Inbreeding is generally avoided in animals due to the risk of inbreeding depression following an increase in homozygous deleterious alleles and loss of heterozygosity. Species that regularly inbreed challenge our understanding of the fitness effects of these risks. We investigated fitness consequences of extended inbreeding in the haplodiploid date-stone beetle, Coccotrypes dactyliperda. We hypothesized that continuous inbreeding could result in reduced fitness, while outbreeding would either increase fitness due to heterosis or lower fitness if co-adapted gene complexes are disrupted. We established three breeding treatments with beetles from two geographically separated populations: Sib-mating (inbreeding), and outbreeding within- and between-populations. Between-population outbreeding groups of both populations had lower fecundity and collapsed before the experiment ended, while sib-mated and within-population breeding groups persisted for ten generations. Sib-mated females had higher fecundity than within- and between-population outbreeding females. Inbreeding coefficients of sib-mated groups were higher than the other treatment groups, yet sib-mated beetles remained genetically polymorphic at the population level. Thus, there was no inbreeding depression, while crossing between distant populations led to outbreeding depression. Our findings are consistent with the life history of C. dactyliperda, in which sib-mating predominates within the date seed, but occasional within-population outbreeding may occur following local dispersal.

A breeding experiment over 10 generations with three breeding treatments: sib-mating, outbreeding within a local population, and outbreeding between distant populations.

Variables measured were fecundity and adult body size.

In select generations, genetic markers were used to determine the level of heterozygosity and inbreeding coefficients of beetles in the experimental treatments and in the original populations.

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