Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees

Abstract

The colony-level phenotype of an insect society emerges from interactions between large numbers of individuals that may differ considerably in their morphology, physiology, and behavior. The proximate and ultimate mechanisms that allow this complex integrated system to form are not fully known, and understanding the evolution of social life strategies is a major topic in systems biology. In solitary insects, behavior, sensory tuning, and reproductive physiology are linked. These associations are controlled in part by pleiotropic networks that organize the sequential expression of phases in the reproductive cycle. Here we explore whether similar associations give rise to different behavioral phenotypes in a eusocial worker caste. We document that the pleiotropic genetic network that controls foraging behavior in functionally sterile honey bee workers (Apis mellifera) has a reproductive component. Associations between behavior, physiology, and sensory tuning in workers with different foraging strategies indicate that the underlying genetic architectures were designed to control a reproductive cycle. Genetic circuits that make up the regulatory "ground plan" of a reproductive strategy may provide powerful building blocks for social life. We suggest that exploitation of this ground plan plays a fundamental role in the evolution of social insect societies.

Fig. 1.

Mean vitellogenin protein levels in the hemolymph of 0-, 5-, and 10-day-old workers from colonies selected for high and low pollen hoarding. The high- and low-strain bees are represented by gray and white bars, respectively. The titers are calculated relative to a β-galactosidase standard. Shown are the results of separate experimental setups in which worker bees from the two strains were introduced into three wild-type “host” colonies. Lines indicating standard errors are represented on top of each bar. Significant differences within age cohorts are indicated with asterisks. The cut-off P value is 0.05 by a Fisher's post hoc test.

Fig. 2.

Mean vitellogenin mRNA levels in the abdomen of 0-, 5-, and 10-day-old high- and low-strain bees. The data from the two strains are represented by gray and white bars, respectively. The mRNA levels are measured as relative quantities (RQ) (see Materials and Methods for information). Lines indicating standard errors are represented on top of each bar. Significant differences within age cohorts are indicated with asterisks. The cut-off P value is 0.05 by a Fisher's post hoc test.

Fig. 3.

Vitellogenin titer plotted against vitellogenin mRNA level. High-strain workers are represented by gray circles, and low-strain workers are represented by white circles. The titers are calculated relative to a β-galactosidase standard, and the mRNA levels are measured as relative quantities (RQ). Each data point is a sample obtained from an individual bee. Shown are data distributions from 0-, 5-, and 10-day-old bees, respectively. The first-order regressions of the mRNA levels on the titers are depicted by dashed and full lines for the high and low pollen-hoarding strains, respectively. In C, the two high-strain samples with titers of >17 μg/μl are not included in the estimation of the regression line.