Epistasis and maternal effects in experimental adaptation to chronic nutritional stress inDrosophila

Abstract

Based on ecological and metabolic arguments, some authors predict that adaptation to novel, harsh environments should involve alleles showing negative (diminishing return) epistasis and/or that it should be mediated in part by evolution of maternal effects. Although the first prediction has been supported in microbes, there has been little experimental support for either prediction in multicellular eukaryotes. Here we use a line-cross design to study the genetic architecture of adaptation to chronic larval malnutrition in a population of Drosophila melanogaster that evolved on an extremely nutrient-poor larval food for 84 generations. We assayed three fitness-related traits (developmental rate, adult female weight and egg-to-adult viability) under the malnutrition conditions in 14 crosses between this selected population and a nonadapted control population originally derived from the same base population. All traits showed a pattern of negative epistasis between alleles improving performance under malnutrition. Furthermore, evolutionary changes in maternal traits accounted for half of the 68% increase in viability and for the whole of 8% reduction in adult female body weight in the selected population (relative to unselected controls). These results thus support both of the above predictions and point to the importance of nonadditive effects in adaptive microevolution.

Quantitative genetics of learning ability and resistance to stress inDrosophila melanogaster

“…This is consistent with previous studies, which found large maternal effects on larval development under malnutrition conditions (Vijendravarma et al. ; Vijendravarma and Kawecki ). This is not surprising when considering the uniparental (maternal) heredity of the egg cytoplasm, which is part of the environment for gene expression and nutrition in the early stages of development.…”

“…For both traits which reflect malnutrition toleranceegg-to-adult viability and developmental rate on poor foodthe variance component attributable to parental effects, r 2 m , was similar in magnitude to the variance of genetic effects. This is consistent with previous studies, which found large maternal effects on larval development under malnutrition conditions (Vijendravarma et al 2010;Vijendravarma and Kawecki 2013). This is not surprising when considering the uniparental (maternal) heredity of the egg cytoplasm, which is part of the environment for gene expression and nutrition in the early stages of development.…”

Gut physiology mediates a trade‐off between adaptation to malnutrition and susceptibility to food‐borne pathogens

“…Rather, these results indicate a design trade-off, whereby some aspects of the gut structure or physiology favoured by selection under malnutrition make it more vulnerable to pathogen damage. The fact that the larvae of the selected populations grow faster than control larvae on poor food but not on standard food, (Kolss et al 2009;Vijendravarma & Kawecki 2013) suggests that they are able to acquire nutrients from the poor food at a higher rate. While it remains to be shown directly, it is likely that the gut characteristics which increase the vulnerability of the malnutrition-adapted populations to P. entomophila have evolved because they enhance nutrient acquisition from low-quality food.…”

“…During this experimental evolution, these selected populations became genetically adapted to this regime of chronic larval malnutrition. In particular, their larvae grow substantially faster than those from control populations on the poor (but not standard) food, suggesting that they manage to extract more nutrients from the poor food (Kolss et al 2009;Vijendravarma & Kawecki 2013). These malnutrition-adapted populations thus offer a unique opportunity to study the consequences of adaptation to malnutrition for resistance and tolerance to foodborne pathogens.…”

Characterization of Reproductive Dormancy in Male Drosophila melanogaster

“…Copulation data are shown as a relative number (percentage) of copulation trials among total number of fly couples subjected to copulation (Partridge and Farquhar, 1981). Egg-to-adult viability is the ratio of the total number of emerged adults to the total number of laid eggs (fraction of eggs developing into adulthood) (Vijendravarma and Kawecki, 2013). Data are shown as an average of 6 independent replicates with 5–7 fly couples for each replicate (30–42 males and females).…”