Male behavioural maturation rate responds to selection on pollen hoarding in honeybees

Abstract

Division of labour in social insect colonies relies on behavioural functional differentiation (specialization) of individuals with similar genomes. However, individual behavioural traits do not evolve independently of each other (behavioural syndromes). A prime example is the suite of behavioural differences in honeybee workers that has evolved in response to bidirectional selection on pollen hoarding of honeybee colonies (pollen-hoarding syndrome). More generally, these differences reflect functional differentiation between nectar and pollen foragers. We demonstrate here that this pollen-hoarding syndrome extends to drones. Similar to what has been shown in workers, drones from the high-pollen-hoarding strain had a higher locomotion activity after emergence, and they initiated flight earlier than did males derived from the low-pollen-hoarding strain, with hybrids intermediate. However, these two behavioural traits were unlinked at the individual level. We also found that social environment (the colony) affects the age at which drones initiate flight. The indirect selection responses of male behaviour suggest that male and worker evolution are not independent and may constrain each other's evolution. Furthermore, we identified three distinct peaks in the probability of flight initiation over the course of the experiment and a decreased phenotypic variability in the 'hybrid' males, contrary to quantitative genetic expectations.Social insects owe much of their evolutionary success to the coordinated action of behaviourally specialized members of their colonies (Oster & Wilson 1978; Winston 1987;Hölldobler & Wilson 1990). Division of labour is a hallmark of social evolution (Beshers & Fewell 2001), and among honeybee workers, it is mainly determined by age and genetic effects (Winston 1987). To promote individual specialization, the response thresholds to different task stimuli should vary independently among individuals (Beshers & Fewell 2001). This seems not to be the case: honeybees show well-established behavioural differences among races that extend to multiple behavioural phenotypes, as well as to morphology and life history (Winston 1987). Similar multiple behavioural phenotypes in honeybees are also correlated at the individual level (Page & Erber 2002;Pankiw 2003;Scheiner et al. 2004), indicating their evolution as behavioural syndromes (array of correlated behavioural characteristics: Sih et al. 2004). Linked sets of behavioural traits may have arisen through adaptation in certain contexts (Amdam et al. 2004), but the correlation among behavioural traits may constrain the division of labour in social insects, and behavioural optimization in general (Price & Langen 1992;Sih et al. 2004 One of the best-studied examples of behavioural syndromes in insects is the behavioural differentiation among workers of two strains of honeybees that have been bidirectionally selected over multiple generations for different amounts of pollen stored in their nests . Many different aspects of foraging behaviour Wadd...

The Development and Evolution of Division of Labor and Foraging Specialization in a Social Insect (Apis mellifera L.)

“…High-strain workers were more active than low-strain workers, consistent with the results from wild-type bees (Humphries et al, 2005). Rueppell et al, 2005 tested high-and low-strain males (drones) for locomotor activity under light and dark conditions. High-strain drones were more active under both conditions, which is consistent with the results from workers.…”

A Game Theoretical Analysis of the Mating Sign Behavior in the Honey Bee

“…In this biologically plausible scenario, drones do not gain any fitness from leaving the mating sign to increase subsequent mating chances. Note that we have enough room for making N sS smaller and σ/υ bigger and still not violating (22) which means that signer is not ESS even if the experimental data used here were not nearly exact.…”

“…which, by (22), means that signer is not ESS. In this biologically plausible scenario, drones do not gain any fitness from leaving the mating sign to increase subsequent mating chances.…”

“…Honey bees provide probably the most striking case because queens of several species in their genus Apis can mate with over forty different males (drones) during a very short time at the beginning of their lives [5,26]. Honey bee queens and drones mature for about one week in their parental colony before they leave for mating flights [30,22]. On these mating flights both sexes fly to mating arenas, called drone congregation areas (DCAs), where mate location and mating takes place [16].…”

The Ability of Honey Bee Drones to Ejaculate

“…The drones reared in larger colonies achieve greater reproductive success; more often copulate with the queen, and also have a larger share in the number of offspring (Kraus et al, 2003). The drones reared under optimum thermal and feeding conditions have greater chance of mating (Jaycox, 1961;Rueppell et al, 2006;Czekońska et al, 2013). Drones reared in colonies of different quality, differ in the age when they reach the ability to copulate with the queen (Rhodes et al, 2011;Czekońska et al, 2015).…”