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      Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations

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          Abstract

          Phenotypic variation is critical for the long-term persistence of species and populations. Anthropogenic activities have caused substantial shifts and reductions in phenotypic variation across diverse taxa, but the underlying mechanism(s) (i.e., phenotypic plasticity and/or genetic evolution) and long-term consequences (e.g., ability to recover phenotypic variation) are unclear. Here we investigate the widespread and dramatic changes in adult migration characteristics of wild Chinook salmon caused by dam construction and other anthropogenic activities. Strikingly, we find an extremely robust association between migration phenotype (i.e., spring-run or fall-run) and a single locus, and that the rapid phenotypic shift observed after a recent dam construction is explained by dramatic allele frequency change at this locus. Furthermore, modeling demonstrates that continued selection against the spring-run phenotype could rapidly lead to complete loss of the spring-run allele, and an empirical analysis of populations that have already lost the spring-run phenotype reveals they are not acting as sustainable reservoirs of the allele. Finally, ancient DNA analysis suggests the spring-run allele was abundant in historical habitat that will soon become accessible through a large-scale restoration (i.e., dam removal) project, but our findings suggest that widespread declines and extirpation of the spring-run phenotype and allele will challenge reestablishment of the spring-run phenotype in this and future restoration projects. These results reveal the mechanisms and consequences of human-induced phenotypic change and highlight the need to conserve and restore critical adaptive variation before the potential for recovery is lost.

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          Most cited references43

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          Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity.

          The flow regime is regarded by many aquatic ecologists to be the key driver of river and floodplain wetland ecosystems. We have focused this literature review around four key principles to highlight the important mechanisms that link hydrology and aquatic biodiversity and to illustrate the consequent impacts of altered flow regimes: Firstly, flow is a major determinant of physical habitat in streams, which in turn is a major determinant of biotic composition; Secondly, aquatic species have evolved life history strategies primarily in direct response to the natural flow regimes; Thirdly, maintenance of natural patterns of longitudinal and lateral connectivity is essential to the viability of populations of many riverine species; Finally, the invasion and success of exotic and introduced species in rivers is facilitated by the alteration of flow regimes. The impacts of flow change are manifest across broad taxonomic groups including riverine plants, invertebrates, and fish. Despite growing recognition of these relationships, ecologists still struggle to predict and quantify biotic responses to altered flow regimes. One obvious difficulty is the ability to distinguish the direct effects of modified flow regimes from impacts associated with land-use change that often accompanies water resource development. Currently, evidence about how rivers function in relation to flow regime and the flows that aquatic organisms need exists largely as a series of untested hypotheses. To overcome these problems, aquatic science needs to move quickly into a manipulative or experimental phase, preferably with the aims of restoration and measuring ecosystem response.
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            Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change

            Climate change is a major threat to global biodiversity. A novel integrated framework to assess vulnerability and prioritize research and management action aims to improve our ability to respond to this emerging crisis.
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              Keeping up with a warming world; assessing the rate of adaptation to climate change.

              The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity. The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions. Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.
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                Author and article information

                Journal
                Proceedings of the National Academy of Sciences
                Proc Natl Acad Sci USA
                Proceedings of the National Academy of Sciences
                0027-8424
                1091-6490
                December 04 2018
                : 201811559
                Article
                10.1073/pnas.1811559115
                6320526
                30514813
                35388b08-817c-4031-9ceb-98ed84df3f55
                © 2018

                Free to read

                http://www.pnas.org/site/misc/userlicense.xhtml

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