Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond
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 bas...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | iScience |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223019090 |
| _version_ | 1797647832034836480 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Bertrand Fouks |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-11T15:23:18Z |
| format | Article |
| id | doaj.art-94af9dc0ec1e4b2ea626cda2bc856a4e |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-11T15:23:18Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-94af9dc0ec1e4b2ea626cda2bc856a4e2023-10-28T05:08:41ZengElsevieriScience2589-00422023-10-012610107832Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyondBertrand Fouks0Mark C. Harrison1Alina A. Mikhailova2Elisabeth Marchal3Sinead English4Madeleine Carruthers5Emily C. Jennings6Ezemuoka L. Chiamaka7Ronja A. Frigard8Martin Pippel9Geoffrey M. Attardo10Joshua B. Benoit11Erich Bornberg-Bauer12Stephen S. Tobe13University of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, GermanyUniversity of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, GermanyUniversity of Münster, Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Hüfferstrasse 1, 48149 Münster, GermanyDepartment of Biology, Molecular Developmental Physiology and Signal Transduction Lab., Division of Animal Physiology and Neurobiology, Naamsestraat 59-Box 2465, B-3000 Leuven, BelgiumSchool of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UKSchool of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UKDepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USADepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USADepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USAMax Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, GermanyDepartment of Entomology and Nematology, College of Agriculture and Environmental Sciences, University of California, Davis, Davis, CA, USADepartment of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA; Corresponding authorUniversity 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 authorDepartment 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, CanadaSummary: 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.http://www.sciencedirect.com/science/article/pii/S2589004223019090GenomicsEvolutionary developmental biologyTranscriptomics |
| spellingShingle | 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 Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond iScience Genomics Evolutionary developmental biology Transcriptomics |
| title | Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond |
| title_full | Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond |
| title_fullStr | Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond |
| title_full_unstemmed | Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond |
| title_short | Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond |
| title_sort | live bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond |
| topic | Genomics Evolutionary developmental biology Transcriptomics |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223019090 |
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