Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond

Bertrand Fouks; Mark C Harrison; Alina A Mikhailova; Elisabeth Marchal; Sinead English; Madeleine Carruthers; Emily C Jennings; Ezemuoka L Chiamaka; Ronja A Frigard; Martin Pippel; Geoffrey M Attardo; Joshua B Benoit; Erich Bornberg-Bauer; Stephen S Tobe

doi:10.1016/j.isci.2023.107832

Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond

iScience. 2023 Sep 9;26(10):107832. doi: 10.1016/j.isci.2023.107832. eCollection 2023 Oct 20.

Authors

Affiliations

¹ University of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, Germany.
² Department of Biology, Molecular Developmental Physiology and Signal Transduction Lab., Division of Animal Physiology and Neurobiology, Naamsestraat 59-Box 2465, B-3000 Leuven, Belgium.
³ School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK.
⁴ Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA.
⁵ Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany.
⁶ Department of Entomology and Nematology, College of Agriculture and Environmental Sciences, University of California, Davis, Davis, CA, USA.
⁷ Department of Protein Evolution, Max Planck Institute for Biology, Max-Planck-Ring 5, 72076 Tübingen, Germany.
⁸ Department of Cell and Systems Biology, University of Toronto, Toronto, Canada.

Abstract

Live birth (viviparity) has arisen repeatedly and independently among animals. We sequenced the genome and transcriptome of the viviparous Pacific beetle-mimic cockroach and performed comparative analyses with two other viviparous insect lineages, tsetse flies and aphids, to unravel the basis underlying the transition to viviparity in insects. We identified pathways undergoing adaptive evolution for insects, involved in urogenital remodeling, tracheal system, heart development, and nutrient metabolism. Transcriptomic analysis of cockroach and tsetse flies revealed that uterine remodeling and nutrient production are increased and the immune response is altered during pregnancy, facilitating structural and physiological changes to accommodate and nourish the progeny. These patterns of convergent evolution of viviparity among insects, together with similar adaptive mechanisms identified among vertebrates, highlight that the transition to viviparity requires changes in urogenital remodeling, enhanced tracheal and heart development (corresponding to angiogenesis in vertebrates), altered nutrient metabolism, and shifted immunity in animal systems.

Keywords: Evolutionary developmental biology; Genomics; Transcriptomics.

Grants and funding

R01 AI148551/AI/NIAID NIH HHS/United States