The external rumen of dung beetles: Complex interactions between larvae and their ontogenetic environments shape growth and life history

Organisms are not just passive recipients of environmental pressures but are able to shape the environment they experience. However, the mechanisms and the evolutionary implications of such niche construction remain poorly understood. Larvae of the gazelle dung beetle (Digitonthophagus gazella) extensively modify their environment and benefit from microbial symbionts to digest their cellulose-rich diet. These modifications are so extensive that previous research suggests that dung beetle larvae establish an “external rumen”, where behavioral adaptations promote beneficial symbionts that enhance nutrient availability in the developmental environment. However, the mechanisms underlying these environmental modifications and their impact on species differences remain unclear. To investigate the external rumen hypothesis, we study the impact of larval environmental modifications on adult life-history traits in the dung beetle Digitonthophagus gazella. We did this by transplanting eggs into modified and unmodified environments, whilst excluding maternally derived microbes. Additionally, we include a heterospecific (Onthophagus binodis) manipulated environment to investigate the evolution of species-specific effects. Counter to expectations, we find larval modifications by conspecifics did not confer a benefit to D. gazella in any aspect measured. However, surprisingly, focal from heterospecific treatments emerged significantly quicker. Additionally, we highlight the primary condition of the developmental environment as an essential factor in determining fitness benefits compared to any additive environmental effects. Our research adds to the growing literature on organism-environment interactions and demonstrates that the relationship between dung beetle larvae and their developmental environment is complex and is not consistent with the presence of a simple external rumen.