Nonadditive indirect effects of group genetic diversity on larval viability in Drosophila melanogaster imply key role of maternal decision-making

Genetic variation can have important consequences for populations: high population genetic diversity is typically associated with ecological success. Some mechanisms that account for these benefits assume that local social groups with high genetic diversity are more successful than low-diversity groups. At the same time, active decision-making by individuals can influence group genetic diversity. Here, we examine how maternal decisions that determine group genetic diversity influence the viability of Drosophila melanogaster larvae. Our groups contained wild-type larvae, whose genetic diversity we manipulated, and genetically marked 'tester' larvae, whose genotype and frequency were identical in all trials. We measured wild-type and tester viability for each group. Surprisingly, the viability of wild-type larvae was neither augmented nor reduced when group genetic diversity was altered. However, the viability of the tester genotype was substantially depressed in large, high-diversity groups. Further, not all high-diversity groups produced this effect: certain combinations of wild-type genotypes were deleterious to tester viability, while other groups of the same diversity-but containing different wild-type genotypes-were not deleterious. These deleterious combinations of wild-type genotypes could not be predicted by observing the performance of the same tester and wild-type genotypes in low-diversity groups. Taken together, these results suggest that nonadditive interactions among genotypes, rather than genetic diversity per se, account for between-group differences in viability in D. melanogaster and that predicting the consequences of genetic diversity at the population level may not be straightforward.