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
Affiliations
Bertrand Fouks
University of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, Germany
Mark C. Harrison
University of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, Germany
Alina A. Mikhailova
University of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, Germany
Elisabeth Marchal
Department of Biology, Molecular Developmental Physiology and Signal Transduction Lab., Division of Animal Physiology and Neurobiology, Naamsestraat 59-Box 2465, B-3000 Leuven, Belgium
Sinead English
School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK
Madeleine Carruthers
School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK
Emily C. Jennings
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA
Ezemuoka L. Chiamaka
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA
Ronja A. Frigard
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA
Martin Pippel
Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany
Geoffrey M. Attardo
Department of Entomology and Nematology, College of Agriculture and Environmental Sciences, University of California, Davis, Davis, CA, USA
Joshua B. Benoit
Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA; Corresponding author
Erich Bornberg-Bauer
University of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, Germany; Department of Protein Evolution, Max Planck Institute for Biology, Max-Planck-Ring 5, 72076 Tübingen, Germany; Corresponding author
Stephen S. Tobe
Department of Biology, Molecular Developmental Physiology and Signal Transduction Lab., Division of Animal Physiology and Neurobiology, Naamsestraat 59-Box 2465, B-3000 Leuven, Belgium; Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
Summary: 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.
