Rapid Loss of Nutritional Symbionts in an Endemic Hawaiian Herbivore Radiation Is Associated with Plant Galling Habit.

IF 11 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular biology and evolution Pub Date : 2024-09-04 DOI:10.1093/molbev/msae190
Allison K Hansen, Jacob A Argondona, Sen Miao, Diana M Percy, Patrick H Degnan
{"title":"Rapid Loss of Nutritional Symbionts in an Endemic Hawaiian Herbivore Radiation Is Associated with Plant Galling Habit.","authors":"Allison K Hansen, Jacob A Argondona, Sen Miao, Diana M Percy, Patrick H Degnan","doi":"10.1093/molbev/msae190","DOIUrl":null,"url":null,"abstract":"<p><p>Insect herbivores frequently cospeciate with symbionts that enable them to survive on nutritionally unbalanced diets. While ancient symbiont gain and loss events have been pivotal for insect diversification and feeding niche specialization, evidence of recent events is scarce. We examine the recent loss of nutritional symbionts (in as little as 1 MY) in sap-feeding Pariaconus, an endemic Hawaiian insect genus that has undergone adaptive radiation, evolving various galling and free-living ecologies on a single host-plant species, Metrosideros polymorpha within the last ∼5 MY. Using 16S rRNA sequencing, we investigated the bacterial microbiomes of 19 Pariaconus species and identified distinct symbiont profiles associated with specific host-plant ecologies. Phylogenetic analyses and metagenomic reconstructions revealed significant differences in microbial diversity and functions among psyllids with different host-plant ecologies. Within a few millions of years, Pariaconus species convergently evolved the closed-gall habit twice. This shift to enclosed galls coincided with the loss of the Morganella-like symbiont that provides the essential amino acid arginine to free-living and open-gall sister species. After the Pariaconus lineage left Kauai and colonized younger islands, both open- and closed-gall species lost the Dickeya-like symbiont. This symbiont is crucial for synthesizing essential amino acids (phenylalanine, tyrosine, and lysine) as well as B vitamins in free-living species. The recurrent loss of these symbionts in galling species reinforces evidence that galls are nutrient sinks and, combined with the rapidity of the evolutionary timeline, highlights the dynamic role of insect-symbiont relationships during the diversification of feeding ecologies. We propose new Candidatus names for the novel Morganella-like and Dickeya-like symbionts.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0000,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11425488/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular biology and evolution","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/molbev/msae190","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Insect herbivores frequently cospeciate with symbionts that enable them to survive on nutritionally unbalanced diets. While ancient symbiont gain and loss events have been pivotal for insect diversification and feeding niche specialization, evidence of recent events is scarce. We examine the recent loss of nutritional symbionts (in as little as 1 MY) in sap-feeding Pariaconus, an endemic Hawaiian insect genus that has undergone adaptive radiation, evolving various galling and free-living ecologies on a single host-plant species, Metrosideros polymorpha within the last ∼5 MY. Using 16S rRNA sequencing, we investigated the bacterial microbiomes of 19 Pariaconus species and identified distinct symbiont profiles associated with specific host-plant ecologies. Phylogenetic analyses and metagenomic reconstructions revealed significant differences in microbial diversity and functions among psyllids with different host-plant ecologies. Within a few millions of years, Pariaconus species convergently evolved the closed-gall habit twice. This shift to enclosed galls coincided with the loss of the Morganella-like symbiont that provides the essential amino acid arginine to free-living and open-gall sister species. After the Pariaconus lineage left Kauai and colonized younger islands, both open- and closed-gall species lost the Dickeya-like symbiont. This symbiont is crucial for synthesizing essential amino acids (phenylalanine, tyrosine, and lysine) as well as B vitamins in free-living species. The recurrent loss of these symbionts in galling species reinforces evidence that galls are nutrient sinks and, combined with the rapidity of the evolutionary timeline, highlights the dynamic role of insect-symbiont relationships during the diversification of feeding ecologies. We propose new Candidatus names for the novel Morganella-like and Dickeya-like symbionts.

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
夏威夷特有食草动物辐射中营养共生体的快速丧失与植物啃咬习性有关。
昆虫食草动物经常与共生体共生,使它们能够在营养不均衡的食物中生存。虽然古代共生体的增殖和丧失对昆虫的多样化和食性特化至关重要,但近期共生体丧失的证据却很少。我们研究了夏威夷特有的食树液昆虫 Pariaconus 最近的营养共生体丧失情况(短短 1 个千年),该昆虫属经历了适应性辐射,在过去的∼5 个千年中在单一寄主植物 Metrosideros polymorpha 上进化出了各种啃食和自由生活生态。通过 16S rRNA 测序,我们研究了 19 个蝇蛆属物种的细菌微生物组,并确定了与特定寄主植物生态相关的不同共生体特征。系统发育分析和元基因组重建显示,不同寄主植物生态环境下的银铃虫在微生物多样性和功能方面存在显著差异。在几个千年内,Pariaconus 的物种两次趋同地进化出封闭的虫瘿习性。在向密闭虫瘿进化的同时,为自由生活和露瘿姊妹种提供必需氨基酸精氨酸的摩根菌类共生体也消失了。当 Pariaconus 一族离开可爱岛并移居到更小的岛屿上后,开放型和封闭型瘿蚊物种都失去了 Dickeya 类共生体。这种共生体对自由生活物种合成必需氨基酸(苯丙氨酸、酪氨酸、赖氨酸)和 B 维生素至关重要。这些共生体在有虫瘿物种中的反复丧失加强了虫瘿是营养汇的证据,再加上进化时间线的快速性,突出了昆虫-共生体关系在取食生态多样化过程中的动态作用。我们为新的类摩根菌共生体和类Dickeya共生体提出了新的Candidatus名称。
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
Molecular biology and evolution
Molecular biology and evolution 生物-进化生物学
CiteScore
19.70
自引率
3.70%
发文量
257
审稿时长
1 months
期刊介绍: Molecular Biology and Evolution Journal Overview: Publishes research at the interface of molecular (including genomics) and evolutionary biology Considers manuscripts containing patterns, processes, and predictions at all levels of organization: population, taxonomic, functional, and phenotypic Interested in fundamental discoveries, new and improved methods, resources, technologies, and theories advancing evolutionary research Publishes balanced reviews of recent developments in genome evolution and forward-looking perspectives suggesting future directions in molecular evolution applications.
期刊最新文献
Conjugation mediates large-scale chromosomal transfer in Streptomyces driving diversification of antibiotic biosynthetic gene clusters. Multiple-wave admixture and adaptive evolution of the Pamirian Wakhi people. Integrating contact tracing data to enhance outbreak phylodynamic inference: a deep learning approach. Rewiring of uric acid metabolism in the intestine promotes high-altitude hypoxia adaptation in humans. Specialization restricts the evolutionary paths available to yeast sugar transporters.
×
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