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EVOLUTION
A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera

Amro Zayed and Charles W. Whitfield^*

Department of Entomology, University of Illinois at Urbana–Champaign, Urbana, IL 61801

Communicated by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, January 7, 2008 (received for review November 29, 2007)

Abstract

Apis mellifera originated in Africa and extended its range into Eurasia in two or more ancient expansions. In 1956, honey bees of African origin were introduced into South America, their descendents admixing with previously introduced European bees, giving rise to the highly invasive and economically devastating "Africanized" honey bee. Here we ask whether the honey bee's out-of-Africa expansions, both ancient and recent (invasive), were associated with a genome-wide signature of positive selection, detected by contrasting genetic differentiation estimates (F_ST) between coding and noncoding SNPs. In native populations, SNPs in protein-coding regions had significantly higher F_ST estimates than those in noncoding regions, indicating adaptive evolution in the genome driven by positive selection. This signal of selection was associated with the expansion of honey bees from Africa into Western and Northern Europe, perhaps reflecting adaptation to temperate environments. We estimate that positive selection acted on a minimum of 852–1,371 genes or 10% of the bee's coding genome. We also detected positive selection associated with the invasion of African-derived honey bees in the New World. We found that introgression of European-derived alleles into Africanized bees was significantly greater for coding than noncoding regions. Our findings demonstrate that Africanized bees exploited the genetic diversity present from preexisting introductions in an adaptive way. Finally, we found a significant negative correlation between F_ST estimates and the local GC content surrounding coding SNPs, suggesting that AT-rich genes play an important role in adaptive evolution in the honey bee.

adaptive evolution | F_ST | genetic differentiation

Author contributions: A.Z. and C.W.W. designed research; A.Z. performed research; A.Z. analyzed data; and A.Z. and C.W.W. wrote the paper.

The authors declare no conflict of interest.

*To whom correspondence should be addressed at: Department of Entomology, University of Illinois at Urbana–Champaign, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801. E-mail: charlie{at}life.uiuc.edu

© 2008 by The National Academy of Sciences of the USA

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