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      Speeding Up Microevolution: The Effects of Increasing Temperature on Selection and Genetic Variance in a Wild Bird Population

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      PLoS Biology
      Public Library of Science

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          Abstract

          The authors show that environmental variation may lead to a positive association between the annual strength of selection and expression of genetic variance in a wild bird population, which can speed up microevolution and have important consequences for how fast natural populations adapt to environmental changes.

          Abstract

          The amount of genetic variance underlying a phenotypic trait and the strength of selection acting on that trait are two key parameters that determine any evolutionary response to selection. Despite substantial evidence that, in natural populations, both parameters may vary across environmental conditions, very little is known about the extent to which they may covary in response to environmental heterogeneity. Here we show that, in a wild population of great tits ( Parus major), the strength of the directional selection gradients on timing of breeding increased with increasing spring temperatures, and that genotype-by-environment interactions also predicted an increase in additive genetic variance, and heritability, of timing of breeding with increasing spring temperature. Consequently, we therefore tested for an association between the annual selection gradients and levels of additive genetic variance expressed each year; this association was positive, but non-significant. However, there was a significant positive association between the annual selection differentials and the corresponding heritability. Such associations could potentially speed up the rate of micro-evolution and offer a largely ignored mechanism by which natural populations may adapt to environmental changes.

          Author Summary

          The speed of evolutionary change in a phenotypic trait is determined by two key components: the amount of genetic variance underlying the trait and the strength of selection acting on it. Many studies have shown that both selection and expression of genetic variance may depend on the environmental conditions the population experiences. However, the possibility that the strength of selection and the expression of genetic variance become positively or negatively associated as a result of this environmental covariance, so as to speed up or hamper an evolutionary response, has been largely ignored. Here we show that, in a wild bird population, the annual strength of selection on and the expression of genetic variance in timing of breeding (a key life history trait) are positively associated due to changing environmental conditions (warmer temperatures). Such a positive association should potentially speed up any microevolutionary response to selection (such as that imposed by climate warming). Our results illustrate the existence of substantial temporal variation in response to environmental heterogeneity, and thus highlight a so far neglected mechanism that may be important in determining the evolutionary dynamics in natural populations.

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          The strength of phenotypic selection in natural populations.

          How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.
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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

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                February 2011
                February 2011
                1 February 2011
                : 9
                : 2
                : e1000585
                Affiliations
                [1 ]Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
                [2 ]Department of Animal Ecology, Evolutionary Biology Centre (EBC), Uppsala University, Uppsala, Sweden
                [3 ]Netherlands Institute of Ecology (NIOO-KNAW), Heteren, The Netherlands
                The University of North Carolina, United States of America
                Author notes

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: AH MEV LEBK. Analyzed the data: AH. Wrote the paper: AH MEV LEBK.

                Article
                10-PLBI-RA-6938R3
                10.1371/journal.pbio.1000585
                3051266
                21408101
                76013957-b0ce-479b-aa06-b41d200443a0
                Husby et al. 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
                : 9 April 2010
                : 9 December 2010
                Page count
                Pages: 9
                Categories
                Research Article
                Evolutionary Biology/Evolutionary and Comparative Genetics
                Evolutionary Biology/Evolutionary Ecology
                Genetics and Genomics/Complex Traits

                Life sciences
                Life sciences

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