The PNAS Early Edition this week includes a paper by bee genome researchers Amro Zayed and Charles Whitfield. After a short review of honeybee phylogeny, they demonstrate two things:
1. An ancient dispersal of honeybees from Africa into Europe was accompanied by a pulse of positive selection on coding genes, amounting to selection on approximately 10 percent of bee genes.
2. As Africanized bees have spread across South and into North America, adaptive genes from the existing populations of European bees have introgressed into the Africanized population, increasing under positive selection.
These are remarkable parallels to the worldwide evolution of humans. In bees, the geographic pattern is not the same, and the timescale is different, but the overall genetic impact is quite similar.
Here's the bee history:
In its native range, A. mellifera is classified into approximately two dozen subspecies, which are further organized into four major geographically and genetically distinct groups: African, Western and Central Asian (hereafter referred to as Asian), Eastern European, and Western and Northern European (hereafter referred to as West European) (9-11). European honey bees were introduced by humans to the New World by European settlers as early as the 1600s. In Brazil in 1956, an intentional introduction of African honey bees (A. mellifera scutellata), which hybridized with previously introduced European bees, led to the establishment and spread of the highly invasive and economically devastating Africanized honey bees in North America and South America (12). Subsequent studies have shown that Africanized bees are predominantly African in ancestry with minor but consistent contribution from European genotypes (11, 12). Using recently developed SNP panels, Whitfield et al . (11) demonstrated that the honey bee originated in Africa and subsequently expanded into Eurasia in two or more independent ancient expansions. One expansion gave rise to Western European honey bees, and at least one other independent expansion gave rise to Asian and Eastern European honey bees. Honey bee subspecies vary in a host of phenotypic traits, such as morphology, behavior, physiology, and gene expression (9-11, 13, 14) (Zayed and Whitfield 2008:3421).
I was not aware of the initial dispersals of bees into Europe and Asia. The genetic data show that the Western European strains are the ones with the most adaptive evolution since their dispersal from Africa. The separate ancient bee dispersals were documented by Whitfield et al. (2006), but they were not able to provide date estimates for the ancient dispersals, and none are attempted in this study.
This is the kind of test that ought to fail in most wild populations. Without a shift in the adaptive landscape, the fraction of new mutations with potential adaptive value is bound to be small -- because species are optimized to the environments that they have occupied for a long time. But European bees have a number of recent environmental changes, ranging from the simple effect of moving from a tropical to a temperate environment, the need to use new and different flora, and the effects of domestication. In a very numerous, rapidly dispersing species, these effects led to a rapid adaptive response in a large proportion of genes. These are the basic principles underlying the recent acceleration of positive selection in our lineage also.
The introgression of European genes into the dispersing Africanized bees in the Americas is interesting, because it seems counter-intuitive. The main differences between Africanized bees and European bees involve adaptations to climate. European bees put up lots of honey for the winter, and swarm less frequently, in addition to being more sedate. African bees don't bother with as much honey, which together with their more frequent swarming would seem to be a good fit for the tropical pattern of seasonality. These African traits explain why the African bees have spread at the expense of the European bees across the tropical New World. But Africanized bees have picked up a lot of genes from the European bees in the New World.
The authors propose some possible explanations:
The adaptive value of functional (coding) portions of Western European genomes could be related to positive selection on novel variation in West European bees, to positive selection on novel hybrid gene combinations, and/or to selection for heterozygous genotypes. Our study thus provides direct evidence that invasive populations can exploit hybridization in an adaptive fashion -- a finding of immense relevance to understanding the dynamics of biological invasions (Zayed and Whitfield 2008:3424).
In other words, behavioral correlates of climate may be a target of selection and introgression -- I would speculate because of the intrinsic rarity of adaptive mutations in these functions.
This is a relatively course-grained analysis of positive selection, since the study basically averages within SNP categories, determining FST between pairs of populations. For non-coding SNPs, the Africanized bees are very similar to African bees (FST = 0.05), while for coding SNPs they are twice as divergent (FST = 0.10). That's a lot of difference in allele frequencies over a short time; it must have been caused by strong positive selection across a broad sample of loci. They do not attempt the same kind of "10% of genes" estimate for the introgression, but their figures show that it is quite significant across their data.
I don't know but it may be a while before this initial study can be followed up with recombination based selection tests, because of this little known fact: bees have a recombination rate of 19 cM/Mb -- roughly 15 times higher than humans. Still, Whitfield et al. (2006) found an excess of linkage disequilibrium in the West European subspecies of bees. It now seems likely that some of this LD is explained by the widespread selection documented in the current study.
In other words, the genetic structure of global bee populations provides another strong example of the importance of rapid evolution in abundant species, coupled with ecological changes. Bees also now provide a strong example of adaptive introgression -- in this case, within a very tightly timed dispersal with known climatic conditions.
Zayed A, Whitfield CW. 2008. A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proc Nat Acad Sci USA 105:3421-3426. doi:10.1073/pnas.0800107105
Whitfield CW and 9 others. 2006. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314:642-645. doi:10.1126/science.1132772