Neonicotinoid pesticides can reduce honeybee colony genetic diversity

Abstract

Neonicotinoid insecticides can cause a variety of adverse sub-lethal effects in bees. In social species such as the honeybee, Apis mellifera, queens are essential for reproduction and colony functioning. Therefore, any negative effect of these agricultural chemicals on the mating success of queens may have serious consequences for the fitness of the entire colony. Queens were exposed to the common neonicotinoid pesticides thiamethoxam and clothianidin during their developmental stage. After mating, their spermathecae were dissected to count the number of stored spermatozoa. Furthermore, their worker offspring were genotyped with DNA microsatellites to determine the number of matings and the genotypic composition of the colony. Colonies providing the male mating partners were also inferred. Both neonicotinoid and control queens mated with drones originating from the same drone source colonies, and stored similar number of spermatozoa. However, queens reared in colonies exposed to both neonicotinoids experienced fewer matings. This resulted in a reduction of the genetic diversity in their colonies (i.e. higher intracolonial relatedness). As decreased genetic diversity among worker bees is known to negatively affect colony vitality, neonicotinoids may have a cryptic effect on colony health by reducing the mating frequency of queens.

Fig 1. Corrected Effective Mating inferred from offspring DNA genotyping of control and neonicotinoid honeybee queens (Apis mellifera).

Boxplot shows inter-quartile range (box), median (black line within interquartile range), means (black asterisk); data range (dashed vertical lines). Queens exposed to neonicotinoid pesticides during their developmental stage mated with fewer males, resulting in lower Effective Matings than control queens. *P≤0.1, **P≤0.05, ***P≤0.01 (comparison with Controls).

Fig 2. Corrected Relatedness inferred from offspring DNA genotyping of control and neonicotinoid honeybee queens (Apis mellifera).

Boxplot shows inter-quartile range (box), median (black line within interquartile range), means (black asterisk); data range (dashed vertical lines). Queens exposed to neonicotinoid pesticides during their developmental stage mates with fewer males, resulting in higher Corrected Relatedness among worker offspring than control queens. *P≤0.1, **P≤0.05, ***P≤0.01 (comparison with Controls).

Fig 3. Estimation of the non-sampling error of the number of Drone Source Colonies (i.e. the number of non-sampled colonies) through a fitted Poisson distribution for honeybee (Apis mellifera) mating.

Observed frequencies are plotted in bars, expected frequencies (fitted Poisson distribution) are plotted in grey solid line. Here, singletons were paired to estimate the minimum number of Drone Source Colony. The number of non-detected Drone Source Colonies is 0.40.

Fig 4. Frequency of control and neonicotinoid honeybee (Apis mellifera) queens mated by Drones Source Colony.

Singletons that mated with different types of queen (i.e. control or neonicotinoid) were paired. Frequency of queens that mated with drones from each Drone Source Colony is represented in light grey and dark grey for the control and neonicotinoid queens, respectively.