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Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation

BACKGROUND: Hymenoptera comprise extremely diverse insect species with extensive variation in their life histories. The Dryinidae, a family of solitary wasps of Hymenoptera, have evolved innovations that allow them to hunt using venom and a pair of chelae developed from the fore legs that can grasp...

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Autores principales: Yang, Yi, Ye, Xinhai, Dang, Cong, Cao, Yunshen, Hong, Rui, Sun, Yu H., Xiao, Shan, Mei, Yang, Xu, Le, Fang, Qi, Xiao, Huamei, Li, Fei, Ye, Gongyin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8314478/
https://www.ncbi.nlm.nih.gov/pubmed/34315471
http://dx.doi.org/10.1186/s12915-021-01081-6
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author Yang, Yi
Ye, Xinhai
Dang, Cong
Cao, Yunshen
Hong, Rui
Sun, Yu H.
Xiao, Shan
Mei, Yang
Xu, Le
Fang, Qi
Xiao, Huamei
Li, Fei
Ye, Gongyin
author_facet Yang, Yi
Ye, Xinhai
Dang, Cong
Cao, Yunshen
Hong, Rui
Sun, Yu H.
Xiao, Shan
Mei, Yang
Xu, Le
Fang, Qi
Xiao, Huamei
Li, Fei
Ye, Gongyin
author_sort Yang, Yi
collection PubMed
description BACKGROUND: Hymenoptera comprise extremely diverse insect species with extensive variation in their life histories. The Dryinidae, a family of solitary wasps of Hymenoptera, have evolved innovations that allow them to hunt using venom and a pair of chelae developed from the fore legs that can grasp prey. Dryinidae larvae are also parasitoids of Auchenorrhyncha, a group including common pests such as planthoppers and leafhoppers. Both of these traits make them effective and valuable for pest control, but little is yet known about the genetic basis of its dual adaptation to parasitism and predation. RESULTS: We sequenced and assembled a high-quality genome of the dryinid wasp Gonatopus flavifemur, which at 636.5 Mb is larger than most hymenopterans. The expansion of transposable elements, especially DNA transposons, is a major contributor to the genome size enlargement. Our genome-wide screens reveal a number of positively selected genes and rapidly evolving proteins involved in energy production and motor activity, which may contribute to the predatory adaptation of dryinid wasp. We further show that three female-biased, reproductive-associated yellow genes, in response to the prey feeding behavior, are significantly elevated in adult females, which may facilitate the egg production. Venom is a powerful weapon for dryinid wasp during parasitism and predation. We therefore analyze the transcriptomes of venom glands and describe specific expansions in venom Idgf-like genes and neprilysin-like genes. Furthermore, we find the LWS2-opsin gene is exclusively expressed in male G. flavifemur, which may contribute to partner searching and mating. CONCLUSIONS: Our results provide new insights into the genome evolution, predatory adaptation, venom evolution, and sex-biased genes in G. flavifemur, and present genomic resources for future in-depth comparative analyses of hymenopterans that may benefit pest control. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01081-6.
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spelling pubmed-83144782021-07-28 Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation Yang, Yi Ye, Xinhai Dang, Cong Cao, Yunshen Hong, Rui Sun, Yu H. Xiao, Shan Mei, Yang Xu, Le Fang, Qi Xiao, Huamei Li, Fei Ye, Gongyin BMC Biol Research Article BACKGROUND: Hymenoptera comprise extremely diverse insect species with extensive variation in their life histories. The Dryinidae, a family of solitary wasps of Hymenoptera, have evolved innovations that allow them to hunt using venom and a pair of chelae developed from the fore legs that can grasp prey. Dryinidae larvae are also parasitoids of Auchenorrhyncha, a group including common pests such as planthoppers and leafhoppers. Both of these traits make them effective and valuable for pest control, but little is yet known about the genetic basis of its dual adaptation to parasitism and predation. RESULTS: We sequenced and assembled a high-quality genome of the dryinid wasp Gonatopus flavifemur, which at 636.5 Mb is larger than most hymenopterans. The expansion of transposable elements, especially DNA transposons, is a major contributor to the genome size enlargement. Our genome-wide screens reveal a number of positively selected genes and rapidly evolving proteins involved in energy production and motor activity, which may contribute to the predatory adaptation of dryinid wasp. We further show that three female-biased, reproductive-associated yellow genes, in response to the prey feeding behavior, are significantly elevated in adult females, which may facilitate the egg production. Venom is a powerful weapon for dryinid wasp during parasitism and predation. We therefore analyze the transcriptomes of venom glands and describe specific expansions in venom Idgf-like genes and neprilysin-like genes. Furthermore, we find the LWS2-opsin gene is exclusively expressed in male G. flavifemur, which may contribute to partner searching and mating. CONCLUSIONS: Our results provide new insights into the genome evolution, predatory adaptation, venom evolution, and sex-biased genes in G. flavifemur, and present genomic resources for future in-depth comparative analyses of hymenopterans that may benefit pest control. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01081-6. BioMed Central 2021-07-27 /pmc/articles/PMC8314478/ /pubmed/34315471 http://dx.doi.org/10.1186/s12915-021-01081-6 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Yang, Yi
Ye, Xinhai
Dang, Cong
Cao, Yunshen
Hong, Rui
Sun, Yu H.
Xiao, Shan
Mei, Yang
Xu, Le
Fang, Qi
Xiao, Huamei
Li, Fei
Ye, Gongyin
Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
title Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
title_full Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
title_fullStr Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
title_full_unstemmed Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
title_short Genome of the pincer wasp Gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
title_sort genome of the pincer wasp gonatopus flavifemur reveals unique venom evolution and a dual adaptation to parasitism and predation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8314478/
https://www.ncbi.nlm.nih.gov/pubmed/34315471
http://dx.doi.org/10.1186/s12915-021-01081-6
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