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

Abstract

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.

Genetic past, present, and future of the honey bee (Apis mellifera) in the United States of America

“…AHBs are the descendants of 36 mated A. m. scutellata queens sourced from Tanzania and Transvaal, South Africa (Winston 1992). Their offspring mated with the Brazilian honey bee population (likely M lineage: A. m. iberiensis ) (Crane 1999;Wallberg et al 2014;Whitfield et al 2006), escaped captivity, and spread north and south (Calfee et al 2020;García et al 2018;Winston 1992). Since 1990, AHBs have spread to ten states in the southern US states: Arizona, Arkansas, California, Florida, Louisiana, Oklahoma, Nevada, New Mexico, Texas, and Utah.…”

“…3; Table S3). Most of these studies have focused on mtDNA and microsatellites with only four whole genome re-sequencing studies (Bozek et al 2018;Calfee et al 2020;Cridland et al 2018;Mikheyev et al 2015). Sample sizes have varied immensely.…”

“…to several million for honey bees-provide accurate estimates of genetic diversity for colonies and populations, can increase the accuracy of ancestral sorting, and can allow one to tease apart the roles of demography and selection in contributing to genetic diversity in regions across the genome (Calfee et al 2020;Cridland et al 2018;Harpur et al 2012;Mikheyev et al 2015;Saelao et al 2020;Wallberg et al 2014). There have been five such studies focusing on honey bees in the mainland United States (Bozek et al 2018;Calfee et al 2020;Cridland et al 2018;Mikheyev et al 2015;Saelao et al 2020) (Fig. 3).…”

“…The size and smoothness of this cline suggest there will not be a hard border between EHBs and AHBs, but rather a large hybrid zone extending hundreds of kilometers. Within this area, AHBs will exhibit a variety of intermediate phenotypes selected by climate variation (Calfee et al 2020).…”

“…Understanding honey bee genetics and population structure is vital to understanding and maintaining genetic diversity (Bohling et al 2016;Brito et al 2017;Harpur et al 2012Harpur et al , 2015, discovering loci contributing variation to desirable traits (Bolormaa et al 2017;Harpur et al 2019), and ultimately developing breeding programs (Dekkers 2012;Jarquín et al 2014). Fortunately, the USA has a detailed archival record (Crane 1999;Horn 2005;Oertel 1976a, b, c, d, e;Pellett 1938;Sheppard 1989a, b) and there is a growing number of genetic analyses of honey bee populations (Bozek et al 2018;Calfee et al 2020;Cleary et al 2018;Coulson et al 2005;Cridland et al 2018;Darger 2013;Delaney et al 2009;Kono and Kohn 2015;Magnus et al 2011Magnus et al , 2014Magnus and Szalanski 2010;Mikheyev et al 2015;Pinto et al 2004Pinto et al , 2007Rangel et al 2016Rangel et al , 2020Schiff and Sheppard 1993, 1995Schiff et al 1994;Seeley et al 2015;Szalanski et al 2016a, b;Szalanski and Magnus 2010). Here, we synthesize and review historic records (Table S1, S2) and available genetic data sets (Table S3) to understand how management practices have influenced genetic diversity and differentiation of honey bee populations across the United...…”