The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

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Ovarioles are the functional unit of the female insect reproductive organs and the number of ovarioles per ovary strongly influences egg-laying rate and fecundity. Social evolution in the honeybee (Apis mellifera) has resulted in queens with 200-360 total ovarioles and workers with usually 20 or less. In addition, variation in ovariole number among workers relates to worker sensory tuning, foraging behavior, and the ability to lay unfertilized male-destined eggs. To study the genetic architecture of worker ovariole number, we performed a series of crosses between Africanized and European bees that differ in worker ovariole number. Unexpectedly, these crosses produced transgressive worker phenotypes with extreme ovariole numbers that were sensitive to the social environment. We used a new selective pooled DNA interval mapping approach with two Africanized backcrosses to identify quantitative trait loci (QTL) underlying the transgressive ovary phenotype. We identified one QTL on chromosome 11 and found some evidence for another QTL on chromosome 2. Both QTL regions contain plausible functional candidate genes. The ovariole number of foragers was correlated with the sugar concentration of collected nectar, supporting previous studies showing a link between worker physiology and foraging behavior. We discuss how the phenotype of extreme worker ovariole numbers and the underlying genetic factors we identified could be linked to the development of queen traits.

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THE number of ovariole filaments per ovary is an important female reproductive character that affects fecundity across insect taxa (Richard et al. 2005; Makert et al. 2006). Social insect lineages have evolved a strong dimorphism in ovariole number between reproductive and nonreproductive castes. For example, while most families of bees consistently have 6 total ovarioles, and most species in the family Apidae have 8, the highly social species in the genus Apis (the honeybees) have queens that can have >360 total ovarioles and workers that often have <10 (Winston 1987; Michener 2003). This queen-worker dimorphism is of primary importance because it translates into differential reproductive potential that defines the social roles of these female castes (Winston 1987) and classifies social species in general (Sherman et al. 1995). Furthermore, ovary size (i.e., ovariole number) is the most sensitive indicator of caste-specific development in honeybees (Dedej et al. 1998). The extreme increase in ovariole number for queen honeybees enables high egg-laying rates (>1500 per day) and is apparently a result of selection for increased colony reproduction (growth and fission by swarming) (Seeley 1997). Honeybee queens are thus highly specialized for egg laying, similar to queens of several other social insect taxa, such as army ants or higher termites (Hölldobler and Wilson 1990). Honeybee workers in contrast, do not normally reproduce but perform all other essential activities including foraging for nectar, pollen, and water; caring for brood; and building, maintaining, and defending the colony (Winston 1987; Seeley 1997).

While worker honeybees have drastically reduced ovariolenumbers relative to queens, they have retained functional ovaries and can produce unfertilized (haploid) male-destined eggs in the absence of queen pheromonal inhibition (Velthuis 1970; Page and Robinson 1994). In the absence of a queen, variation in worker ovariole number translates into differential reproductive success (Makert et al. 2006), but in the presence of a queen this variation is correlated with several other worker attributes. Variation in worker ovariole number may underlie the pollen hoarding syndrome of honeybees, a set of correlated behavioral and physiological traits associated with biases in pollen vs. nectar foraging within honeybee colonies (Amdam et al. 2004, 2006). Ovariole number is thus an important phenotype associated with queen-worker dimorphism but also worker reproduction and division of labor. …