The genetic architecture of sucrose responsiveness in the honeybee (Apis mellifera L.)

Abstract

One of the best examples of a natural behavioral syndrome is the pollen-hoarding syndrome in honeybees that ties together multiple behavioral phenotypes, ranging from foraging behavior to behavioral ontogeny and learning performance. A central behavioral factor is the bees' responsiveness to sucrose, measured as their proboscis extension reflex. This study examines the genetics of this trait in diploid worker and haploid male honeybees (drones) to learn more about the genetic architecture of the overall behavioral syndrome, using original strains selected for pollen-hoarding behavior. We show that a significant proportion of the phenotypic variability is determined by genotype in males and workers. Second, our data present overwhelming evidence for pleiotropic effects of previously identified quantitative trait loci for foraging behavior (pln-QTL) and epistatic interactions among them. Furthermore, we report on three genomic QTL scans (two reciprocal worker backcrosses and one drone hybrid population) derived from our selection strains. We present at least one significant and two putative new QTL directly affecting the sucrose response of honeybees. Thus, this study demonstrates the modular genetic architecture of behavioral syndromes in general, and elucidates the genetic architecture of the pollen-hoarding behavioral syndrome in particular. Understanding this behavioral syndrome is important for understanding the division of labor in social insects and social evolution itself.

Figure 1.

Phenotypic distribution of the sucrose response scores of the workers (A) and males (B) used for the quantification of the degree of genetic determination. The differences between worker groups suggest some dominance effects because the high backcross (HBC) is similar to the high pollen-hoarding strain, and low backcross (LBC) is similar to the low strain. The male data fit a general additive model. (A) () Low (n = 96), () LBC (n = 258), () HBC (n = 265), (□) high (n = 93). (B) () Low (n = 81), () hybrid (n = 158), (□) high (n = 34).

Figure 1.

Phenotypic distribution of the sucrose response scores of the workers (A) and males (B) used for the quantification of the degree of genetic determination. The differences between worker groups suggest some dominance effects because the high backcross (HBC) is similar to the high pollen-hoarding strain, and low backcross (LBC) is similar to the low strain. The male data fit a general additive model. (A) () Low (n = 96), () LBC (n = 258), () HBC (n = 265), (□) high (n = 93). (B) () Low (n = 81), () hybrid (n = 158), (□) high (n = 34).

Figure 2.

One putative quantitative trait locus was detected in the high backcross with a likelihood odds ratio (LOD) score of 2.5, explaining 11.7% of the phenotypic variance. It coincided with the previously mapped pln1-QTL. A priori LOD thresholds for significant and suggestive QTL are indicated by a broken and a dotted horizontal line, respectively.

Figure 3.

Two new QTL were detected on two different linkage groups in the low backcross. The first (A) had a LOD score of 3.4 and explained 69.3% of the variance, and the second (B) has a LOD score of 3.1 and explained 14.0% of the overall phenotypic variance.

Figure 3.

Two new QTL were detected on two different linkage groups in the low backcross. The first (A) had a LOD score of 3.4 and explained 69.3% of the variance, and the second (B) has a LOD score of 3.1 and explained 14.0% of the overall phenotypic variance.

Figure 4.

One suggestive QTL was detected in the male (drone) mapping population with a LOD score of 2.3, explaining 7.9% of the total variance.