Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas
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...
| Main Authors: | , , , , |
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| Format: | info:ar-repo/semantics/artículo |
| Language: | Inglés |
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Public Library of Science
2020
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| Subjects: | |
| Online Access: | 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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| author | Calfee, Erin Agra, Marcelo Nicolás Palacio, María Alejandra Ramirez, Santiago Coop, Graham |
| author_browse | Agra, Marcelo Nicolás Calfee, Erin Coop, Graham Palacio, María Alejandra Ramirez, Santiago |
| author_facet | Calfee, Erin Agra, Marcelo Nicolás Palacio, María Alejandra Ramirez, Santiago Coop, Graham |
| author_sort | Calfee, Erin |
| collection | INTA Digital |
| 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. |
| format | info:ar-repo/semantics/artículo |
| id | INTA8414 |
| institution | Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina) |
| language | Inglés |
| publishDate | 2020 |
| publishDateRange | 2020 |
| publishDateSort | 2020 |
| publisher | Public Library of Science |
| publisherStr | Public Library of Science |
| record_format | dspace |
| spelling | INTA84142020-12-14T15:57:02Z Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas Calfee, Erin Agra, Marcelo Nicolás Palacio, María Alejandra Ramirez, Santiago Coop, Graham Abeja Africanizada Apis Mellifera Scutellata Hibridación Invasión Américas Africanized Bees Hibridization Encroachment Americas 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 2020-12-14T15:44:00Z 2020-12-14T15:44:00Z 2020-10 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1009038 http://hdl.handle.net/20.500.12123/8414 1553-7390 1553-7404 https://doi.org/10.1371/journal.pgen.1009038 eng info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by-nc-sa/4.0/ Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) application/pdf Public Library of Science PLoS Genetics 16 (10) : e1009038 (2020) |
| spellingShingle | Abeja Africanizada Apis Mellifera Scutellata Hibridación Invasión Américas Africanized Bees Hibridization Encroachment Americas Calfee, Erin Agra, Marcelo Nicolás Palacio, María Alejandra Ramirez, Santiago Coop, Graham 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 |
| 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_short | 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 |
| topic | Abeja Africanizada Apis Mellifera Scutellata Hibridación Invasión Américas Africanized Bees Hibridization Encroachment Americas |
| 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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