Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera)

Abstract

The all-female worker caste of the honeybee (Apis mellifera) is effectively barren in that workers refrain from laying eggs in the presence of a fecund queen. The mechanism by which workers switch off their ovaries in queenright colonies is pheromonally cued, but there is genetically based variation among individuals: some workers have high thresholds for ovary activation, while for others the response threshold is lower. Genetic variation for threshold response by workers to ovary-suppressing cues is most evident in "anarchist" colonies in which mutant patrilines have a proportion of workers that activate their ovaries and lay eggs, despite the presence of a queen. In this study we use a selected anarchist line to create a backcross queenright colony that segregated for high and low levels of ovary activation. We used 191 informative microsatellite loci, covering all 16 linkage groups to identify QTL for ovary activation and test the hypothesis that anarchy is recessively inherited. We reject this hypothesis, but identify four QTL that together explain approximately 25% of the phenotypic variance for ovary activation in our mapping population. They provide the first molecular evidence for the existence of quantitative loci that influence selfish cheating behavior in a social animal.

Figure 1.—

Backcross design for QTL mapping population. Queen P2 and worker P1 were reared from the anarchy line. Drone P3 was collected from a wild-type colony that (typically) did not show any signs of worker-laid brood. A presumably heterozygous F₁ queen F₁2 was mated to an F₁ anarchist drone F₁1 to give the F₂ generation of workers. The F₂ generation was used as the mapping population.

Figure 2.—

Interval maps of the four linkage groups containing significant QTL at 5% false discovery rate. LOD score (y-axis) was calculated at 1-cM intervals across each linkage group (x-axis). The 5% empirical threshold is indicated by the dashed line. Ninety-five percent confidence intervals are shown by solid bars. Microsatellite marker positions are indicated by peaks just below each x-axis. Maps A, B, C, and D show linkage groups 15, 1, 7, and 13 and QTL OvA1, OvA2, OvA3, and OvA4, respectively.