Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies

Autores
Meredith, Michael; Saint Jean, Gilbert; Egan, Scott P.; Powell, Thomas H. Q.; Hood, Glen R.; Schuler, Hannes; Bruzzese, Daniel J.; Glover, Mary M.; Smith, James J.; Yee, Wee L.; Goughnour, Robert; Rull Gabayet, Juan Antonio; Aluja, Martin; Feder, Jeffrey L.
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear-encoded microsatellites and a wing spot phenotype for cherry-infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed-mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.
Fil: Meredith, Michael. University of Notre Dame-Indiana; Estados Unidos
Fil: Saint Jean, Gilbert. University of Notre Dame-Indiana; Estados Unidos
Fil: Egan, Scott P.. Rice University; Estados Unidos
Fil: Powell, Thomas H. Q.. University of Notre Dame-Indiana; Estados Unidos
Fil: Hood, Glen R.. University of Notre Dame-Indiana; Estados Unidos
Fil: Schuler, Hannes. University of Notre Dame-Indiana; Estados Unidos
Fil: Bruzzese, Daniel J.. University of Notre Dame-Indiana; Estados Unidos
Fil: Glover, Mary M.. University of Notre Dame-Indiana; Estados Unidos
Fil: Smith, James J.. Michigan State University; Estados Unidos
Fil: Yee, Wee L.. Usda-ars; Estados Unidos
Fil: Goughnour, Robert. United States Department of Agriculture. Agricultural Research Service; Argentina
Fil: Rull Gabayet, Juan Antonio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Planta Piloto de Procesos Industriales Microbiológicos; Argentina
Fil: Aluja, Martin. Instituto de Ecología A.c.; México
Fil: Feder, Jeffrey L.. University of Notre Dame-Indiana; Estados Unidos
Materia
ALLOPATRY
CLIMATE CHANGE
ISOLATION BY DISTANCE
MICROSATELLITES
MTDNA
RANGE FRAGMENTATION
RHAGOLETIS CINGULATA
RHAGOLETIS INDIFFERENS
WING SPOT
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/126773

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oai_identifier_str oai:ri.conicet.gov.ar:11336/126773
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) fliesMeredith, MichaelSaint Jean, GilbertEgan, Scott P.Powell, Thomas H. Q.Hood, Glen R.Schuler, HannesBruzzese, Daniel J.Glover, Mary M.Smith, James J.Yee, Wee L.Goughnour, RobertRull Gabayet, Juan AntonioAluja, MartinFeder, Jeffrey L.ALLOPATRYCLIMATE CHANGEISOLATION BY DISTANCEMICROSATELLITESMTDNARANGE FRAGMENTATIONRHAGOLETIS CINGULATARHAGOLETIS INDIFFERENSWING SPOThttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear-encoded microsatellites and a wing spot phenotype for cherry-infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed-mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.Fil: Meredith, Michael. University of Notre Dame-Indiana; Estados UnidosFil: Saint Jean, Gilbert. University of Notre Dame-Indiana; Estados UnidosFil: Egan, Scott P.. Rice University; Estados UnidosFil: Powell, Thomas H. Q.. University of Notre Dame-Indiana; Estados UnidosFil: Hood, Glen R.. University of Notre Dame-Indiana; Estados UnidosFil: Schuler, Hannes. University of Notre Dame-Indiana; Estados UnidosFil: Bruzzese, Daniel J.. University of Notre Dame-Indiana; Estados UnidosFil: Glover, Mary M.. University of Notre Dame-Indiana; Estados UnidosFil: Smith, James J.. Michigan State University; Estados UnidosFil: Yee, Wee L.. Usda-ars; Estados UnidosFil: Goughnour, Robert. United States Department of Agriculture. Agricultural Research Service; ArgentinaFil: Rull Gabayet, Juan Antonio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Planta Piloto de Procesos Industriales Microbiológicos; ArgentinaFil: Aluja, Martin. Instituto de Ecología A.c.; MéxicoFil: Feder, Jeffrey L.. University of Notre Dame-Indiana; Estados UnidosJohn Wiley and Sons Ltd2020-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/126773Meredith, Michael; Saint Jean, Gilbert; Egan, Scott P.; Powell, Thomas H. Q.; Hood, Glen R.; et al.; Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies; John Wiley and Sons Ltd; Ecology and Evolution; 10; 23; 12-2020; 12727-127442045-7758CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/10.1002/ece3.6667info:eu-repo/semantics/altIdentifier/doi/10.1002/ece3.6667info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:05:01Zoai:ri.conicet.gov.ar:11336/126773instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 10:05:01.355CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
title Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
spellingShingle Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
Meredith, Michael
ALLOPATRY
CLIMATE CHANGE
ISOLATION BY DISTANCE
MICROSATELLITES
MTDNA
RANGE FRAGMENTATION
RHAGOLETIS CINGULATA
RHAGOLETIS INDIFFERENS
WING SPOT
title_short Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
title_full Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
title_fullStr Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
title_full_unstemmed Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
title_sort Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
dc.creator.none.fl_str_mv Meredith, Michael
Saint Jean, Gilbert
Egan, Scott P.
Powell, Thomas H. Q.
Hood, Glen R.
Schuler, Hannes
Bruzzese, Daniel J.
Glover, Mary M.
Smith, James J.
Yee, Wee L.
Goughnour, Robert
Rull Gabayet, Juan Antonio
Aluja, Martin
Feder, Jeffrey L.
author Meredith, Michael
author_facet Meredith, Michael
Saint Jean, Gilbert
Egan, Scott P.
Powell, Thomas H. Q.
Hood, Glen R.
Schuler, Hannes
Bruzzese, Daniel J.
Glover, Mary M.
Smith, James J.
Yee, Wee L.
Goughnour, Robert
Rull Gabayet, Juan Antonio
Aluja, Martin
Feder, Jeffrey L.
author_role author
author2 Saint Jean, Gilbert
Egan, Scott P.
Powell, Thomas H. Q.
Hood, Glen R.
Schuler, Hannes
Bruzzese, Daniel J.
Glover, Mary M.
Smith, James J.
Yee, Wee L.
Goughnour, Robert
Rull Gabayet, Juan Antonio
Aluja, Martin
Feder, Jeffrey L.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv ALLOPATRY
CLIMATE CHANGE
ISOLATION BY DISTANCE
MICROSATELLITES
MTDNA
RANGE FRAGMENTATION
RHAGOLETIS CINGULATA
RHAGOLETIS INDIFFERENS
WING SPOT
topic ALLOPATRY
CLIMATE CHANGE
ISOLATION BY DISTANCE
MICROSATELLITES
MTDNA
RANGE FRAGMENTATION
RHAGOLETIS CINGULATA
RHAGOLETIS INDIFFERENS
WING SPOT
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear-encoded microsatellites and a wing spot phenotype for cherry-infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed-mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.
Fil: Meredith, Michael. University of Notre Dame-Indiana; Estados Unidos
Fil: Saint Jean, Gilbert. University of Notre Dame-Indiana; Estados Unidos
Fil: Egan, Scott P.. Rice University; Estados Unidos
Fil: Powell, Thomas H. Q.. University of Notre Dame-Indiana; Estados Unidos
Fil: Hood, Glen R.. University of Notre Dame-Indiana; Estados Unidos
Fil: Schuler, Hannes. University of Notre Dame-Indiana; Estados Unidos
Fil: Bruzzese, Daniel J.. University of Notre Dame-Indiana; Estados Unidos
Fil: Glover, Mary M.. University of Notre Dame-Indiana; Estados Unidos
Fil: Smith, James J.. Michigan State University; Estados Unidos
Fil: Yee, Wee L.. Usda-ars; Estados Unidos
Fil: Goughnour, Robert. United States Department of Agriculture. Agricultural Research Service; Argentina
Fil: Rull Gabayet, Juan Antonio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Planta Piloto de Procesos Industriales Microbiológicos; Argentina
Fil: Aluja, Martin. Instituto de Ecología A.c.; México
Fil: Feder, Jeffrey L.. University of Notre Dame-Indiana; Estados Unidos
description An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear-encoded microsatellites and a wing spot phenotype for cherry-infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed-mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.
publishDate 2020
dc.date.none.fl_str_mv 2020-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/126773
Meredith, Michael; Saint Jean, Gilbert; Egan, Scott P.; Powell, Thomas H. Q.; Hood, Glen R.; et al.; Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies; John Wiley and Sons Ltd; Ecology and Evolution; 10; 23; 12-2020; 12727-12744
2045-7758
CONICET Digital
CONICET
url http://hdl.handle.net/11336/126773
identifier_str_mv Meredith, Michael; Saint Jean, Gilbert; Egan, Scott P.; Powell, Thomas H. Q.; Hood, Glen R.; et al.; Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies; John Wiley and Sons Ltd; Ecology and Evolution; 10; 23; 12-2020; 12727-12744
2045-7758
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/10.1002/ece3.6667
info:eu-repo/semantics/altIdentifier/doi/10.1002/ece3.6667
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv John Wiley and Sons Ltd
publisher.none.fl_str_mv John Wiley and Sons Ltd
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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