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Genetic Rescue of Small Inbred Populations: Meta- Analysis Reveals Large and Consistent Benefits of Gene flow

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Molecular Ecology (2015) 24, 2610–2618 doi: 10.1111/mec.13139 FROM THE COVER Genetic rescue of small inbred populations: meta- analysis reveals large and consistent benefits of gene flow RICHARD FRANKHAM*† *Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia, †Australian Museum, 6 College St, Sydney, NSW 2010, Australia Abstract Many species have fragmented distribution with small isolated populations suffering inbreeding depression and/or reduced ability to evolve. Without gene flow from another population within the species (genetic rescue), these populations are likely to be extirpated. However, there have been only ~ 20 published cases of such outcrossing for conservation purposes, probably a very low proportion of populations that would potentially benefit. As one impediment to genetic rescues is the lack of an overview of the magnitude and consistency of genetic rescue effects in wild species, I carried out a meta-analysis. Outcrossing of inbred populations resulted in beneficial effects in 92.9% of 156 cases screened as having a low risk of outbreeding depression. The med- ian increase in composite fitness (combined fecundity and survival) following out- crossing was 148% in stressful environments and 45% in benign ones. Fitness benefits also increased significantly with maternal DF (reduction in inbreeding coefficient due to gene flow) and for naturally outbreeding versus inbreeding species. However, bene- fits did not differ significantly among invertebrates, vertebrates and plants. Evolution- ary potential for fitness characters in inbred populations also benefited from gene flow. There are no scientific impediments to the widespread use of outcrossing to genetically rescue inbred populations of naturally outbreeding species, provided potential crosses have a low risk of outbreeding depression. I provide revised guide- lines for the management of genetic rescue attempts. Keywords: evolutionary potential, genetic rescue guidelines, heterosis, inbreeding depression, outbreeding depression, outcrossing Received 2 January 2015; revision received 26 February 2015; accepted 27 February 2015 laboratory and agricultural species (heterosis: Sinha & Introduction Khanna 1975; Falconer & Mackay 1996; Frankham Many species have isolated populations that are subject to et al. 2010). For example, heterosis has been funda- inbreeding, loss of genetic diversity and elevated extinction mental to the green revolution that has substantially risks (Frankham et al. 2014). Genetic theory indicates that it increased crop plant yields (Borlaug 2000). Despite should often be possible to genetically rescue such popula- this, only ~ 10–20 genetic rescues have been tions by outcrossing within species (augmenting gene flow: attempted for conservation purposes (Adams et al. Tallmon et al. 2004; Whiteley et al. 2015). However, out- 2011; Frankham et al. 2011), probably a miniscule pro- crossing can also be deleterious (outbreeding depression: portion of the populations that might benefit from Edmands 2007; Frankham et al. 2011). outcrossing (Frankham et al. 2014). The limited use of Crossing of populations has frequently been genetic rescue is probably due to concerns about the used to successfully reverse inbreeding depression in following: Correspondence: Richard Frankham, Fax: 612-9850-8245; 1 outbreeding depression/upsetting local genetic adap- E-mail: [email protected] tation/local purity and provenance, © 2015 John Wiley & Sons Ltd GENETIC RESCUE OF SMALL INBRED POPULATIONS 2611 2 limited quantitative information on the expected con- magnitude of the effect and (iii) whether the screen for sequences of outcrossing, outbreeding depression proposed by Frankham et al. 3 lack of clear guidelines, (2011) is effective in such circumstances. Genetic rescue 4 costs, effects were evaluated for both fitness and ability to 5 risks of disease, pest and parasite spread, evolve (especially in changing environments). 6 disrupting social systems in some animals, 7 moving biological material across political jurisdic- Materials and methods tions, 8 regulatory barriers. Data selection criteria The first three are primarily genetic issues, while the Studies were screened to identify relevant data sets that remainder require consideration, but are rarely insuper- encompassed the following: able barriers to gene flow (see Discussion). Frankham et al. (2011) developed a decision tree for predicting the 1 a parental (target) population known or presumed to risk of outbreeding depression and provided prelimin- be inbred and/or having low genetic diversity, ary evidence that it was effective. This contribution fo- 2 gene flow into the inbred population from one or cusses on the second and third issues. more other (inbred or outbred) populations geneti- Information on the magnitude and consistency of cally isolated from the target population, but belong- genetic rescue effects is critical for cost/benefit analyses ing to the same species, of alternative conservation management options for 3 fitness and/or evolutionary potential data on the fragmented populations. Here, I address this issue inbred and outcrossed populations, using a meta-analysis, a tool widely used to overcome 4 sexually reproducing species, as strictly asexual spe- low statistical power in individual studies and to obtain cies do not experience inbreeding depression, hetero- comprehensive quantitative overviews (Frankham et al. sis or outbreeding depression, 2010; Koricheva et al. 2013). In practice, genetic rescues 5 populations where crosses were assessed as having a are only contemplated for populations with elevated low risk of outbreeding depression, using the Frank- inbreeding and/or reduced genetic diversity, so my ham et al. (2011) decision tree (same species, no fixed study was restricted to them. As both beneficial and chromosomal differences, adapted to similar environ- deleterious effects can occur simultaneously, the practi- ments and gene flow within the last 500 years), cal issue is whether the net effects of outcrossing on fit- 6 wild species, not ones used in plant or animal agri- ness are beneficial or deleterious. culture, forestry or aquaculture and subjected to As genetic rescue for fitness in the absence of out- strong artificial selection (in case domestic species breeding depression involves the reversal of inbreeding have different characteristics to wild ones: Frankham depression (Wright 1977; Vrijenhoek 1994; Falconer & 2009). Mackay 1996), the variables affecting it are expected to be the same as those that predict inbreeding depression, Further details of data selection criteria are given in but with effects in the opposite direction (see Appendix Appendix S3 (Supporting information). S1, Supporting information). Thus, genetic rescue is expected to depend upon the difference in inbreeding Sources of data coefficients between the inbred and outcrossed popula- D D tions in mothers ( Fm) and in zygotes ( Fz), on the Data were obtained from (i) studies already known to environment where the effects are measured (stressful > me; (ii) references in 35 reviews on genetic rescue, out- benign), to be greater for naturally outbreeding than breeding depression and related issues; (iii) 40 inbreeding species and for outbred than inbred immi- advanced level textbooks, research monographs and sci- grants. Genetic rescue effects should be greater in the entific meeting proceedings; (iv) keyword searches for F1 than the F2 and later generations for traits deter- both genetic rescue/heterosis, outbreeding depression mined by the zygotic genotype, but show the opposite and related terms in Google Scholar and Web of Science pattern for traits determined by maternal genotype (see and (v) further references cited within > 400 studies Appendix S2, Supporting information). identified by all the above means. The aims of this study were to determine the follow- The data search revealed 156 comparisons of out- ing: (i) the consistency and magnitude of effects of bred/inbred fitness from 77 taxa (18 invertebrates, 15 outcrossing small inbred populations to another popula- vertebrates and 44 plants) (Table S1, Supporting infor- tion within species (where the cross had a low risk of mation) with references from Darwin (1876) to January outbreeding depression); (ii) variables affecting the 2014. Only fourteen of the taxa were described by the © 2015 John Wiley & Sons Ltd 2612 R. FRANKHAM authors as belonging to a threatened category, and only (see below), (3) data points of (2) that had information a small proportion of crosses were likely performed for on all predictor variables, (4) composite fitness data conservation purposes. Gene flow into inbred popula- with pseudoreplication minimized and (5) data points tions ranged from a single immigrant to crosses with from (4) that had complete information on all predic- several other isolated populations (immigration levels tor variables and restricted to outbreeders (as the of 0.025–0.94). There were only six comparisons found single entry for an inbreeding species was insufficient to for evolutionary potential for fitness traits, all for inver- allow testing of mating system effects). The entries used tebrates (Table S2, Supporting information). in each data set are identified in Table S1 (Supporting information). Pseudoreplication was minimized by reducing the Effect sizes data set to a single entry per inbred/outbred popula- The ratio of mean fitness in outcrossed/inbred popula- tion comparison [usually the one with the greatest sta- tions [genetic
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