Africanization in the United States: Replacement of Feral European Honeybees (Apis Mellifera L.) by an African Hybrid Swarm

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The expansion of Africanized honeybees from South America to the southwestern United States in <50 years is considered one of the most spectacular biological invasions yet documented. In the American tropics, it has been shown that during their expansion Africanized honeybees have low levels of introgressed alleles from resident European populations. In the United States, it has been speculated, but not shown, that Africanized honeybees would hybridize extensively with European honeybees. Here we report a continuous 11-year study investigating temporal changes in the genetic structure of a feral population from the southern United States undergoing Africanization. Our microsatellite data showed that (1) the process of Africanization involved both maternal and paternal bidirectional gene flow between European and Africanized honeybees and (2) the panmitic European population was replaced by panmitic mixtures of A. m. scutellata and European genes within 5 years after Africanization. The post-Africanization gene pool (1998-2001) was composed of a diverse array of recombinant classes with a substantial European genetic contribution (mean 25-37%). Therefore, the resulting feral honeybee population of south Texas was best viewed as a hybrid swarm.

THE evolutionary significance of natural hybridization has been debated for decades (MAYR 1942; ANDERSON 1949; HARRISON 1993; ARNOLD 1997). At one extreme, it has been argued that natural hybridization is an evolutionary dead end due to formation of inviable and/or infertile hybrids (MAYR 1942; BARTON and HEWITT 1985, 1989). At the other extreme, it has been suggested that natural hybridization may lead to new evolutionary lineages due to formation of relatively fit hybrids that expand into novel habitats (ANDERSON 1948; ARNOLD 1997; ELLSTRAND and SCHIERENBECK 2000; BLEEKER 2003). A third potential evolutionary outcome is expansion of an intermixed form within the resident progenitor's habitat, in which case the degree of mixing between hybridizing forms may range from formation of a hybrid swarm to genetic assimilation of one form by the other (GUILDS et al. 1996; RHYMER and SIMBERLOFF 1996; PERRY et al. 2001). Natural hybridization and introgression have been reported in a growing number of biological invasions (RHYMER and SIMBERLOFF 1996). Such invasive events are of great interest to the discipline of evolutionary biology because they provide unique opportunities to study evolutionary processes at initial stages of secondary contact of divergent genomes.

Our study of hybridization, which deals with one of the most spectacular biological invasions yet documented, that of the Africanized honeybees (Apis mellifera L.), builds on the previous studies of Africanization. Africanized honeybees derive from a founder population of the tropical-evolved African subspecies Apis mellifera scutellata brought from South Africa into Brazil in 1956 to interbreed with previously imported temperateevolved European honeybees. The purpose of the introduction was to create a honeybee better adapted to tropical conditions, because the European honeybee colonies were poor honey producers and would survive only when intensively managed (NoGUEiRA-NETO 1964; KERR 1967). Soon after the introduction, queens of A. m. scutellata-were accidentally released into the natural environment (SPIVAK et al. 1991) and their descendants have since expanded throughout South and Central America and have established large feral populations where European colonies could not thrive (TAYLOR 1988; ROUBIK and BOREHAM 1990; WINSTON 1992). The leading edge of the expanding front reached the southern United States in 1990, only 33 years after initial release (SuGDEN and WILLIAMS 1990). Prior to arrival of Africanized honeybees, the United States sustained large feral and managed populations of honeybees predominantly derived from eastern (A. in. ligustica, A. in. carnica, and A. m. caucasia) and western (A. …