Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data

Detalhes bibliográficos
Autor(a) principal: Seabra, Sofia G.
Data de Publicação: 2021
Outros Autores: Rodrigues, Ana S. B., Silva, Sara E., Neto, Ana Carina, Pina-Martins, Francisco, Marabuto, Eduardo, Thompson, Vinton, Wilson, Michael R., Yurtsever, Selçuk, Halkka, Antti, Rebelo, Maria Teresa, Borges, Paulo A. V., Quartau, José A., Jiggins, Chris D., Paulo, Octávio S.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.3/6189
Resumo: Understanding patterns of population differentiation and gene flow in insect vectors of plant diseases is crucial for the implementation of management programs of disease. We investigated morphological and genome-wide variation across the distribution range of the spittlebug Philaenus spumarius (Linnaeus, 1758) (Hemiptera, Auchenorrhyncha, Aphrophoridae), presently the most important vector of the plant pathogenic bacterium Xylella fastidiosa Wells et al., 1987 in Europe. We found genome-wide divergence between P. spumarius and a very closely related species, P. tesselatus Melichar, 1899, at RAD sequencing markers. The two species may be identified by the morphology of male genitalia but are not differentiated at mitochondrial COI, making DNA barcoding with this gene ineffective. This highlights the importance of using integrative approaches in taxonomy. We detected admixture between P. tesselatus from Morocco and P. spumarius from the Iberian Peninsula, suggesting gene-flow between them. Within P. spumarius, we found a pattern of isolation-by-distance in European populations, likely acting alongside other factors restricting gene flow. Varying levels of co-occurrence of different lineages, showing heterogeneous levels of admixture, suggest other isolation mechanisms. The transatlantic populations of North America and Azores were genetically closer to the British population analyzed here, suggesting an origin from North-Western Europe, as already detected with mitochondrial DNA. Nevertheless, these may have been produced through different colonization events. We detected SNPs with signatures of positive selection associated with environmental variables, especially related to extremes and range variation in temperature and precipitation. The population genomics approach provided new insights into the patterns of divergence, gene flow and adaptation in these spittlebugs and led to several hypotheses that require further local investigation.
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spelling Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological dataAedeagusPhilaenus spumariusLocal AdaptationPopulation GenomicsRAD SequencingSpecies DivergenceUnderstanding patterns of population differentiation and gene flow in insect vectors of plant diseases is crucial for the implementation of management programs of disease. We investigated morphological and genome-wide variation across the distribution range of the spittlebug Philaenus spumarius (Linnaeus, 1758) (Hemiptera, Auchenorrhyncha, Aphrophoridae), presently the most important vector of the plant pathogenic bacterium Xylella fastidiosa Wells et al., 1987 in Europe. We found genome-wide divergence between P. spumarius and a very closely related species, P. tesselatus Melichar, 1899, at RAD sequencing markers. The two species may be identified by the morphology of male genitalia but are not differentiated at mitochondrial COI, making DNA barcoding with this gene ineffective. This highlights the importance of using integrative approaches in taxonomy. We detected admixture between P. tesselatus from Morocco and P. spumarius from the Iberian Peninsula, suggesting gene-flow between them. Within P. spumarius, we found a pattern of isolation-by-distance in European populations, likely acting alongside other factors restricting gene flow. Varying levels of co-occurrence of different lineages, showing heterogeneous levels of admixture, suggest other isolation mechanisms. The transatlantic populations of North America and Azores were genetically closer to the British population analyzed here, suggesting an origin from North-Western Europe, as already detected with mitochondrial DNA. Nevertheless, these may have been produced through different colonization events. We detected SNPs with signatures of positive selection associated with environmental variables, especially related to extremes and range variation in temperature and precipitation. The population genomics approach provided new insights into the patterns of divergence, gene flow and adaptation in these spittlebugs and led to several hypotheses that require further local investigation.This work was financially supported by Portuguese national funds through FCT-Fundacao para a Ciencia e a Tecnologia, I.P., Portugal: Project PTDC/BIA-BEC/098783/2008; Project FCTPTDC/BIA-BEC/100182/2008; Grant SFRH/BPD/26365/2006 (to Sofia G Seabra); Grant SFRH/BD/73879/2010 (to Ana SB Rodrigues); Contrato de Trabalho Norma Transitoria - DL57/2016/CP1479/(to Sofia G Seabra); cE3c Unit FCT funding in the frame of the project UIDB/00329/2020; CESAM funding UIDP/50017/2020 + UIDB/50017/2020-POCI-01-0145-FEDER-007638; PIDDAC; co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.PeerJRepositório da Universidade dos AçoresSeabra, Sofia G.Rodrigues, Ana S. B.Silva, Sara E.Neto, Ana CarinaPina-Martins, FranciscoMarabuto, EduardoThompson, VintonWilson, Michael R.Yurtsever, SelçukHalkka, AnttiRebelo, Maria TeresaBorges, Paulo A. V.Quartau, José A.Jiggins, Chris D.Paulo, Octávio S.2022-02-12T17:08:32Z2021-062021-06-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.3/6189engSeabra, S.G., Rodrigues, A.S.B., Silva, S.E., Neto, A.C., Pina-Martins, F., Marabuto, E., Thompson, V., Wilson, M.R., Yurtsever, S., Halkka, A., Rebelo, M.T., Borges, P.A.V., Quartau, J.A., Jiggins, C.D. & Paulo, O.S. (2021). Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data. “PeerJ”, 9, e11425. DOI: 10.7717/peerj.1142510.7717/peerj.114252167-8359PMC817691234131518000656971100005info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2022-12-20T14:34:38Zoai:repositorio.uac.pt:10400.3/6189Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T16:28:21.457706Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
title Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
spellingShingle Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
Seabra, Sofia G.
Aedeagus
Philaenus spumarius
Local Adaptation
Population Genomics
RAD Sequencing
Species Divergence
title_short Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
title_full Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
title_fullStr Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
title_full_unstemmed Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
title_sort Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data
author Seabra, Sofia G.
author_facet Seabra, Sofia G.
Rodrigues, Ana S. B.
Silva, Sara E.
Neto, Ana Carina
Pina-Martins, Francisco
Marabuto, Eduardo
Thompson, Vinton
Wilson, Michael R.
Yurtsever, Selçuk
Halkka, Antti
Rebelo, Maria Teresa
Borges, Paulo A. V.
Quartau, José A.
Jiggins, Chris D.
Paulo, Octávio S.
author_role author
author2 Rodrigues, Ana S. B.
Silva, Sara E.
Neto, Ana Carina
Pina-Martins, Francisco
Marabuto, Eduardo
Thompson, Vinton
Wilson, Michael R.
Yurtsever, Selçuk
Halkka, Antti
Rebelo, Maria Teresa
Borges, Paulo A. V.
Quartau, José A.
Jiggins, Chris D.
Paulo, Octávio S.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Repositório da Universidade dos Açores
dc.contributor.author.fl_str_mv Seabra, Sofia G.
Rodrigues, Ana S. B.
Silva, Sara E.
Neto, Ana Carina
Pina-Martins, Francisco
Marabuto, Eduardo
Thompson, Vinton
Wilson, Michael R.
Yurtsever, Selçuk
Halkka, Antti
Rebelo, Maria Teresa
Borges, Paulo A. V.
Quartau, José A.
Jiggins, Chris D.
Paulo, Octávio S.
dc.subject.por.fl_str_mv Aedeagus
Philaenus spumarius
Local Adaptation
Population Genomics
RAD Sequencing
Species Divergence
topic Aedeagus
Philaenus spumarius
Local Adaptation
Population Genomics
RAD Sequencing
Species Divergence
description Understanding patterns of population differentiation and gene flow in insect vectors of plant diseases is crucial for the implementation of management programs of disease. We investigated morphological and genome-wide variation across the distribution range of the spittlebug Philaenus spumarius (Linnaeus, 1758) (Hemiptera, Auchenorrhyncha, Aphrophoridae), presently the most important vector of the plant pathogenic bacterium Xylella fastidiosa Wells et al., 1987 in Europe. We found genome-wide divergence between P. spumarius and a very closely related species, P. tesselatus Melichar, 1899, at RAD sequencing markers. The two species may be identified by the morphology of male genitalia but are not differentiated at mitochondrial COI, making DNA barcoding with this gene ineffective. This highlights the importance of using integrative approaches in taxonomy. We detected admixture between P. tesselatus from Morocco and P. spumarius from the Iberian Peninsula, suggesting gene-flow between them. Within P. spumarius, we found a pattern of isolation-by-distance in European populations, likely acting alongside other factors restricting gene flow. Varying levels of co-occurrence of different lineages, showing heterogeneous levels of admixture, suggest other isolation mechanisms. The transatlantic populations of North America and Azores were genetically closer to the British population analyzed here, suggesting an origin from North-Western Europe, as already detected with mitochondrial DNA. Nevertheless, these may have been produced through different colonization events. We detected SNPs with signatures of positive selection associated with environmental variables, especially related to extremes and range variation in temperature and precipitation. The population genomics approach provided new insights into the patterns of divergence, gene flow and adaptation in these spittlebugs and led to several hypotheses that require further local investigation.
publishDate 2021
dc.date.none.fl_str_mv 2021-06
2021-06-01T00:00:00Z
2022-02-12T17:08:32Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.3/6189
url http://hdl.handle.net/10400.3/6189
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Seabra, S.G., Rodrigues, A.S.B., Silva, S.E., Neto, A.C., Pina-Martins, F., Marabuto, E., Thompson, V., Wilson, M.R., Yurtsever, S., Halkka, A., Rebelo, M.T., Borges, P.A.V., Quartau, J.A., Jiggins, C.D. & Paulo, O.S. (2021). Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data. “PeerJ”, 9, e11425. DOI: 10.7717/peerj.11425
10.7717/peerj.11425
2167-8359
PMC8176912
34131518
000656971100005
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
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