Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum

Amelia R.I. Lindsey; Yogeshwar D. Kelkar; Xin Wu; Dan Sun; Ellen O. Martinson; Zhichao Yan; Paul F. Rugman-Jones; Daniel S.T. Hughes; Shwetha C. Murali; Jiaxin Qu; Shannon Dugan; Sandra L. Lee; Hsu Chao; Huyen Dinh; Yi Han; Harsha Vardhan Doddapaneni; Kim C. Worley; Donna M. Muzny; Gongyin Ye; Richard A. Gibbs; Stephen Richards; Soojin V. Yi; Richard Stouthamer; John H. Werren

doi:10.1186/s12915-018-0520-9

Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum

Amelia R.I. Lindsey, Yogeshwar D. Kelkar, Xin Wu, Dan Sun, Ellen O. Martinson, Zhichao Yan, Paul F. Rugman-Jones, Daniel S.T. Hughes, Shwetha C. Murali, Jiaxin Qu, Shannon Dugan, Sandra L. Lee, Hsu Chao, Huyen Dinh, Yi Han, Harsha Vardhan Doddapaneni, Kim C. Worley, Donna M. Muzny, Gongyin Ye, Richard A. GibbsStephen Richards, Soojin V. Yi, Richard Stouthamer, John H. Werren

Research output: Contribution to journal › Article › peer-review

49 Scopus citations

Abstract

Background: Trichogrammatids are minute parasitoid wasps that develop within other insect eggs. They are less than half a millimeter long, smaller than some protozoans. The Trichogrammatidae are one of the earliest branching families of Chalcidoidea: a diverse superfamily of approximately half a million species of parasitoid wasps, proposed to have evolved from a miniaturized ancestor. Trichogramma are frequently used in agriculture, released as biological control agents against major moth and butterfly pests. Additionally, Trichogramma are well known for their symbiotic bacteria that induce asexual reproduction in infected females. Knowledge of the genome sequence of Trichogramma is a major step towards further understanding its biology and potential applications in pest control. Results: We report the 195-Mb genome sequence of Trichogramma pretiosum and uncover signatures of miniaturization and adaptation in Trichogramma and related parasitoids. Comparative analyses reveal relatively rapid evolution of proteins involved in ribosome biogenesis and function, transcriptional regulation, and ploidy regulation. Chalcids also show loss or especially rapid evolution of 285 gene clusters conserved in other Hymenoptera, including many that are involved in signal transduction and embryonic development. Comparisons between sexual and asexual lineages of Trichogramma pretiosum reveal that there is no strong evidence for genome degradation (e.g., gene loss) in the asexual lineage, although it does contain a lower repeat content than the sexual lineage. Trichogramma shows particularly rapid genome evolution compared to other hymenopterans. We speculate these changes reflect adaptations to miniaturization, and to life as a specialized egg parasitoid. Conclusions: The genomes of Trichogramma and related parasitoids are a valuable resource for future studies of these diverse and economically important insects, including explorations of parasitoid biology, symbiosis, asexuality, biological control, and the evolution of miniaturization. Understanding the molecular determinants of parasitism can also inform mass rearing of Trichogramma and other parasitoids for biological control.

Original language	English (US)
Article number	54
Journal	BMC Biology
Volume	16
Issue number	1
DOIs	https://doi.org/10.1186/s12915-018-0520-9
State	Published - May 18 2018
Externally published	Yes

Bibliographical note

Funding Information:
We thank Bob Schmitz for help with the whole genome bisulfite sequencing. We thank Hans Smid, Eric A. Smith, and three anonymous reviewers for feedback on earlier drafts of the manuscript. We thank the staff at the Baylor College of Medicine HGSC for their contributions, and we acknowledge Monica Poelchau and Christopher Childers for their contributions to the i5k workspace. This work was supported by the National Human Genome Research Institute (U54 HG003273 to RAG); the National Science Foundation (DEB 1501227 to ARIL, DEB 1257053 and IOS 1456233 to JHW, and MCB 1615664 to SVY); the United States Department of Agriculture (NIFA 194617 to RS and NIFA 2016-67011-24778 to ARIL); and Robert and Peggy van den Bosch Memorial Scholarships to ARIL. None of the funding bodies had any role in the design of the study; collection, analysis, and interpretation of data; or in writing of the manuscript

Publisher Copyright:
© 2018 Lindsey et al.

Keywords

Biological control
Chalcidoidea
Comparative genomics
Methylation
Miniaturization
Parthenogenesis
Symbiosis
Wolbachia

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1186/s12915-018-0520-9

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Lindsey, A. R. I., Kelkar, Y. D., Wu, X., Sun, D., Martinson, E. O., Yan, Z., Rugman-Jones, P. F., Hughes, D. S. T., Murali, S. C., Qu, J., Dugan, S., Lee, S. L., Chao, H., Dinh, H., Han, Y., Doddapaneni, H. V., Worley, K. C., Muzny, D. M., Ye, G., ... Werren, J. H. (2018). Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum. BMC Biology, 16(1), Article 54. https://doi.org/10.1186/s12915-018-0520-9

Lindsey, ARI, Kelkar, YD, Wu, X, Sun, D, Martinson, EO, Yan, Z, Rugman-Jones, PF, Hughes, DST, Murali, SC, Qu, J, Dugan, S, Lee, SL, Chao, H, Dinh, H, Han, Y, Doddapaneni, HV, Worley, KC, Muzny, DM, Ye, G, Gibbs, RA, Richards, S, Yi, SV, Stouthamer, R & Werren, JH 2018, 'Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum', BMC Biology, vol. 16, no. 1, 54. https://doi.org/10.1186/s12915-018-0520-9

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abstract = "Background: Trichogrammatids are minute parasitoid wasps that develop within other insect eggs. They are less than half a millimeter long, smaller than some protozoans. The Trichogrammatidae are one of the earliest branching families of Chalcidoidea: a diverse superfamily of approximately half a million species of parasitoid wasps, proposed to have evolved from a miniaturized ancestor. Trichogramma are frequently used in agriculture, released as biological control agents against major moth and butterfly pests. Additionally, Trichogramma are well known for their symbiotic bacteria that induce asexual reproduction in infected females. Knowledge of the genome sequence of Trichogramma is a major step towards further understanding its biology and potential applications in pest control. Results: We report the 195-Mb genome sequence of Trichogramma pretiosum and uncover signatures of miniaturization and adaptation in Trichogramma and related parasitoids. Comparative analyses reveal relatively rapid evolution of proteins involved in ribosome biogenesis and function, transcriptional regulation, and ploidy regulation. Chalcids also show loss or especially rapid evolution of 285 gene clusters conserved in other Hymenoptera, including many that are involved in signal transduction and embryonic development. Comparisons between sexual and asexual lineages of Trichogramma pretiosum reveal that there is no strong evidence for genome degradation (e.g., gene loss) in the asexual lineage, although it does contain a lower repeat content than the sexual lineage. Trichogramma shows particularly rapid genome evolution compared to other hymenopterans. We speculate these changes reflect adaptations to miniaturization, and to life as a specialized egg parasitoid. Conclusions: The genomes of Trichogramma and related parasitoids are a valuable resource for future studies of these diverse and economically important insects, including explorations of parasitoid biology, symbiosis, asexuality, biological control, and the evolution of miniaturization. Understanding the molecular determinants of parasitism can also inform mass rearing of Trichogramma and other parasitoids for biological control.",

keywords = "Biological control, Chalcidoidea, Comparative genomics, Methylation, Miniaturization, Parthenogenesis, Symbiosis, Wolbachia",

author = "Lindsey, {Amelia R.I.} and Kelkar, {Yogeshwar D.} and Xin Wu and Dan Sun and Martinson, {Ellen O.} and Zhichao Yan and Rugman-Jones, {Paul F.} and Hughes, {Daniel S.T.} and Murali, {Shwetha C.} and Jiaxin Qu and Shannon Dugan and Lee, {Sandra L.} and Hsu Chao and Huyen Dinh and Yi Han and Doddapaneni, {Harsha Vardhan} and Worley, {Kim C.} and Muzny, {Donna M.} and Gongyin Ye and Gibbs, {Richard A.} and Stephen Richards and Yi, {Soojin V.} and Richard Stouthamer and Werren, {John H.}",

note = "Funding Information: We thank Bob Schmitz for help with the whole genome bisulfite sequencing. We thank Hans Smid, Eric A. Smith, and three anonymous reviewers for feedback on earlier drafts of the manuscript. We thank the staff at the Baylor College of Medicine HGSC for their contributions, and we acknowledge Monica Poelchau and Christopher Childers for their contributions to the i5k workspace. This work was supported by the National Human Genome Research Institute (U54 HG003273 to RAG); the National Science Foundation (DEB 1501227 to ARIL, DEB 1257053 and IOS 1456233 to JHW, and MCB 1615664 to SVY); the United States Department of Agriculture (NIFA 194617 to RS and NIFA 2016-67011-24778 to ARIL); and Robert and Peggy van den Bosch Memorial Scholarships to ARIL. None of the funding bodies had any role in the design of the study; collection, analysis, and interpretation of data; or in writing of the manuscript Publisher Copyright: {\textcopyright} 2018 Lindsey et al.",

year = "2018",

month = may,

day = "18",

doi = "10.1186/s12915-018-0520-9",

language = "English (US)",

volume = "16",

journal = "BMC Biology",

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TY - JOUR

T1 - Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum

AU - Lindsey, Amelia R.I.

AU - Kelkar, Yogeshwar D.

AU - Wu, Xin

AU - Sun, Dan

AU - Martinson, Ellen O.

AU - Yan, Zhichao

AU - Rugman-Jones, Paul F.

AU - Hughes, Daniel S.T.

AU - Murali, Shwetha C.

AU - Qu, Jiaxin

AU - Dugan, Shannon

AU - Lee, Sandra L.

AU - Chao, Hsu

AU - Dinh, Huyen

AU - Han, Yi

AU - Doddapaneni, Harsha Vardhan

AU - Worley, Kim C.

AU - Muzny, Donna M.

AU - Ye, Gongyin

AU - Gibbs, Richard A.

AU - Richards, Stephen

AU - Yi, Soojin V.

AU - Stouthamer, Richard

AU - Werren, John H.

N1 - Funding Information: We thank Bob Schmitz for help with the whole genome bisulfite sequencing. We thank Hans Smid, Eric A. Smith, and three anonymous reviewers for feedback on earlier drafts of the manuscript. We thank the staff at the Baylor College of Medicine HGSC for their contributions, and we acknowledge Monica Poelchau and Christopher Childers for their contributions to the i5k workspace. This work was supported by the National Human Genome Research Institute (U54 HG003273 to RAG); the National Science Foundation (DEB 1501227 to ARIL, DEB 1257053 and IOS 1456233 to JHW, and MCB 1615664 to SVY); the United States Department of Agriculture (NIFA 194617 to RS and NIFA 2016-67011-24778 to ARIL); and Robert and Peggy van den Bosch Memorial Scholarships to ARIL. None of the funding bodies had any role in the design of the study; collection, analysis, and interpretation of data; or in writing of the manuscript Publisher Copyright: © 2018 Lindsey et al.

PY - 2018/5/18

Y1 - 2018/5/18

N2 - Background: Trichogrammatids are minute parasitoid wasps that develop within other insect eggs. They are less than half a millimeter long, smaller than some protozoans. The Trichogrammatidae are one of the earliest branching families of Chalcidoidea: a diverse superfamily of approximately half a million species of parasitoid wasps, proposed to have evolved from a miniaturized ancestor. Trichogramma are frequently used in agriculture, released as biological control agents against major moth and butterfly pests. Additionally, Trichogramma are well known for their symbiotic bacteria that induce asexual reproduction in infected females. Knowledge of the genome sequence of Trichogramma is a major step towards further understanding its biology and potential applications in pest control. Results: We report the 195-Mb genome sequence of Trichogramma pretiosum and uncover signatures of miniaturization and adaptation in Trichogramma and related parasitoids. Comparative analyses reveal relatively rapid evolution of proteins involved in ribosome biogenesis and function, transcriptional regulation, and ploidy regulation. Chalcids also show loss or especially rapid evolution of 285 gene clusters conserved in other Hymenoptera, including many that are involved in signal transduction and embryonic development. Comparisons between sexual and asexual lineages of Trichogramma pretiosum reveal that there is no strong evidence for genome degradation (e.g., gene loss) in the asexual lineage, although it does contain a lower repeat content than the sexual lineage. Trichogramma shows particularly rapid genome evolution compared to other hymenopterans. We speculate these changes reflect adaptations to miniaturization, and to life as a specialized egg parasitoid. Conclusions: The genomes of Trichogramma and related parasitoids are a valuable resource for future studies of these diverse and economically important insects, including explorations of parasitoid biology, symbiosis, asexuality, biological control, and the evolution of miniaturization. Understanding the molecular determinants of parasitism can also inform mass rearing of Trichogramma and other parasitoids for biological control.

AB - Background: Trichogrammatids are minute parasitoid wasps that develop within other insect eggs. They are less than half a millimeter long, smaller than some protozoans. The Trichogrammatidae are one of the earliest branching families of Chalcidoidea: a diverse superfamily of approximately half a million species of parasitoid wasps, proposed to have evolved from a miniaturized ancestor. Trichogramma are frequently used in agriculture, released as biological control agents against major moth and butterfly pests. Additionally, Trichogramma are well known for their symbiotic bacteria that induce asexual reproduction in infected females. Knowledge of the genome sequence of Trichogramma is a major step towards further understanding its biology and potential applications in pest control. Results: We report the 195-Mb genome sequence of Trichogramma pretiosum and uncover signatures of miniaturization and adaptation in Trichogramma and related parasitoids. Comparative analyses reveal relatively rapid evolution of proteins involved in ribosome biogenesis and function, transcriptional regulation, and ploidy regulation. Chalcids also show loss or especially rapid evolution of 285 gene clusters conserved in other Hymenoptera, including many that are involved in signal transduction and embryonic development. Comparisons between sexual and asexual lineages of Trichogramma pretiosum reveal that there is no strong evidence for genome degradation (e.g., gene loss) in the asexual lineage, although it does contain a lower repeat content than the sexual lineage. Trichogramma shows particularly rapid genome evolution compared to other hymenopterans. We speculate these changes reflect adaptations to miniaturization, and to life as a specialized egg parasitoid. Conclusions: The genomes of Trichogramma and related parasitoids are a valuable resource for future studies of these diverse and economically important insects, including explorations of parasitoid biology, symbiosis, asexuality, biological control, and the evolution of miniaturization. Understanding the molecular determinants of parasitism can also inform mass rearing of Trichogramma and other parasitoids for biological control.

KW - Biological control

KW - Chalcidoidea

KW - Comparative genomics

KW - Methylation

KW - Miniaturization

KW - Parthenogenesis

KW - Symbiosis

KW - Wolbachia

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Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum

Abstract

Bibliographical note

Keywords

UN SDGs

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