Academic journal article Genetics

The Different Sources of Variation in Inbreeding Depression, Heterosis and Outbreeding Depression in a Metapopulation of Physa Acuta

Academic journal article Genetics

The Different Sources of Variation in Inbreeding Depression, Heterosis and Outbreeding Depression in a Metapopulation of Physa Acuta

Article excerpt

ABSTRACT

Understanding how parental distance affects offspring fitness, i.e., the effects of inbreeding and outbreeding in natural populations, is a major goal in evolutionary biology. While inbreeding is often associated with fitness reduction (inbreeding depression), interpopulation outcrossing may have either positive (heterosis) or negative (outbreeding depression) effects. Within a metapopulation, all phenomena may occur with various intensities depending on the focal population (especially its effective size) and the trait studied. However, little is known about interpopulation variation at this scale. We here examine variation in inbreeding depression, heterosis, and outbreeding depression on life-history traits across a full-life cycle, within a metapopulation of the hermaphroditic snail Physa acuta. We show that all three phenomena can co-occur at this scale, although they are not always expressed on the same traits. A large variation in inbreeding depression, heterosis, and outbreeding depression is observed among local populations. We provide evidence that, as expected from theory, small and isolated populations enjoy higher heterosis upon outcrossing than do large, open populations. These results emphasize the need for an integrated theory accounting for the effects of both deleterious mutations and genetic incompatibilities within metapopulations and to take into account the variability of the focal population to understand the genetic consequences of inbreeding and outbreeding at this scale.

THE importance of inbreeding and outbreeding on fitness has been recognized for a long time (Darwin 1876; Dobzhansky 1936; Wright 1937; Crow 1948) and has more recently reclaimed importance on theoretical (Lynch 1991; Schierup and Christiansen 1996; Merilä and Sheldon 1999; Bierne et al. 2002; Edmands and Timmerman 2003; Shpak 2005) and conservational (Frankham 1999; Quilichini et al. 2001; Marr et al. 2002; Tallmon et al. 2004; Aspi et al. 2006; Willi et al. 2007) grounds. It is widely assumed that there is some optimal genetic distance (or degree of relatedness) between parents, above and below which offspring fitness decreases (Price and Waser 1979; Waser 1993). However, little can be predicted about this optimum, essentially because the two sides are explained by different theories and assumed to result from different categories of mutations.

Within populations, mating between relatives (inbreeding) is often associated with reduction in performance when compared to outbreeding, a phenomenon known as inbreeding depression (Charlesworth and Charlesworth 1987, 1999). Inbreeding depression has been observed in most plant and animal species (Husband and Schemske 1996; Crnokrak and Roff 1999; Keller and Waller 2002) and has been usually attributed to the expression of recessive lethal and sublethal mutations maintained in appreciable frequency in large outbred populations (Mukai et al. 1974; Deng et al. 1998; Keller and Waller 2002). To a lesser extent, overdominance (Charlesworth and Charlesworth 1999; Li et al. 2001) and epistasis (Lynch 1991; Lynch andWalsh 1998)may also contribute to the low performance in inbred individuals.

The same category of mutations is thought to be responsible for heterosis, i.e., the higher fitness in interpopulation hybrids compared to offspring of withinpopulation crosses (Lynch and Walsh 1998). Heterosis seems to be mainly produced by the presence of complementary sets of deleterious recessive alleles within both parental populations and the masking of their effects in the F^sub 1^ heterozygotes (Lynch and Walsh 1998; Remington and O'Malley 2000). Such alleles generally have small effects on fitness; hence they can approach fixation by random genetic drift in some isolated populations (Kimura et al. 1963; Lynch 1991; Whitlock et al. 2000). As for inbreeding depression, overdominance and epistatic interactions may also be involved in heterosis (Lynch 1991; Lynch and Walsh 1998). …

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