Maternal effect obscures adaptation to adverse environments and hinders divergence in Drosophila melanogaster

Abstract

Adaptation to contrasting environments can facilitate ecological divergence and sympatric speciation. Factors that influence the probability and tempo of these processes are poorly known. We performed an evolutionary experiment on Drosophila melanogaster in order to attain better understanding of adaptation dynamics and to model the initial steps of sympatric speciation. In our experiment, several populations are being cultured either on standard rich medium (RM) or on nutrient-deficient starch-based medium (SM). After 10 generations, experimental populations demonstrated unexpected changes in their fitness: on the starch medium, flies grown on RM (FRM) outcompeted those that were cultured on SM (FSM), while on the rich medium, FRM were outcompeted by FSM. That is, experimental populations demonstrated higher fitness on the foreign medium, but were outcompeted by the aliens on the one they had been accustomed to. To explain the paradox, we hypothesize that the observed low fitness of FSM on SM was due to maternal effect, or the "effect of starving mother". The FSM flies are probably better adapted to SM, but the phenotypic outcome of their adaptations is obscured because the females grown on the poor medium invest less in their offspring (for instance, they may produce nutrient-deficient eggs). Larvae hatched from such eggs develop successfully on the rich medium RM, but experience delayed growth and/or lower survival rate on the nutrient-deficient medium SM. To test the hypothesis, we measured the fitness of the flies FSM after culturing them for one generation on RM, in order to remove the assumed maternal effect. As expected, this time FSM demonstrated higher fitness on SM compared to control flies (FRM) and to FSM before the removal of the maternal effect. The results support the idea that non-adaptive phenotypic plasticity and maternal effects can mask adaptation to adverse environments and prohibit ecological divergence and speciation by allowing the migrants from favourable habitats to outcompete resident individuals in adverse ecotopes despite the possible presence of specific adaptations in the latter.