Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas

Autores
Calfee, Erin; Agra, Marcelo Nicolás; Palacio, María Alejandra; Ramirez, Santiago; Coop, Graham
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Recent biological invasions offer ‘natural’ laboratories to understand the genetics and ecology of adaptation, hybridization, and range limits. One of the most impressive and well-documented biological invasions of the 20th century began in 1957 when Apis mellifera scutellata honey bees swarmed out of managed experimental colonies in Brazil. This newly-imported subspecies, native to southern and eastern Africa, both hybridized with and out-competed previously-introduced European honey bee subspecies. Populations of scutellata-European hybrid honey bees rapidly expanded and spread across much of the Americas in less than 50 years. We use broad geographic sampling and whole genome sequencing of over 300 bees to map the distribution of scutellata ancestry where the northern and southern invasions have presently stalled, forming replicated hybrid zones with European bee populations in California and Argentina. California is much farther from Brazil, yet these hybrid zones occur at very similar latitudes, consistent with the invasion having reached a climate barrier. At these range limits, we observe genome-wide clines for scutellata ancestry, and parallel clines for wing length that span hundreds of kilometers, supporting a smooth transition from climates favoring scutellata-European hybrid bees to climates where they cannot survive winter. We find no large effect loci maintaining exceptionally steep ancestry transitions. Instead, we find most individual loci have concordant ancestry clines across South America, with a build-up of somewhat steeper clines in regions of the genome with low recombination rates, consistent with many loci of small effect contributing to climate-associated fitness trade-offs. Additionally, we find no substantial reductions in genetic diversity associated with rapid expansions nor complete dropout of scutellata ancestry at any individual loci on either continent, which suggests that the competitive fitness advantage of scutellata ancestry at lower latitudes has a polygenic basis and that scutellata-European hybrid bees maintained large population sizes during their invasion. To test for parallel selection across continents, we develop a null model that accounts for drift in ancestry frequencies during the rapid expansion. We identify several peaks within a larger genomic region where selection has pushed scutellata ancestry to high frequency hundreds of kilometers past the present cline centers in both North and South America and that may underlie high-fitness traits driving the invasion.
EEA Balcarce
Fil: Calfee, Erin. University of California. Department of Evolution and Ecology. Center for Population Biology; Estados Unidos
Fil: Agra, Marcelo Nicolás. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Balcarce; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias; Argentina.
Fil: Palacio, María Alejandra. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Balcarce; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias; Argentina.
Fil: Ramírez, Santiago. University of California. Department of Evolution and Ecology. Center for Population Biology; Estados Unidos
Fil: Coop, Graham. University of California. Department of Evolution and Ecology . Center for Population Biology; Estados Unidos
Fuente
PLoS Genetics 16 (10) : e1009038 (2020)
Materia
Abeja Africanizada
Apis Mellifera Scutellata
Hibridación
Invasión
Américas
Africanized Bees
Hibridization
Encroachment
Americas
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
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spelling Selection and hybridization shaped the rapid spread of African honey bee ancestry in the AmericasCalfee, ErinAgra, Marcelo NicolásPalacio, María AlejandraRamirez, SantiagoCoop, GrahamAbeja AfricanizadaApis Mellifera ScutellataHibridaciónInvasiónAméricasAfricanized BeesHibridizationEncroachmentAmericasRecent biological invasions offer ‘natural’ laboratories to understand the genetics and ecology of adaptation, hybridization, and range limits. One of the most impressive and well-documented biological invasions of the 20th century began in 1957 when Apis mellifera scutellata honey bees swarmed out of managed experimental colonies in Brazil. This newly-imported subspecies, native to southern and eastern Africa, both hybridized with and out-competed previously-introduced European honey bee subspecies. Populations of scutellata-European hybrid honey bees rapidly expanded and spread across much of the Americas in less than 50 years. We use broad geographic sampling and whole genome sequencing of over 300 bees to map the distribution of scutellata ancestry where the northern and southern invasions have presently stalled, forming replicated hybrid zones with European bee populations in California and Argentina. California is much farther from Brazil, yet these hybrid zones occur at very similar latitudes, consistent with the invasion having reached a climate barrier. At these range limits, we observe genome-wide clines for scutellata ancestry, and parallel clines for wing length that span hundreds of kilometers, supporting a smooth transition from climates favoring scutellata-European hybrid bees to climates where they cannot survive winter. We find no large effect loci maintaining exceptionally steep ancestry transitions. Instead, we find most individual loci have concordant ancestry clines across South America, with a build-up of somewhat steeper clines in regions of the genome with low recombination rates, consistent with many loci of small effect contributing to climate-associated fitness trade-offs. Additionally, we find no substantial reductions in genetic diversity associated with rapid expansions nor complete dropout of scutellata ancestry at any individual loci on either continent, which suggests that the competitive fitness advantage of scutellata ancestry at lower latitudes has a polygenic basis and that scutellata-European hybrid bees maintained large population sizes during their invasion. To test for parallel selection across continents, we develop a null model that accounts for drift in ancestry frequencies during the rapid expansion. We identify several peaks within a larger genomic region where selection has pushed scutellata ancestry to high frequency hundreds of kilometers past the present cline centers in both North and South America and that may underlie high-fitness traits driving the invasion.EEA BalcarceFil: Calfee, Erin. University of California. Department of Evolution and Ecology. Center for Population Biology; Estados UnidosFil: Agra, Marcelo Nicolás. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Balcarce; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias; Argentina.Fil: Palacio, María Alejandra. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Balcarce; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias; Argentina.Fil: Ramírez, Santiago. University of California. Department of Evolution and Ecology. Center for Population Biology; Estados UnidosFil: Coop, Graham. University of California. Department of Evolution and Ecology . Center for Population Biology; Estados UnidosPublic Library of Science2020-12-14T15:44:00Z2020-12-14T15:44:00Z2020-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttps://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1009038http://hdl.handle.net/20.500.12123/84141553-73901553-7404https://doi.org/10.1371/journal.pgen.1009038PLoS Genetics 16 (10) : e1009038 (2020)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)2025-09-04T09:48:43Zoai:localhost:20.500.12123/8414instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-04 09:48:44.019INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
title Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
spellingShingle Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
Calfee, Erin
Abeja Africanizada
Apis Mellifera Scutellata
Hibridación
Invasión
Américas
Africanized Bees
Hibridization
Encroachment
Americas
title_short Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
title_full Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
title_fullStr Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
title_full_unstemmed Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
title_sort Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
dc.creator.none.fl_str_mv Calfee, Erin
Agra, Marcelo Nicolás
Palacio, María Alejandra
Ramirez, Santiago
Coop, Graham
author Calfee, Erin
author_facet Calfee, Erin
Agra, Marcelo Nicolás
Palacio, María Alejandra
Ramirez, Santiago
Coop, Graham
author_role author
author2 Agra, Marcelo Nicolás
Palacio, María Alejandra
Ramirez, Santiago
Coop, Graham
author2_role author
author
author
author
dc.subject.none.fl_str_mv Abeja Africanizada
Apis Mellifera Scutellata
Hibridación
Invasión
Américas
Africanized Bees
Hibridization
Encroachment
Americas
topic Abeja Africanizada
Apis Mellifera Scutellata
Hibridación
Invasión
Américas
Africanized Bees
Hibridization
Encroachment
Americas
dc.description.none.fl_txt_mv Recent biological invasions offer ‘natural’ laboratories to understand the genetics and ecology of adaptation, hybridization, and range limits. One of the most impressive and well-documented biological invasions of the 20th century began in 1957 when Apis mellifera scutellata honey bees swarmed out of managed experimental colonies in Brazil. This newly-imported subspecies, native to southern and eastern Africa, both hybridized with and out-competed previously-introduced European honey bee subspecies. Populations of scutellata-European hybrid honey bees rapidly expanded and spread across much of the Americas in less than 50 years. We use broad geographic sampling and whole genome sequencing of over 300 bees to map the distribution of scutellata ancestry where the northern and southern invasions have presently stalled, forming replicated hybrid zones with European bee populations in California and Argentina. California is much farther from Brazil, yet these hybrid zones occur at very similar latitudes, consistent with the invasion having reached a climate barrier. At these range limits, we observe genome-wide clines for scutellata ancestry, and parallel clines for wing length that span hundreds of kilometers, supporting a smooth transition from climates favoring scutellata-European hybrid bees to climates where they cannot survive winter. We find no large effect loci maintaining exceptionally steep ancestry transitions. Instead, we find most individual loci have concordant ancestry clines across South America, with a build-up of somewhat steeper clines in regions of the genome with low recombination rates, consistent with many loci of small effect contributing to climate-associated fitness trade-offs. Additionally, we find no substantial reductions in genetic diversity associated with rapid expansions nor complete dropout of scutellata ancestry at any individual loci on either continent, which suggests that the competitive fitness advantage of scutellata ancestry at lower latitudes has a polygenic basis and that scutellata-European hybrid bees maintained large population sizes during their invasion. To test for parallel selection across continents, we develop a null model that accounts for drift in ancestry frequencies during the rapid expansion. We identify several peaks within a larger genomic region where selection has pushed scutellata ancestry to high frequency hundreds of kilometers past the present cline centers in both North and South America and that may underlie high-fitness traits driving the invasion.
EEA Balcarce
Fil: Calfee, Erin. University of California. Department of Evolution and Ecology. Center for Population Biology; Estados Unidos
Fil: Agra, Marcelo Nicolás. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Balcarce; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias; Argentina.
Fil: Palacio, María Alejandra. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Balcarce; Argentina. Universidad Nacional de Mar del Plata. Facultad de Ciencias Agrarias; Argentina.
Fil: Ramírez, Santiago. University of California. Department of Evolution and Ecology. Center for Population Biology; Estados Unidos
Fil: Coop, Graham. University of California. Department of Evolution and Ecology . Center for Population Biology; Estados Unidos
description Recent biological invasions offer ‘natural’ laboratories to understand the genetics and ecology of adaptation, hybridization, and range limits. One of the most impressive and well-documented biological invasions of the 20th century began in 1957 when Apis mellifera scutellata honey bees swarmed out of managed experimental colonies in Brazil. This newly-imported subspecies, native to southern and eastern Africa, both hybridized with and out-competed previously-introduced European honey bee subspecies. Populations of scutellata-European hybrid honey bees rapidly expanded and spread across much of the Americas in less than 50 years. We use broad geographic sampling and whole genome sequencing of over 300 bees to map the distribution of scutellata ancestry where the northern and southern invasions have presently stalled, forming replicated hybrid zones with European bee populations in California and Argentina. California is much farther from Brazil, yet these hybrid zones occur at very similar latitudes, consistent with the invasion having reached a climate barrier. At these range limits, we observe genome-wide clines for scutellata ancestry, and parallel clines for wing length that span hundreds of kilometers, supporting a smooth transition from climates favoring scutellata-European hybrid bees to climates where they cannot survive winter. We find no large effect loci maintaining exceptionally steep ancestry transitions. Instead, we find most individual loci have concordant ancestry clines across South America, with a build-up of somewhat steeper clines in regions of the genome with low recombination rates, consistent with many loci of small effect contributing to climate-associated fitness trade-offs. Additionally, we find no substantial reductions in genetic diversity associated with rapid expansions nor complete dropout of scutellata ancestry at any individual loci on either continent, which suggests that the competitive fitness advantage of scutellata ancestry at lower latitudes has a polygenic basis and that scutellata-European hybrid bees maintained large population sizes during their invasion. To test for parallel selection across continents, we develop a null model that accounts for drift in ancestry frequencies during the rapid expansion. We identify several peaks within a larger genomic region where selection has pushed scutellata ancestry to high frequency hundreds of kilometers past the present cline centers in both North and South America and that may underlie high-fitness traits driving the invasion.
publishDate 2020
dc.date.none.fl_str_mv 2020-12-14T15:44:00Z
2020-12-14T15:44:00Z
2020-10
dc.type.none.fl_str_mv info:eu-repo/semantics/article
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dc.identifier.none.fl_str_mv https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1009038
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1553-7390
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https://doi.org/10.1371/journal.pgen.1009038
url https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1009038
http://hdl.handle.net/20.500.12123/8414
https://doi.org/10.1371/journal.pgen.1009038
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rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv PLoS Genetics 16 (10) : e1009038 (2020)
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