Gut microbiota diversity in a dung beetle (Catharsius molossus) across geographical variations and brood ball-mediated microbial transmission

PLoS One. 2024 Jun 21;19(6):e0304908. doi: 10.1371/journal.pone.0304908. eCollection 2024.

Abstract

The dung beetle primarily feeds on the feces of herbivorous animals and play a crucial role in ecological processes like material cycles and soil improvement. This study aims to explore the diversity and composition of the gut microbiota of Catharsius molossus (a renowned dung beetle originating from China and introduced to multiple countries for its ecological value) and exploring whether these gut microbes are transmitted vertically across generations. Using 16S rRNA and ITS rRNA gene sequencing techniques, we described the diversity and composition of gut microbes in C. molossus from different localities and different developmental stages (Egg, young larvae and old larvae). We discovered that the diversity of gut microbiota of dung beetles varied obviously among different geographical localities and different developmental stages, and we also discussed the potential influencing factors. Interestingly, the microbial community structure within the brood balls is more similar to male dung beetle than to that of females, which is consistent with the observation that the brood ball is constructed by the male dung beetle, with the female laying egg in it at the final step. This unique breeding method facilitates offspring in inheriting microbial communities from both the mother and the father. Initially, the larvae's gut microbiota closely mirrors that of the parental gift in these brood balls. As larvae grow, significant changes occur in their gut microbiota, including an increase in symbiotic bacteria like Lactococcus and Enterococcus. Analysis of the gut bacteria of adult dung beetles across various localities and different developmental stages identified nine core genera in adults, contributing to 67.80% of the total microbial abundance, and 11 core genera in beetles at different developmental stages, accounting for 49.13% of the total. Notably, seven genera were common between these two core groups. Our results suggest that Parental gifts can play a role in the vertical transmission of microbes, and the abundance of probiotics increases with larval development, supporting the hypothesis that "larval feeding behavior occurs in two stages: larvae first feed on parental gifts to acquire necessary microbes, then enrich symbiotic microbiota through consuming their own feces."

MeSH terms

  • Animals
  • Bacteria / classification
  • Bacteria / genetics
  • Biodiversity
  • China
  • Coleoptera* / microbiology
  • Female
  • Gastrointestinal Microbiome*
  • Larva* / microbiology
  • Male
  • Phylogeny
  • RNA, Ribosomal, 16S* / genetics

Substances

  • RNA, Ribosomal, 16S

Grants and funding

This work was generously supported by grants from the Science and Technology Department of Yunnan Province, with grant numbers 202302AE090009 and 202204BI090010, and the Lancang-Mekong Cooperation Special Fund Projects, under grant number JiaoWaiSiYa[2020]619. We declare that the sponsors or funders did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The entire research process was conducted independently by the authors, ensuring the integrity and objectivity of the work.