Transmission of beneficial yeasts accompanies offspring production in Drosophila – an initial evolutionary stage of insect maternal care through manipulation of microbial load?

Parent-to-offspring transmission of beneficial microorganisms is
intimately interwoven with the evolution of social behaviors. Ancestral
stages of complex sociality-microbe vectoring interrelationships may be
characterized by high costs of intensive parental care and hence only a
weak link between the transmission of microbial symbionts and offspring
production. We investigate the relationship between yeast symbiont
transmission and egg-laying, as well as some general factors thought to
drive the 'farming' of microscopic fungi by the fruit fly
Drosophila melanogaster, an insect with no obvious parental care but which
is highly dependent on dietary microbes during offspring development. The
process of transmitting microbes involves flies ingesting microbes from
their previous environment, storing and vectoring them, and finally
depositing them in a new environment. This study revealed that fecal
materials of adult flies play a significant role in this process, as they
contain viable yeast cells that support larval development. During single
patch visits, egg-laying female flies transmitted more yeast cells than
non-egg-laying females, suggesting that dietary symbiont transmission is
not random, but linked to offspring production. The crop, an extension of
the foregut, was identified as an organ capable of storing viable yeast
cells during travel between egg-laying sites. However, the amount of yeast
in the crop reduced rapidly during periods of starvation. Although females
starved for 24 hours deposited a smaller amount of yeast than those
starved for 6 hours, the yeast inoculum produced still promoted the
development of larval offspring. The results of these experiments suggest
that female Drosophila fruit flies have the ability to store and regulate
the transfer of microorganisms beneficial to their offspring via the
shedding of fecal material. We argue that our observation may represent an
initial evolutionary stage of maternal care through the manipulation of
microbial load, from which more specialized feedbacks of sociality and
microbe management may evolve.