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.

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.

The European honeybee, Apis mellifera L. (Hymenoptera: Apidae), is considered as a main contributor to pollination of important crops and to honey production. Originally, beekeeping in Argentina was performed in an extended area covering the north and central region of the country and involving A. mellifera of European origin. Later, honeybees of African origin entered South America through Brazil and hybridized with European genetic resources, giving rise to Africanized populations that are characterized by a more aggressive behavior among other unfavorable traits. In this study, a genetic characterization of 396 honeybee colonies from the most important apicultural region of Argentina is presented in order to provide an updated description of population structure and genetic diversity of commercial and feral colonies. Diversity was analyzed using mitochondrial (COI-COII region) and nuclear (eight microsatellites) markers. Three European (M4, C1, C2J) and three African (A1, A4, A30) haplotypes were detected. European haplotypes were mostly found in commercial apiaries, whereas African haplotypes were detected at high frequencies in feral colonies. Microsatellite data were analyzed to estimate population genetic variability at the province level and to evaluate genetic admixture. A high level of hybridization between Africanized and European honeybees was detected with a significant latitudinal cline from north to south. Extensive population admixture resulted in the definition of four clusters that included both feral and commercial colonies and that are explained not only by geographical distribution and degree of Africanization but also by human influence through beekeeping activities.

European lineages of Apis mellifera were first introduced into America for beekeeping purposes. A subsequent introduction and accidental release of A. m. scutellata resulted in hybridization events that gave rise to Africanized populations that rapidly spread throughout the continent. In Argentina, Africanized honey bees (AHBs) have been mostly detected in northern regions of the territory, and represent a valuable genetic resource for the selection of stocks with advantageous characteristics for beekeeping. The objective of the present study was to profile honey bee colonies of wild origin with potential beneficial traits for apiculture using morphological, molecular and behavioral traits. Honey bee colonies chosen for evaluation were located in two different agro-ecological regions in north-western Argentina (Tucumán province): The Chaco Depressed Plain (Leales apiary) and the Piedmont (Famaillá apiary). Each apiary was surveyed three times during the 2017–2018 season (mid-season, wintertime, and early spring) for: brood population, phoretic Varroa level and defensive behavior (run, fly, sting, and hang). At the midpoint of the beekeeping season colonies were also characterized by morphometry (45 variables) and mitochondrial haplotypes (COI–COII intergenic region). Apiaries studied showed similar patterns throughout the beekeeping season, for most of the characteristics monitored. However, significant variation in defensive behavior parameters was found between apiaries at the different times of evaluation. Twelve of 45 morphometric variables also showed significant differences between apiaries. The mitochondrial haplotype analysis revealed a high representation of African A4 and A1 haplotypes (91%) in both apiaries. Haplotype variation was associated with morphometric and behavioral traits. Multivariate analyses [principal component analysis (PCA) and principal coordinate analysis (PCoA)] including morphometric and behavior variables explained 65.3% (PCA) and 48.1% (PCoA) of the variability observed between colonies in the first two components. Several morphometric parameters and “fly” behavior were mainly associated with the separation of the colonies. The results from this study point to a possible association between morphometric and behavioral variation and the adaptation of honey bee colonies to differential agro-ecological conditions. We discuss how the detected variation between apiaries can be used for the selection and preservation of honey bee ecotypes in regional breeding programs.