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      Does human-induced hybridization have long-term genetic effects? Empirical testing with domesticated, wild and hybridized fish populations

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          Abstract

          Current conservation practices exclude human-generated hybridized populations from protection, as the genetic effects of hybridization in the wild have been observed to be long-lasting based on neutral genetic markers and are considered potentially irreversible. Theory, however, predicts otherwise for genes under selection. We transplanted combinations of wild, domesticated and hybridized populations of a fish species to new environments. We then compared survival, phenotypic variation and plasticity to determine whether hybridization affects adaptive potential after multiple generations of selection in the wild. Although the fitness of our hybridized populations at the onset of hybridization cannot be assessed, our results suggest that within five to eleven generations, selection can remove introduced foreign genes from wild populations that have hybridized with domesticated conspecifics. The end result is hybridized populations that, in terms of survival, phenotypic plasticity, mean trait expression and overall general responses to environmental change, closely resemble neighbouring wild populations. These results have important implications for considering the potential conservation value of hybridized populations and illustrate the effectiveness of selection in a local environment.

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          Most cited references49

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          Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild.

          Captive breeding is used to supplement populations of many species that are declining in the wild. The suitability of and long-term species survival from such programs remain largely untested, however. We measured lifetime reproductive success of the first two generations of steelhead trout that were reared in captivity and bred in the wild after they were released. By reconstructing a three-generation pedigree with microsatellite markers, we show that genetic effects of domestication reduce subsequent reproductive capabilities by approximately 40% per captive-reared generation when fish are moved to natural environments. These results suggest that even a few generations of domestication may have negative effects on natural reproduction in the wild and that the repeated use of captive-reared parents to supplement wild populations should be carefully reconsidered.
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            Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management.

            As populations become increasingly fragmented, managers are often faced with the dilemma that intentional hybridization might save a population from inbreeding depression but it might also induce outbreeding depression. While empirical evidence for inbreeding depression is vastly greater than that for outbreeding depression, the available data suggest that risks of outbreeding, particularly in the second generation, are on par with the risks of inbreeding. Predicting the relative risks in any particular situation is complicated by variation among taxa, characters being measured, level of divergence between hybridizing populations, mating history, environmental conditions and the potential for inbreeding and outbreeding effects to be occurring simultaneously. Further work on consequences of interpopulation hybridization is sorely needed with particular emphasis on the taxonomic scope, the duration of fitness problems and the joint effects of inbreeding and outbreeding. Meanwhile, managers can minimize the risks of both inbreeding and outbreeding by using intentional hybridization only for populations clearly suffering from inbreeding depression, maximizing the genetic and adaptive similarity between populations, and testing the effects of hybridization for at least two generations whenever possible.
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              Extent and scale of local adaptation in salmonid fishes: review and meta-analysis.

              What is the extent and scale of local adaptation (LA)? How quickly does LA arise? And what is its underlying molecular basis? Our review and meta-analysis on salmonid fishes estimates the frequency of LA to be ∼55-70%, with local populations having a 1.2 times average fitness advantage relative to foreign populations or to their performance in new environments. Salmonid LA is evident at a variety of spatial scales (for example, few km to>1000 km) and can manifest itself quickly (6-30 generations). As the geographic scale between populations increases, LA is generally more frequent and stronger. Yet the extent of LA in salmonids does not appear to differ from that in other assessed taxa. Moreover, the frequency with which foreign salmonid populations outperform local populations (∼23-35%) suggests that drift, gene flow and plasticity often limit or mediate LA. The relatively few studies based on candidate gene and genomewide analyses have identified footprints of selection at both small and large geographical scales, likely reflecting the specific functional properties of loci and the associated selection regimes (for example, local niche partitioning, pathogens, parasites, photoperiodicity and seasonal timing). The molecular basis of LA in salmonids is still largely unknown, but differential expression at the same few genes is implicated in the convergent evolution of certain phenotypes. Collectively, future research will benefit from an integration of classical and molecular approaches to understand: (i) species differences and how they originate, (ii) variation in adaptation across scales, life stages, population sizes and environmental gradients, and (iii) evolutionary responses to human activities.
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                Author and article information

                Journal
                Evol Appl
                Evol Appl
                eva
                Evolutionary Applications
                Blackwell Publishing Ltd (Oxford, UK )
                1752-4571
                1752-4571
                December 2014
                27 August 2014
                : 7
                : 10
                : 1180-1191
                Affiliations
                [1 ]Department of Biology, Concordia University Montreal, QC, Canada
                [2 ]Aquatic Biodiversity and Conservation Unit, Ontario Ministry of Natural Resources Peterborough, ON, Canada
                Author notes
                Correspondence Dylan J. Fraser, Department of Biology, Concordia University, 7141 Sherbrooke St. W, Montreal, QC, Canada H4B 1R6., Tel.: +(514) 848-2424 extn. 8729;, fax: +(514) 848-2881;, e-mail: dylan.fraser@ 123456concordia.ca
                Article
                10.1111/eva.12199
                4275090
                25558279
                581e6ef4-f0dd-412d-b94e-1adfcd54a73d
                © 2014 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 October 2013
                : 13 July 2014
                Categories
                Original Articles

                Evolutionary Biology
                adaptive potential,domestic,hatchery,hybridization,phenotypic plasticity,salvelinus fontinalis,selection,survival,transplant

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