Matrotrophic viviparity constrains microbiome acquisition during gestation in a live-bearing cockroach, Diploptera punctata

Emily C. Jennings, Matthew W. Korthauer, Trinity L. Hamilton, Joshua B. Benoit

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome-development-reproduction dynamics since reproductive modes ranging from oviparity to multiple types of viviparity are found in these animals. One such invertebrate is the live-bearing cockroach, Diploptera punctata. Females carry embryos in their brood sac, which acts as the functional equivalent of the uterus and placenta. In our study, 16S rRNA sequencing was used to characterize maternal and embryonic microbiomes as well as the development of the whole-body microbiome across nymphal development. We identified 50 phyla and 121 classes overall and found that mothers and their developing embryos had significantly different microbial communities. Of particular interest is the notable lack of diversity in the embryonic microbiome, which is comprised exclusively of Blattabacteria, indicating microbial transmission of only this symbiont during gestation. Our analysis of postnatal development reveals that significant amounts of non-Blattabacteria species are not able to colonize newborn D. punctata until melanization, after which the microbial community rapidly and dynamically diversifies. While the role of these microbes during development has not been characterized, Blattabacteria must serve a critical role providing specific micronutrients lacking in milk secretions to the embryos during gestation. This research provides insight into the microbiome development, specifically with relation to viviparity, provisioning of milk-like secretions, and mother–offspring interactions during pregnancy.

Original languageEnglish (US)
Pages (from-to)10601-10614
Number of pages14
JournalEcology and Evolution
Volume9
Issue number18
DOIs
StatePublished - Sep 1 2019

Bibliographical note

Funding Information:
This work was supported by a University of Cincinnati Sigma Xi Grant in Aid of Research and from the University of Cincinnati Wieman Wendell Benedict Fund to E.C.J. Funding and additional support were provided by the University of Cincinnati as a Faculty Development Research Grant, the Ohio Supercomputer Center, and, in part, through the National Science Foundation DEB-1654417 to J.B.B.

Publisher Copyright:
© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

Keywords

  • Diploptera punctata
  • insect
  • live birth
  • microbiome
  • reproduction
  • vertical transmission
  • viviparity

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