Between-partner concordance of vertically transmitted gut microbiota diminishes reproductive output in the dung beetle Onthophagus taurus

Abstract

In this study, we explored the potential contribution of the gut microbiome to reproductive isolation in tunnelling dung beetles, using Onthophagus taurus (Schreber, 1759) and its sister species O. illyricus (Scopoli, 1763) as a model system (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini). Gut microbiota play critical roles in normative development of these beetles, and are vertically inherited via a maternally derived faecal pellet called the pedestal. We first compared the developmental outcomes of individuals reared with pedestals derived from either the same or the sister species (Self and Cross inoculation treatments, respectively). We then crossed the resulting adult O. taurus in three combinations (Self female X Self male; Self female X Cross male; Cross female X Self male). We predicted that if the vertically transmitted gut microbiome plays a role in reproductive isolation by facilitating species recognition, the Self X Self line would have improved reproductive outcomes compared to the lines in which partners had mismatched gut microbiomes. Instead, we found that between-partner concordance of maternally transmitted gut microbiota resulted in fewer offspring, and that this reduction was due to partial pre-copulatory isolation as evidenced by reduced sperm transfer in the Self X Self line. This pattern is consistent either with microbiome-mediated familiarity/kin recognition, or with absence of mate choice in crosses with mismatched microbiomes. We discuss our results in the light of recent research on the influence of extracellular microbial symbionts over insects' mating preferences.