Reticulate evolution and honey

The American Honey Producers Association—in testimony given before the United States Senate Committee on Agriculture, Nutrition and Forestry (AHPA 2007)—provided the following details concerning the crucial effect of Apis mellifera (i.e., the honeybee) on the production of human plant-based foods: (1) income from sales of honey during 2006, in the top six producing states alone, exceeded US$80 million; (2) pollination services provided by captive hives are essential for the multibillion dollar agricultural industry; (3) honeybees pollinate >90 crop species as diverse as melons and broccoli (and including nonfood crops such as cotton); (4) crops such as almonds, which are the major agricultural export of California (this state provides 100% of almonds used in the United States and 80% of those used worldwide), depend entirely on A. mellifera for pollination; and (5) as of 2006, >140 billion honeybees (i.e., 2 million colonies) were needed to service US crop plants. Applying this formula to global crop production illustrates the vast dependency—for both food and income—of human populations on A. mellifera.

The evolutionary origin of honeybees has been pinpointed to the continent of Africa, with subsequent spreading of populations (both with and without human-mediated transport) to Eurasia and the New World (Whitfield et al. 2006). Evidence from numerous analyses suggests that the evolutionary history of A. mellifera has involved extensive reticulation. With regard to European populations, a phylogenetic analysis by Arias and Sheppard (1996) detected numerous instances of discordance that they attributed to intersubspecific introgression. For example, Italy was a geographic region identified by Arias and Sheppard (1996) as providing "substantial evidence of subspecific introgression." Consistent with this hypothesis, a subsequent population genetic analysis of Apis mellifera ligustica (continental Italian samples) and Apis mellifera sicula (Sicilian samples) confirmed the hybrid origin of both subspecies (Franck et al. 2000).

The best-documented instance of reticulate evolution of A. mellifera involves introgressive hybridization in the New World between the earlier introduced European honeybees with populations of the African lineage, Apis mellifera scutellata. At least seven European subspecies were introduced into North America alone (beginning in 1622 and continuing for several hundred years; Whitfield et al. 2006). Similarly, introductions of

subspecies from both western and eastern Europe were made into South America. The introductions of multiple lineages of European origin resulted in admixed populations. However, the greatest genetic exchange was catalyzed by the introduction of African A. m. scutellata into Brazil in 1956 (Whitfield et al. 2006).

The spread of the African A. mellifera lineage into the New World has involved extensive introgres-sion with European taxa (Figure 7.1). So extensive has been the genetic assimilation of the European subspecies by A. m. scutellata that the process has been termed "Africanization" and the resulting populations "Africanized" (e.g., Clarke et al. 2002; Pinto et al. 2004, 2005). For example, of 775 samples from Brazil and Uruguay, >90% possessed mtDNA variants from A. m. scutellata (Figure 7.1; Collet et al. 2006). Similarly, Mexican honeybee populations sampled by Kraus et al. (2007) possessed African mtDNA at frequencies ranging from 67% to 95% and African nuclear alleles at a frequency of ~58%. Finally, a feral honeybee population in southern Texas demonstrated a changeover in genetic composition indicating that a "panmictic European population was replaced by panmictic mixtures of A. m. scutellata and European genes within 5 years." (Pinto et al. 2005).

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