The legacy of a butterfly's parental microbiome on offspring performance

ABSTRACT

An insect's phenotype can be shaped by experiences made by the parental generation. However, effects of the parental symbiotic microbiome and host plant use on the offspring are unclear. We addressed this gap of knowledge by studying Pieris brassicae, a multivoltine butterfly species feeding on different brassicaceous plants across generations. We investigated how disturbance of the parental bacterial community by an antibiotic treatment affects F1 larval traits. We tested the effects in dependence of whether F1 larvae are feeding on the same or a different plant species than their parents. The parental treatment alone had no impact on the biomass of F1 larvae feeding on the parental plant species. However, the parental treatment had a detrimental effect on F1 larval biomass when F1 larvae experienced a different host plant than their parents. This effect was linked to higher larval prophenoloxidase activity and greater downregulation of a major allergen (MA), a glucosinolate detoxification gene of P. brassicae. Bacterial abundance in untreated adult parents was high, while it was very low in F1 larvae from either parental type, and thus, unlikely to directly influence larval traits. Our results suggest that transgenerational effects of the parental microbiome on the offspring's phenotype become evident when the offspring is exposed to a transgenerational host plant shift.

IMPORTANCE Resident bacterial communities are almost absent in larvae of butterflies, and thus, are unlikely to affect their host. In contrast, adult butterflies contain conspicuous amounts of bacteria. While the host plant and immune state of adult parental butterflies are known to affect offspring traits, it has been unclear whether also the parental microbiome imposes direct effects on the offspring. Here, we show that disturbance of the bacterial community in parental butterflies by an antibiotic treatment has a detrimental effect on those offspring larvae feeding on a different host plant than their parents. Hence, the study indicates that disturbance of an insect's parental microbiome by an antibiotic treatment shapes how the offspring individuals can adjust themselves to a novel host plant.