corals to adapt and survive. Although it is important to address the root causes of changing climate, it is also prudent to explore the potential to augment the capacity of reef organisms to tolerate stress and to facilitate recovery after disturbances. Here, we review the risks and benefits of the improvement of natural and commercial stocks in noncoral reef systems and advocate a series of experiments to determine the feasibility of developing coral stocks with enhanced stress tolerance through the acceleration of naturally occurring processes, an approach known as (human)-assisted evolution, while at the same time initiating a public dialogue on the risks and benefits of this approach.

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          Most cited references82

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          Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming

          Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity, despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusk larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting that it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single-species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature.
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            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.
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              Stress tolerance in plants via habitat-adapted symbiosis.

              We demonstrate that native grass species from coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively. Symbiotically conferred stress tolerance is a habitat-specific phenomenon with geothermal endophytes conferring heat but not salt tolerance, and coastal endophytes conferring salt but not heat tolerance. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not confer these stress tolerances. Moreover, fungal endophytes from agricultural crops conferred disease resistance and not salt or heat tolerance. We define habitat-specific, symbiotically-conferred stress tolerance as habitat-adapted symbiosis and hypothesize that it is responsible for the establishment of plants in high-stress habitats. The agricultural, coastal and geothermal plant endophytes also colonized tomato (a model eudicot) and conferred disease, salt and heat tolerance, respectively. In addition, the coastal plant endophyte colonized rice (a model monocot) and conferred salt tolerance. These endophytes have a broad host range encompassing both monocots and eudicots. Interestingly, the endophytes also conferred drought tolerance to plants regardless of the habitat of origin. Abiotic stress tolerance correlated either with a decrease in water consumption or reactive oxygen sensitivity/generation but not to increased osmolyte production. The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural and native plant communities.
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                Author and article information

                Journal
                Proc. Natl. Acad. Sci. U.S.A.
                Proceedings of the National Academy of Sciences of the United States of America
                1091-6490
                0027-8424
                Feb 24 2015
                : 112
                : 8
                Affiliations
                [1 ] Australian Institute of Marine Science, Townsville MC, QLD 4810, Australia; and m.vanoppen@aims.gov.au.
                [2 ] Australian Institute of Marine Science, Townsville MC, QLD 4810, Australia; and.
                [3 ] Hawaii Institute of Marine Biology, Kaneohe, HI 96744.
                Article
                1422301112
                10.1073/pnas.1422301112
                25646461
                aa589132-aabe-4fe2-a206-1cffdd439c65
                History

                adaptation,climate change,microbial symbionts,selective breeding,transgenerational acclimatization

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