Cross‐decades stability of an avian hybrid zone

Wang, Silu; Rohwer, Sievert; Delmore, Kira E.; Irwin, Darren E.

doi:10.1111/jeb.13524

Cited by 45 publications

(78 citation statements)

References 48 publications

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“…To more precisely infer the current shape and position of the two hybrid zones, we fit a classic logistic cline model to inferred genome-wide individual scutellata ancestry proportions [ 65 – 67 ]: where A i is the genome-wide scutellata ancestry proportion inferred for the i th individual bee, x i is their latitude, M is the asymptotic maximum scutellata ancestry approaching the equator, which is set at 0.84 (i.e. frequency in Brazil [ 37 ]), c is the cline center, and is the cline width (i.e.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2020

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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.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2020

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Section: Resultsmentioning

confidence: 99%

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

Calfee

Agra

Palacio

et al. 2020

Preprint

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AbstractRecent 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 Brazil with the escape of introduced African honey bees (Apis mellifera scutellata) in 1957. In less than 50 years, populations of ‘Africanized’ honey bees spread across much of the Americas, hybridizing with and outcompeting resident European honey bees. We use broad geographic sampling and whole genome sequencing of over 300 bees to map the distribution of African ancestry where the northern and southern invasions have presently stalled, forming replicated hybrid zones between Africanized and European bees 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 African ancestry, and parallel clines for wing length that span hundreds of kilometers, supporting a smooth transition from climates favoring Africanized 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 African ancestry at any individual loci on either continent, which suggests that the competitive fitness advantage of African ancestry at lower latitudes has a polygenic basis and that Africanized 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 African ancestry to high frequency hundreds of kilometers past the present cline centers in both North and South America and that may underlie high-fitness African traits driving the invasion.Author SummaryCrop pollination around the world relies on local honey bee populations, which vary in their behaviors and climatic ranges. Africanized honey bees (‘killer bees’) have been some of the most widely successful; originating in a 1950s experimental breeding program in Brazil, they rapidly came to dominate across most of the Americas. As a recent genetic mixture of imported African bees and European subspecies, Africanized honey bees have a patchwork of ancestry across their genomes, which we leverage to identify loci with an excess of African or European ancestry due to selection. We additionally use the natural replication in this invasion to compare outcomes between North and South America (California and Argentina). We identify several genomic regions with exceptionally high African ancestry across continents and that may underlie favored Africanized bee traits (e.g. Varroa mite resistance). We find evidence that a climatic barrier has dramatically slowed the invasion at similar latitudes on both continents. African-to-European ancestry transition zones span hundreds of kilometers where bees have intermediate African ancestry proportions, which can be used to map the genetic basis of segregating traits (here, wing length), and calls into question the biological basis for binary Africanized vs. European bee classifications.

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“…1C) across the hybrid zone and extending into the ranges of townsendi and occidentalis. Among the 265 individuals (Table S1), 250 of them were involved in our previous work in this system (Wang et al 2019) with 15 additional samples from 2005-2008 sampling included in this study to increase the sample size.…”

Section: Samplingmentioning

confidence: 99%

“…S1). Instead of scoring species-specific plumage variation as discrete variables (Wang et al 2019), for the present study we further quantified pigmentation of the patches using continuous variables. A single observer (JM) processed all field and museum photos (Table S1).…”

Section: Plumage Measurementsmentioning

confidence: 99%

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Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species

et al. 2020

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Speciation is one of the most important processes in biology, yet the study of the genomic changes underlying this process is in its infancy. North American warbler species Setophaga townsendi and Setophaga occidentalis hybridize in a stable hybrid zone, following a period of geographic separation. Genomic differentiation accumulated during geographic isolation can be homogenized by introgression at secondary contact, whereas genetic regions that cause low hybrid fitness can be shielded from such introgression. Here, we examined the genomic underpinning of speciation by investigating (1) the genetic basis of divergent pigmentation traits between species, (2) variation in differentiation across the genome, and (3) the evidence for selection maintaining differentiation in the pigmentation genes. Using tens of thousands of single nucleotide polymorphisms (SNPs) genotyped in hundreds of individuals within and near the hybrid zone, genome-wide association mapping revealed a single SNP associated with cheek, crown, breast coloration, and flank streaking, reflecting pleiotropy (one gene affecting multiple traits) or close physical linkage of different genes affecting different traits. This SNP is within an intron of the RALY gene, hence we refer to it as the RALY SNP. We then examined between-species genomic differentiation, using both genotyping-by-sequencing and whole genome sequencing. We found that the RALY SNP is within one of the highest peaks of differentiation, which contains three genes known to influence pigmentation: ASIP, EIF2S2, and RALY (the ASIP-RALY gene block). Heterozygotes at this gene block are likely of reduced fitness, as the geographic cline of the RALY SNP has been narrow over two decades. Together, these results reflect at least one barrier to gene flow within this narrow (∼200 kb) genomic region that modulates plumage difference between species. Despite extensive gene flow between species across the genome, this study provides evidence that selection on a phenotype-associated genomic region maintains a stable species boundary.

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Cross‐decades stability of an avian hybrid zone

Cited by 45 publications

References 48 publications

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

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

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

Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species

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