Legacy of a Butterfly’s Parental Microbiome in Offspring Performance

Abstract

An insect’s phenotype can be influenced by the experiences of the parental generation. However, the 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 antibiotic treatment affects F1 larval traits. We tested the effects depending on whether F1 larvae are feeding on the same plant species as their parents or on a different one. 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 had a different host plant than their parents. This effect was linked to higher larval prophenoloxidase activity and greater downregulation of the major allergen gene (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.

Parasitism by endoparasitoid wasps alters the internal but not the external microbiome in host caterpillars

“…[ 18 , 34 , 39 – 41 ]. In contrast to other studies that found very low bacterial abundances in P. brassicae caterpillars [ 42 ], estimation of the bacterial abundance by qPCR suggested higher bacterial densities in our samples. This was confirmed by plating a selection of samples on trypticase soy agar supplemented with 0.5 g/L cycloheximide (up to10 4 bacterial colony forming units (cfu) per specimen) (Additional file 1 : Table S9).…”

The Gut Microbiome of an Indigenous Agropastoralist Population in a Remote Area of Colombia with High Rates of Gastrointestinal Infections and Dysbiosis

“…We found that changes in relative abundances of genera for the three populations were related to ETEC-positive (Kruskal–Wallis p -value < 9 × 10 −4 ), EAEC-negative ( p -value < 0.0058), and Giardia -positive ( p -value < 0) individuals. Later, we combined the microbiome OTU genera data with all demographic (gender, age, location) and clinical data (BMI, symptoms, presence of pathogens and parasites) to assess the association of the microbiome data with these factors through generalized mixed models [ 48 ]. For simplicity, in these tests we utilized only the differentially abundant genera: Sutterella , Faecalibacterium , Clostridium , Prevotella , Parabacteroides , Butyrivibrio , Dialister , and Odoribacter , and the demographic and clinical data as response variables.…”

The gut bacterial community affects immunity but not metabolism in a specialist herbivorous butterfly

“…To date, evidence of transgenerational effects of the microbiota in insects is in general scarce, this is especially true for Lepidoptera. The impact of parental microbiota on the fitness of their offspring was recently tested in the large cabbage white butterfly, Pieris brassicae (Paniagua Voirol, Weinhold, Johnston, Fatouros, & Hilker, 2020). This study showed that altered microbial community in the mothers has no detrimental effects on the performances of their offspring when both parents and larvae fed the same host plant, but it negatively affects offspring feeding on host plants with higher sinigrin (a defensive metabolite) content than the host plant on which the mothers fed (Paniagua Voirol et al, 2020).…”

“…The impact of parental microbiota on the fitness of their offspring was recently tested in the large cabbage white butterfly, Pieris brassicae (Paniagua Voirol, Weinhold, Johnston, Fatouros, & Hilker, 2020). This study showed that altered microbial community in the mothers has no detrimental effects on the performances of their offspring when both parents and larvae fed the same host plant, but it negatively affects offspring feeding on host plants with higher sinigrin (a defensive metabolite) content than the host plant on which the mothers fed (Paniagua Voirol et al, 2020). The authors suggest that disturbances in the parental microbiota may affect the ability of their offspring to cope with the stress of host plant shift.…”