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

Adaptation to contrasting environments can facilitate ecological divergence and sympatric speciation. The factors that influence the probability and rate of these processes are poorly known. We performed an evolutionary experiment on Drosophila melanogaster in order to attain a better understanding of adaptation dynamics and to model the initial steps of sympatric speciation. In our experiment, several populations were cultured either on standard rich medium (MR) or on nutrient-deficient starch-based medium (MS). After ten generations, the experimental populations demonstrated unexpected changes in their fitness: on the starch medium, flies (Drosophila melanogaster, D.m.) grown on MR (D.m._MR) outcompeted those that were cultured on MS, whereas Dm_MR were outcompeted by D.m._MS on the rich medium. That is, experimental populations demonstrated higher fitness on the foreign medium but were outcompeted by the aliens on the medium they were accustomed to. To explain the paradox, we hypothesize that the observed low fitness of D.m._MS on MS was due to maternal effect, or the “effect of the starving mother.” D.m._MS are probably better adapted to MS, 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 MR but experience delayed growth and/or lower survival rate on the nutrient-deficient MS. To test the hypothesis, we measured the fitness of the flies D.m._MS after culturing them for one generation on MR in order to remove the assumed maternal effect. As expected, in this case D.m._MSdemonstrated higher fitness on MR compared to control flies (D.m._MR) and to D.m._MS 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.