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.