Spatially Varying Wolbachia Frequencies Reveal the Invasion Origin of an Agricultural Pest Recently Introduced From Europe to North America

IF 3.5 2区 生物学 Q1 EVOLUTIONARY BIOLOGY Evolutionary Applications Pub Date : 2024-09-20 DOI:10.1111/eva.70016
Sonja Lečić, Thomas M. Wolfe, Animesh Ghosh, Serdar Satar, Camilla Souza Beraldo, Emily Smith, Jason J. Dombroskie, Emily Jernigan, Glen Ray Hood, Hannes Schuler, Christian Stauffer
{"title":"Spatially Varying Wolbachia Frequencies Reveal the Invasion Origin of an Agricultural Pest Recently Introduced From Europe to North America","authors":"Sonja Lečić,&nbsp;Thomas M. Wolfe,&nbsp;Animesh Ghosh,&nbsp;Serdar Satar,&nbsp;Camilla Souza Beraldo,&nbsp;Emily Smith,&nbsp;Jason J. Dombroskie,&nbsp;Emily Jernigan,&nbsp;Glen Ray Hood,&nbsp;Hannes Schuler,&nbsp;Christian Stauffer","doi":"10.1111/eva.70016","DOIUrl":null,"url":null,"abstract":"<p>The introduction of non-native species across the world represents a major global challenge. Retracing invasion origin is an important first step in understanding the invasion process, often requiring detailed sampling within the native range. Insect species frequently host <i>Wolbachia</i>, a widespread endosymbiotic bacterium that manipulates host reproduction to increase infected female fitness. Here, we draw on the spatial variation in infection frequencies of an actively spreading <i>Wolbachia</i> strain <i>w</i>Cer2 to investigate the invasion origin of the European cherry fruit fly, <i>Rhagoletis cerasi.</i> This pest of cherries was introduced from Europe to North America within the last decade. First, we screen the introduced fly population for the presence of <i>Wolbachia</i>. The introduced populations lack the <i>w</i>Cer2 strain and the strongly associated mitochondrial haplotype, suggesting strain absence due to founder effects with invading individuals originating from <i>w</i>Cer2-uninfected native population(s). To narrow down geographic regions of invasion origin, we perform spatial interpolation of the <i>w</i>Cer2 infection frequency across the native range and predict the infection frequency in unsampled regions. For this, we use an extensive dataset of <i>R. cerasi</i> infection covering 238 populations across Europe over 25 years, complemented with 14 additional populations analyzed for this study. We find that <i>R. cerasi</i> was unlikely introduced from <i>w</i>Cer2-infected populations in Central and Western Europe. We propose <i>w</i>Cer2-uninfected populations from Eastern Europe and the Mediterranean region as the most likely candidates for the invasion origin. This work utilizes <i>Wolbachia</i> as an indirect instrument to provide insights into the invasion source of <i>R. cerasi</i> in North America, revealing yet another application for this multifaceted heritable endosymbiont. Given the prevalence of biological invasions, rapidly uncovering invasion origins gives fundamental insights into how invasive species adapt to new environments.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2024-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70016","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Evolutionary Applications","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/eva.70016","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"EVOLUTIONARY BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

The introduction of non-native species across the world represents a major global challenge. Retracing invasion origin is an important first step in understanding the invasion process, often requiring detailed sampling within the native range. Insect species frequently host Wolbachia, a widespread endosymbiotic bacterium that manipulates host reproduction to increase infected female fitness. Here, we draw on the spatial variation in infection frequencies of an actively spreading Wolbachia strain wCer2 to investigate the invasion origin of the European cherry fruit fly, Rhagoletis cerasi. This pest of cherries was introduced from Europe to North America within the last decade. First, we screen the introduced fly population for the presence of Wolbachia. The introduced populations lack the wCer2 strain and the strongly associated mitochondrial haplotype, suggesting strain absence due to founder effects with invading individuals originating from wCer2-uninfected native population(s). To narrow down geographic regions of invasion origin, we perform spatial interpolation of the wCer2 infection frequency across the native range and predict the infection frequency in unsampled regions. For this, we use an extensive dataset of R. cerasi infection covering 238 populations across Europe over 25 years, complemented with 14 additional populations analyzed for this study. We find that R. cerasi was unlikely introduced from wCer2-infected populations in Central and Western Europe. We propose wCer2-uninfected populations from Eastern Europe and the Mediterranean region as the most likely candidates for the invasion origin. This work utilizes Wolbachia as an indirect instrument to provide insights into the invasion source of R. cerasi in North America, revealing yet another application for this multifaceted heritable endosymbiont. Given the prevalence of biological invasions, rapidly uncovering invasion origins gives fundamental insights into how invasive species adapt to new environments.

Abstract Image

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
空间变化的沃尔巴克氏体频率揭示了最近从欧洲引入北美的一种农业害虫的入侵起源
非本地物种在世界各地的引入是一项重大的全球性挑战。追溯入侵起源是了解入侵过程的重要第一步,通常需要在原生地进行详细取样。昆虫物种经常寄生沃尔巴克氏菌,这是一种广泛存在的内共生细菌,可操纵宿主的繁殖以提高受感染雌虫的适应性。在这里,我们利用积极传播的沃尔巴奇菌株 wCer2 感染频率的空间变化来研究欧洲樱桃果蝇(Rhagoletis cerasi)的入侵起源。这种樱桃害虫是在过去十年中从欧洲引入北美的。首先,我们对引进的蝇种群进行了沃尔巴克氏体筛选。引入的种群缺乏 wCer2 菌株和与之密切相关的线粒体单倍型,这表明菌株的缺失是由于来自未感染 wCer2 的本地种群的入侵个体的创始效应造成的。为了缩小入侵起源的地理区域,我们对整个原生种群的 wCer2 感染频率进行了空间插值,并预测了未采样区域的感染频率。为此,我们使用了一个广泛的 R. cerasi 感染数据集,该数据集覆盖了欧洲 238 个种群,历时 25 年,本研究还分析了另外 14 个种群。我们发现,R. cerasi不太可能是从中欧和西欧的 wCer2 感染种群中引入的。我们认为东欧和地中海地区未感染 wCer2 的种群最有可能是入侵源。这项研究利用沃尔巴克氏体作为间接工具,深入分析了北美 R. cerasi 的入侵来源,揭示了这种多方面遗传内生共生体的另一种应用。鉴于生物入侵的普遍性,快速揭示入侵源可从根本上了解入侵物种如何适应新环境。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Evolutionary Applications
Evolutionary Applications 生物-进化生物学
CiteScore
8.50
自引率
7.30%
发文量
175
审稿时长
6 months
期刊介绍: Evolutionary Applications is a fully peer reviewed open access journal. It publishes papers that utilize concepts from evolutionary biology to address biological questions of health, social and economic relevance. Papers are expected to employ evolutionary concepts or methods to make contributions to areas such as (but not limited to): medicine, agriculture, forestry, exploitation and management (fisheries and wildlife), aquaculture, conservation biology, environmental sciences (including climate change and invasion biology), microbiology, and toxicology. All taxonomic groups are covered from microbes, fungi, plants and animals. In order to better serve the community, we also now strongly encourage submissions of papers making use of modern molecular and genetic methods (population and functional genomics, transcriptomics, proteomics, epigenetics, quantitative genetics, association and linkage mapping) to address important questions in any of these disciplines and in an applied evolutionary framework. Theoretical, empirical, synthesis or perspective papers are welcome.
期刊最新文献
Tracking the North American Asian Longhorned Beetle Invasion With Genomics Prioritizing Conservation Areas for the Hyacinth Macaw (Anodorhynchus hyacinthinus) in Brazil From Low-Coverage Genomic Data Genomic Data Support the Revision of Provenance Regions Delimitation for Scots Pine Sex Pheromone Mediates Resource Partitioning Between Drosophila melanogaster and D. suzukii Estimating Demographic Parameters for Bearded Seals, Erignathus barbatus, in Alaska Using Close-Kin Mark-Recapture Methods
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1