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

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

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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.

Original language	English
Article number	107832
Number of pages	18
Journal	iScience
Volume	26
Issue number	10
Early online date	9 Sept 2023
DOIs	https://doi.org/10.1016/j.isci.2023.107832
Publication status	Published - 20 Oct 2023
Externally published	Yes

Bibliographical note

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Funder

This work was supported by a Discovery grant, no. 9408-08 from the Natural Sciences and Engineering Research Council of Canada to S.S.T, National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Number R01AI148551 and National Science Foundation DEB1654417 (to J.B.B. for shared computational resources), B.F. was supported by an EU-H2020 MSCA-IF-2020 fellowship (101024100, TEEPI), M.C.H. was supported by a DFG grant BO2544/11-2 to E.B.B, A.M. was supported by a DFG grant HA8997/1-1 to M.C.H. and S.E. was supported by a Royal Society Dorothy Hodgkin Fellowship (DH140236).

Funding

This work was supported by a Discovery grant, no. 9408-08 from the Natural Sciences and Engineering Research Council of Canada to S.S.T, National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Number R01AI148551 and National Science Foundation DEB1654417 (to J.B.B. for shared computational resources), B.F. was supported by an EU-H2020 MSCA-IF-2020 fellowship (101024100, TEEPI), M.C.H. was supported by a DFG grant BO2544/11-2 to E.B.B, A.M. was supported by a DFG grant HA8997/1-1 to M.C.H. and S.E. was supported by a Royal Society Dorothy Hodgkin Fellowship (DH140236).

Funders	Funder number
Natural Sciences and Engineering Research Council of Canada	9408-08
National Institutes of Health	R01AI148551
National Science Foundation	DEB1654417
European Horizon 2020	101024100
Deutsche Forschungsgemeinschaft	BO2544/11-2, HA8997/1-1
The Royal Society	DH140236

Keywords

Genomics
Evolutionary developmental biology
Transcriptomics

Access to Document

10.1016/j.isci.2023.107832Licence: CC BY-NC-ND

Harrison2023VoRFinal published version, 7.21 MBLicence: CC BY-NC-ND

Cite this

Fouks, B., Harrison, M. C., Mikhailova, A. A., Marchal, E., English, S., Carruthers, M., Jennings, E. C., Chiamaka, E. L., Frigard, R. A., Pippel, M., Attardo, G. M., Benoit, J. B., Bornberg‐Bauer, E., & Tobe, S. S. (2023). Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond. iScience, 26(10), Article 107832. https://doi.org/10.1016/j.isci.2023.107832

Fouks, B, Harrison, MC, Mikhailova, AA, Marchal, E, English, S, Carruthers, M, Jennings, EC, Chiamaka, EL, Frigard, RA, Pippel, M, Attardo, GM, Benoit, JB, Bornberg‐Bauer, E & Tobe, SS 2023, 'Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond', iScience, vol. 26, no. 10, 107832. https://doi.org/10.1016/j.isci.2023.107832

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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.",

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

Abstract

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