Maternal and host effects mediate the adaptive expansion and contraction of the microbiome during ontogeny in a holometabolous, polyphagous insect

Abstract

1. Polyphagous, holometabolous insects adapt to rapid diet shifts imposed by their ecology and their life cycle. One shift is linked to development, as larvae and adults usually dwell and feed in different environments, using different resources.The second is caused by changes in larval hosts, often occurring at each generation. Studies show that the insect's microbiome also changes in relation to development and larval host. However, parental and larval host contributions to its structure and trans-generational dynamics remain uncharted.2. We investigated the sources of variation of the microbiome of the highly polyphagous Mediterranean fruit fly by tracking microbiome structure and its potential functional impact in fly lineages over generations and fruit host shifts, using 16S rRNA gene amplicon single variant analysis.3. Bacterial community alpha-diversity expanded and contracted cyclically in a life stagedependent manner with the mothers' microbiome community 'resetting' to the same structure across generations. Expansion occurred at the larval stage, while alphadiversity decreased in tenerals, and significantly in mothers. In contrast, richness was highest in mothers, with rare taxa expanding in larvae depending upon fruit type. 4. Metabolic predictions using PICRUSt pointed to increased metabolism of vitamins in mothers, and of aromatic compouds in larvae and tenerals, while indicator species analysis suggested fruit host composition-dependent potential functional adaptations. 5. Our data indicate lineage, fruit host and their interactions as the main sources of microbiome variation and provide examples of possible metabolic developmental and ecological adaptations. Taken together, these data support the hypothesis that microbiome diversity and microbiome-driven local adaptations act as a mechanism sustaining polyphagy.

Anna Karenina as a promoter of microbial diversity in the cosmopolitan agricultural pest Zeugodacus cucurbitae (Diptera, Tephritidae)

“…We suggest that the significantly higher α diversity observed in larvae from these farms also reflects the stochastic changes promoted by AKEs in stressed larvae. These results might also be in line with those of Jose et al [ 28 ] who reported higher α diversity in medfly larvae feeding on different fruits and lower diversity in adult mothers (in which they observed a strong bias towards high abundance of few bacterial species). We speculate that the effects related to fruit host in Jose et al [ 28 ] might also have been affected by AKEs, as larvae feeding on heterogeneous crops are allegedly subjected to heterogeneous levels of environmental stress.…”

“…However, in tephritid agricultural pests, a crop effect is not always detectable as the dominant driver of microbial diversity. In fact, other and less obvious processes [ 28 ] and the effects of high spatial heterogeneity [ 29 , 30 ] interact as drivers of microbial diversity and contribute to the variability of patterns observed. The recent work of Jose et al [ 28 ] elegantly demonstrates how crop-induced adaptation and lineage-dependent maternal effects are two interacting drivers of microbial diversity in a cosmopolitan polyphagous fruit fly.…”

“…In fact, other and less obvious processes [ 28 ] and the effects of high spatial heterogeneity [ 29 , 30 ] interact as drivers of microbial diversity and contribute to the variability of patterns observed. The recent work of Jose et al [ 28 ] elegantly demonstrates how crop-induced adaptation and lineage-dependent maternal effects are two interacting drivers of microbial diversity in a cosmopolitan polyphagous fruit fly. The Authors show how microbial diversity in Ceratitis capitata (Wiedemann) expands and contracts cyclically through the insect life stages.…”

“…Bacterial α diversity increases in larvae due to the expansion of rare taxa, while decreases in adults, where the microbial patterns of the maternal stages “reset” to a more uniform structure across generations. Also the microbial patterns described by Jose et al [ 28 ] are very heterogeneous and the Authors suggest that high microbial diversity might facilitate adaptation to the crop (i.e. the environment in which larvae develop), and might contribute to the insect’s polyphagous abilities.…”

“…In this paper, we try and expand this model [sensu 31 ] by verifying if other synergetic processes might promote fruit fly microbial diversity, and facilitate adaptive responses not only to crops but also, and more in general, to changing environmental conditions. In this context, the Anna Karenina principle [ 32 ] might represent an ecological/evolutionary process contributing to the high heterogeneity of microbial communities often observed in larval tephritids [ 28 – 30 ]. The Anna Karenina principle quotes the first lines of Tolstoy’s novel: “All happy families look alike; each unhappy family is unhappy in its own way”.…”