Shaping offspring success – Microbial transmission during oviposition, aggregation, and mutualistic interactions as evolutionary precursors to maternal care in Drosophila melanogaster

Drosophila melanogaster is generally regarded as a species that reproduces without parental care. Female flies oviposit on ephemeral substrates such as decaying fruit and then depart, leaving their offspring exposed to microbial competition, resource depletion, and rapid habitat decay. In insects, parental care encompasses traits such as provisioning, guarding, or nest construction that enhance offspring fitness but often reduce parental survival or future reproductive success. It is best understood as a continuum, extending from complete absence of care to highly specialized obligate care, with D. melanogaster classically positioned at the no-care end. Yet even without direct post-oviposition care, female activities can still modify the ontogenetic environment in ways that benefit offspring. This dissertation investigates how D. melanogaster modifies its breeding substrates and how this affects larval survival and development.
Female flies transmitted beneficial yeasts during oviposition. Egg-laying females deposited more yeasts than non-egg-laying females, demonstrating that transmission was associated with reproductive activity rather than incidental shedding. In mono-association assays, these yeasts improved larval survival, thereby confirming their role as facultative dietary symbionts. In this way, oviposition not only introduced offspring to a suitable substrate but also enhanced its baseline resource quality, transforming ephemeral fruits into more dependable ontogenetic environments.
Female aggregation at oviposition sites likely results in the mixing of microbiota from different origins, thereby influencing microbial assembly and shaping community composition and diversity in the substrates. To simulate this process, microbiota from flies reared on different fruits were applied to apple, tomato, and lemon substrates, with larval aggregation effects tested at two densities. Developmental outcomes depended on both microbiota origin and larval density, varying across substrates. In general, high larval density reduced survival and slowed development but increased microbial diversity, except in lemon substrates, where larvae associated with lemon-derived microbiota achieved higher weights regardless of density.
Female flies also vectored the phoretic nematodes Panagrellus redivivoides to oviposition sites, where the nematodes suppressed the growth of filamentous mold fungi such as Botrytis cinerea, Penicillium expansum, and Geotrichum candidum, all potential threats to brood survival. Although females derived no direct benefit, the association stabilized breeding substrates by limiting fungal spread.
Together, these studies show how maternal and social behaviors initiate a cascade of environmentally mediated effects that reshape the ontogenetic environments of D. melanogaster. Through microbial provisioning, aggregation, and the vectoring of nematodes, female flies restructure breeding substrates in ways that reliably enhance offspring survival and, in some contexts, influence growth. What might appear as incidental by-products of reproduction instead emerge as coordinated contributions that link individual behavior to broader community dynamics.
These findings extend beyond offspring success to highlight the broader ecological role of D. melanogaster in ephemeral habitats. By shaping microbial succession, influencing nutrient cycling, and restructuring community assembly within decomposer environments, flies function as ecosystem engineers. Notably, these pathways operate without specialized symbioses; they rely on opportunistic associations assembled anew at each breeding site. Such environmentally mediated effects blur the boundaries between ecological interaction, niche construction, and parental care, demonstrating that these domains overlap and are not discrete.
This work lays a foundation for testing these processes under natural conditions and across ecological communities. Comparative studies of other saprophagous insects and taxa with varying levels of parental care could reveal how widespread such strategies are, clarifying the evolutionary origins of parental investment and the role of insect-microbe interactions in shaping ephemeral habitats.
In conclusion, this dissertation repositions D. melanogaster at an early transitional stage on the parental care continuum, showing that behaviors once regarded as incidental can contribute to environmentally mediated effects that may represent early evolutionary precursors to more complex forms of maternal care.