Abstract

Conservation biologists routinely face the dilemma of keeping small, fragmented populations isolated, wherein inbreeding depression may ensue, or mixing such populations, which may exacerbate population declines via outbreeding depression. The joint evaluation of inbreeding and outbreeding risks in the wild cannot be readily conducted in endangered species, so a suggested ‘safe’ strategy is to mix ecologically and genetically similar populations. To evaluate this strategy, we carried out a reciprocal transplant experiment involving three neighboring populations of endangered Atlantic salmon (Salmo salar) now bred in captivity and maintained in captive and wild environments. Pure, inbred, and outbred (first and second generation) cross types were released and recaptured in the wild to simultaneously test for local adaptation, inbreeding depression, and outbreeding depression. We found little evidence of inbreeding depression after one generation of inbreeding and little evidence of either heterosis or outbreeding depression via genetic incompatibilities after one or two generations of outbreeding. A trend for outbreeding depression via the loss of local adaptation was documented in one of three populations. The effects of inbreeding were not significantly different from the effects of outbreeding. Hence, at the geographic scale evaluated (34–50 km), inbreeding for one generation and outbreeding over two generations may have similar effects on the persistence of small populations. The results further suggested that outbreeding outcomes may be highly variable or unpredictable at small genetic distances. Our work highlights the necessity of evaluating the relative costs of inbreeding and outbreeding in the conservation and management of endangered species on a case-by-case basis.

Highlights

  • Human-induced fragmentation and depletion of many natural populations have resulted in a growing vulnerability to inbreeding depression and a loss of genetic diversity (Frankham 2005)

  • Local adaptation Five months after release, we found a trend for local adaptation in only one of the three populations: ECO

  • ECO did not meet the ‘home versus away’ criterion of local adaptation (Kawecki and Ebert 2004), it is more important to conservation research that ECO performed better than GRV and STW within ECO River (‘local versus foreign’ criterion) than how ECO performed in GRV and STW Rivers (‘home versus away’ criterion)

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Summary

Introduction

Human-induced fragmentation and depletion of many natural populations have resulted in a growing vulnerability to inbreeding depression and a loss of genetic diversity (Frankham 2005). While even low levels of gene flow may restore inbred populations to more demographically and genetically healthy states because of increased heterozygosity (Westermeier et al 1998; Pimm et al 2006), population mixing can result in outbreeding depression, wherein outbred cross types have reduced fitness relative to parental populations (Dobzhansky 1950; Templeton 1986) Such outbreeding depression may be extrinsically based, involving the loss of local adaptation, or intrinsically based through the disruption of coadapted gene complexes – the latter usually does not arise until the second or later outbred generations when full recombination of parental genomes occurs (Edmands 2007). Should one maintain small, fragmented populations, isolated from one another, with the risk that inbreeding depression will ensue? Or should one actively or passively allow populations to interbreed, thereby reducing risks posed by inbreeding depression but increasing the probability of outbreeding depression? While a suggested ‘safe’ strategy may be to mix inbred populations that are as ecologically and genetically similar as possible (Edmands 2007), the joint evaluation of inbreeding and outbreeding in the wild is necessary, but is rarely conducted, to evaluate their relative expected impacts on population viability

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