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

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

18 Citations (Scopus)

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	7 Sept 2023
DOIs	https://doi.org/10.1016/j.isci.2023.107832
Publication status	Published - 20 Oct 2023

Bibliographical note

Funding Information:
We thank David L. Denlinger for comments and suggestions on an early draft of this manuscript and Carsten Kemena, Elias Dohmen, and Anna Grandchamp for their help in troubleshooting the comparative genomics pipeline. 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 ). Stephen S. Tobe sadly passed away during the final production of this manuscript. Dr. Tobe made critical contributions to this article and his work on invertebrate biology has been foundational.

Publisher Copyright:
© 2023 The Author(s)

Keywords

Evolutionary developmental biology
Genomics
Transcriptomics

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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

@article{86eec77b394a4aa3845daf8f7f77b089,

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

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",

author = "Bertrand Fouks and Harrison, \{Mark C.\} and Mikhailova, \{Alina A.\} and Elisabeth Marchal and Sinead English and Madeleine Carruthers and Jennings, \{Emily C.\} and Chiamaka, \{Ezemuoka L.\} and Frigard, \{Ronja A.\} and Martin Pippel and Attardo, \{Geoffrey M.\} and Benoit, \{Joshua B.\} and Erich Bornberg-Bauer and Tobe, \{Stephen S.\}",

note = "Funding Information: We thank David L. Denlinger for comments and suggestions on an early draft of this manuscript and Carsten Kemena, Elias Dohmen, and Anna Grandchamp for their help in troubleshooting the comparative genomics pipeline. 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 ). Stephen S. Tobe sadly passed away during the final production of this manuscript. Dr. Tobe made critical contributions to this article and his work on invertebrate biology has been foundational. Publisher Copyright: {\textcopyright} 2023 The Author(s)",

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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

TY - JOUR

T1 - Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond

AU - Fouks, Bertrand

AU - Harrison, Mark C.

AU - Mikhailova, Alina A.

AU - Marchal, Elisabeth

AU - English, Sinead

AU - Carruthers, Madeleine

AU - Jennings, Emily C.

AU - Chiamaka, Ezemuoka L.

AU - Frigard, Ronja A.

AU - Pippel, Martin

AU - Attardo, Geoffrey M.

AU - Benoit, Joshua B.

AU - Bornberg-Bauer, Erich

AU - Tobe, Stephen S.

N1 - Funding Information: We thank David L. Denlinger for comments and suggestions on an early draft of this manuscript and Carsten Kemena, Elias Dohmen, and Anna Grandchamp for their help in troubleshooting the comparative genomics pipeline. 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 ). Stephen S. Tobe sadly passed away during the final production of this manuscript. Dr. Tobe made critical contributions to this article and his work on invertebrate biology has been foundational. Publisher Copyright: © 2023 The Author(s)

PY - 2023/10/20

Y1 - 2023/10/20

N2 - 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.

AB - 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.

KW - Evolutionary developmental biology

KW - Genomics

KW - Transcriptomics

UR - https://www.scopus.com/pages/publications/85173471903

UR - http://10.1101/2022.02.03.478960

U2 - 10.1016/j.isci.2023.107832

DO - 10.1016/j.isci.2023.107832

M3 - Article (Academic Journal)

C2 - 37829199

SN - 2589-0042

VL - 26

JO - iScience

JF - iScience

IS - 10

M1 - 107832

ER -

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

Abstract

Bibliographical note

Keywords

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