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The Environmental Dependence of Inbreeding Depression in a Wild Bird Population
Marta Szulkin*, Ben C. Sheldon Department of Zoology, Edward Grey Institute, University of Oxford, Oxford, United Kingdom

Background. Inbreeding depression occurs when the offspring produced as a result of matings between relatives show reduced fitness, and is generally understood as a consequence of the elevatedexpression of deleterious recessive alleles. How inbreeding depression varies across environments is of importance for the evolution of inbreeding avoidance behaviour, and for understanding extinction risks in small populations. However, inbreeding-by-environment (I6E) interactions have rarely been investigated in wild populations. Methodology/Principal Findings. We analysed 41 years of breedingevents from a wild great tit (Parus major) population and used 11 measures of the environment to categorise environments as relatively good or poor, testing whether these measures influenced inbreeding depression. Although inbreeding always, and environmental quality often, significantly affected reproductive success, there was little evidence for statistically significant I6E interactions at thelevel of individual analyses. However, point estimates of the effect of the environment on inbreeding depression were sometimes considerable, and we show that variation in the magnitude of the I6E interaction across environments is consistent with the expectation that this interaction is more marked across environmental axes with a closer link to overall fitness, with the environmental dependenceof inbreeding depression being elevated under such conditions. Hence, our analyses provide evidence for an environmental dependence of the inbreeding6environment interaction: effectively an I6E6E. Conclusions/Significance. Overall, our analyses suggest that I6E interactions may be substantial in wild populations, when measured across relevant environmental contrasts, although their detection forsingle traits may require very large samples, or high rates of inbreeding.
Citation: Szulkin M, Sheldon BC (2007) The Environmental Dependence of Inbreeding Depression in a Wild Bird Population. PLoS ONE 2(10): e1027. doi:10.1371/journal.pone.0001027

INTRODUCTION
Inbreeding depression, caused by the expression of deleterious recessive alleles [1,2], reduces the fitness of homozygous individualsrelative to outbred members of the same population. It is assumed that inbreeding depression is mainly caused by dominance effects– i.e. the expression of recessive deleterious alleles, and not because of a specific advantage of heterozygotes (the overdominance hypothesis) [1,3]. Thus, the strength of inbreeding depression will depend on the genetic load carried by a population. As a consequence,inbreeding depression may not always be visible in inbred individuals, and even within populations it may be environmentally-dependent [4,5]. Interactions between the inbreeding coefficient and an environmental variable on a fitness-related trait (I6E interactions) indicate that, depending on the quality of the environment, inbreeding depression is variable in magnitude. In addition, however,environments differ in their relevance to overall fitness: some environmental factors may strongly influence fitness, whereas others may have only a weak influence on fitness. Evidence from comparisons of the magnitude of dominance variance across characters suggests that this component of genetic variance is larger for traits with a closer link to fitness, such as life-history characters [6]. Giventhat inbreeding depression is more marked for such characters, we should expect that the effect of the environment on inbreeding depression will be greater across environmental axes that themselves explain a greater proportion of fitness variation. Evidence for I6E interactions is accumulating: although some studies have not found evidence for I6E interaction, a recent review by Armbruster and...
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