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      Genes Left Behind: Climate Change Threatens Cryptic Genetic Diversity in the Canopy-Forming Seaweed Bifurcaria bifurcata

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          Abstract

          The global redistribution of biodiversity will intensify in the coming decades of climate change, making projections of species range shifts and of associated genetic losses important components of conservation planning. Highly-structured marine species, notably brown seaweeds, often harbor unique genetic variation at warmer low-latitude rear edges and thus are of particular concern. Here, a combination of Ecological Niche Models (ENMs) and molecular data is used to forecast the potential near-future impacts of climate change for a warm-temperate, canopy forming seaweed, Bifurcaria bifurcata. ENMs for B. bifurcata were developed using marine and terrestrial climatic variables, and its range projected for 2040-50 and 2090-2100 under two greenhouse emission scenarios. Geographical patterns of genetic diversity were assessed by screening 18 populations spawning the entire distribution for two organelle genes and 6 microsatellite markers. The southern limit of B. bifurcata was predicted to shift northwards to central Morocco by the mid-century. By 2090-2100, depending on the emission scenario, it could either retreat further north to western Iberia or be relocated back to Western Sahara. At the opposing margin, B. bifurcata was predicted to expand its range to Scotland or even Norway. Microsatellite diversity and endemism were highest in Morocco, where a unique and very restricted lineage was also identified. Our results imply that B. bifurcata will maintain a relatively broad latitudinal distribution. Although its persistence is not threatened, the predicted extirpation of a unique southern lineage or even the entire Moroccan diversity hotspot will erase a rich evolutionary legacy and shrink global diversity to current (low) European levels. NW Africa and similarly understudied southern regions should receive added attention if expected range changes and diversity loss of warm-temperate species is not to occur unnoticed.

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          Conserving biodiversity under climate change: the rear edge matters.

          Modern climate change is producing poleward range shifts of numerous taxa, communities and ecosystems worldwide. The response of species to changing environments is likely to be determined largely by population responses at range margins. In contrast to the expanding edge, the low-latitude limit (rear edge) of species ranges remains understudied, and the critical importance of rear edge populations as long-term stores of species' genetic diversity and foci of speciation has been little acknowledged. We review recent findings from the fossil record, phylogeography and ecology to illustrate that rear edge populations are often disproportionately important for the survival and evolution of biota. Their ecological features, dynamics and conservation requirements differ from those of populations in other parts of the range, and some commonly recommended conservation practices might therefore be of little use or even counterproductive for rear edge populations.
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            The impacts of climate change in coastal marine systems.

            Anthropogenically induced global climate change has profound implications for marine ecosystems and the economic and social systems that depend upon them. The relationship between temperature and individual performance is reasonably well understood, and much climate-related research has focused on potential shifts in distribution and abundance driven directly by temperature. However, recent work has revealed that both abiotic changes and biological responses in the ocean will be substantially more complex. For example, changes in ocean chemistry may be more important than changes in temperature for the performance and survival of many organisms. Ocean circulation, which drives larval transport, will also change, with important consequences for population dynamics. Furthermore, climatic impacts on one or a few 'leverage species' may result in sweeping community-level changes. Finally, synergistic effects between climate and other anthropogenic variables, particularly fishing pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve living marine systems in the face of climate change will require improvements to the existing predictive framework. Key directions for future research include identifying key demographic transitions that influence population dynamics, predicting changes in the community-level impacts of ecologically dominant species, incorporating populations' ability to evolve (adapt), and understanding the scales over which climate will change and living systems will respond.
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              Ecological consequences of genetic diversity.

              Understanding the ecological consequences of biodiversity is a fundamental challenge. Research on a key component of biodiversity, genetic diversity, has traditionally focused on its importance in evolutionary processes, but classical studies in evolutionary biology, agronomy and conservation biology indicate that genetic diversity might also have important ecological effects. Our review of the literature reveals significant effects of genetic diversity on ecological processes such as primary productivity, population recovery from disturbance, interspecific competition, community structure, and fluxes of energy and nutrients. Thus, genetic diversity can have important ecological consequences at the population, community and ecosystem levels, and in some cases the effects are comparable in magnitude to the effects of species diversity. However, it is not clear how widely these results apply in nature, as studies to date have been biased towards manipulations of plant clonal diversity, and little is known about the relative importance of genetic diversity vs. other factors that influence ecological processes of interest. Future studies should focus not only on documenting the presence of genetic diversity effects but also on identifying underlying mechanisms and predicting when such effects are likely to occur in nature.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                15 July 2015
                2015
                : 10
                : 7
                : e0131530
                Affiliations
                [001]Centro de Ciências do Mar da Universidade do Algarve, Faro, Portugal
                University of Connecticut, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JN GAP EAS. Performed the experiments: JN JA NCC FF. Analyzed the data: JN JA NCC. Contributed reagents/materials/analysis tools: JN JA FF. Wrote the paper: JN JA GAP EAS.

                Article
                PONE-D-14-54608
                10.1371/journal.pone.0131530
                4503591
                26177545
                1a44cbc0-6abd-4271-9ef3-4948ffa4cce8
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 5 December 2014
                : 3 June 2015
                Page count
                Figures: 7, Tables: 1, Pages: 21
                Funding
                This work was funded by Portuguese FCT (Fundação para a Ciência e a Tecnologia) through projects EDGES (PTDC/AAC-CLI/109108/2008), ReUp (EXPL/BIA-BIC/1471/2012) and EXTANT (EXCL/AAG-GLO/0661/2012) and a postdoctoral fellowship to JN (SFRH/BPD/88935/2012).
                Categories
                Research Article
                Custom metadata
                Sequences are available from Genbank (nos. KR002845-48 and KR002849-55). R code used for the SDM analyzes, raster files with environmental (climatic) data, and microsatellite data are available in the Figshare repository at http://dx.doi.org/10.6084/m9.figshare.1371115.

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