Fact SheetMating for queen quality

Honey bee queens mate with 12 males on average (Tarpy et al. 2004). By mating with a large number of males, queens avoid low brood viability. Additional benefits include increased disease resistance, health, colony homeostasis, survival and productivity (Palmer & Oldroyd 2000, Oldroyd & Fewell 2007).

Colonies with queens inseminated with semen from 15 drones outperform colonies with queens inseminated with semen from a single drone – producing more comb, having higher foraging rates and producing more honey and a larger workforce (Mattila & Seeley 2007).

In another study, colonies with queens with an effective mate number (mₑ; Box 1) over 7 were 2.86 times more likely to survive than those with a queen with mₑ < 7 (Tarpy et al. 2013). There was no effect of mₑ on whether queens were superseded. However, of those queens that were superseded, queens with a lower mₑ were superseded faster than those with a higher mₑ. Whether the same effect on survival would be seen in Australia is unclear, as our winters are less harsh and we have not experienced colony collapse disorder. Nevertheless, it is accepted that genetically diverse colonies outperform less genetically diverse colonies (Palmer & Oldroyd 2000, Oldroyd & Fewell 2007).

Some concern has been expressed that queens produced either early or late in the season may not have enough males to mate with, and therefore may be of lower quality than those produced mid-season. In this study we sampled offspring from queens mated in early-spring (October) and autumn (March). We worked with 4 queen producers each season, aiming to sample the earliest and latest queens that they produced.

Study outcomes

• The queens produced by different queen producers did not vary in their mating quality. Early-spring queens mated with an average of 15.5 males, while autumn queens mated with an average of 13.6 males. Average mₑ in early-spring was 10.6, while it was 9.0 in

autumn. 92.8% of early-spring queens had mₑ >7 and were considered sufficiently mated. However, 33.8% of autumn queens had mₑ <7, and therefore could be considered inadequately mated (Figure 1).

• The number of colonies contributing drones to the mating pool of each queen producer were similarly high in early-spring (120.5, on average) and autumn (112.0, on average; Table 1).

• These results show that while there are a similar number of colonies contributing drones to the mating pool in early-spring and autumn, a proportion of queens are insufficiently mated in autumn. This suggests that while a similarly high number of colonies are producing drone in both seasons, the number of drones produced per colony is lower in autumn.

• Queens were not inbred. The heterozygosity and fixation index (FIS), both measures of inbreeding, were normal (Table 2).

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Table 1 Number of colonies contributing to the mating pool of 5 queen producers. NA: no samples collected from this queen producer at this time point.

Queen Producer Number of colonies contributing to the mating pool

Early-spring Autumn

1 161 110

2 118 116

3 111 103

4 92 NA

5 NA 119

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Figure 1 Mean and standard error of the number of mates (m) and effective mate number (mₑ) of queens produced by four queen producers in spring and autumn. The red circles are queens with mₑ < 7.

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Box 1: Effective mate number

The number of males (m) a queen mates with can be a poor indication of her mating quality. Paternity skew occurs when there are differences in the proportion of offspring produced from each male the queen mated with. For example, if a queen mated with 5 males and they all had even paternity then each male would have a 20% share of the offspring. If a queen mated with 5 males, but one of them had an 80% share of the offspring then the genetic diversity in that colony is less than the first colony, even though the queen mated with the same number of males.

The effective mate number (mₑ) formula (Tarpy et al. 2004) takes reproductive skew into account, and provides a better indication of a queen’s mating quality. There is never a completely even share of offspring and this cannot be affected by management practices. However, if worker-produced drones are smaller because they have not been reared in drone-comb then they may produce less semen and this could contribute to paternity skew.

Recommendations

The number of drones a queen mates with can be influenced by the weather, availability of forage, availability of drones and genetic background. Therefore, mating number is likely to vary between seasons and from year to year, depending on the conditions. The length of the queen production season depends on these variables.

There has been much focus on the production of drones for early season queens, and the assumption is that preparations in early-spring will be sufficient for the entire queen production season. This study has shown that our focus on early-spring production has achieved good results, and similar investment in assuring drone numbers and quality later in the season should now be made (Chapman et al. 2018).

Drone production can be increased through supplementary feeding and the provision of drone comb. Large colonies with good food stores produce more drones than weaker colonies. Supplementary feeding can also improve drone fertility (Boes 2010, Rousseau & Giovenazzo 2016).

Colonies begin to evict drones as forage depletes. Eviction of drones may be delayed by supplementary feeding or the removal of the queen. The size of the colony does not influence eviction (Free & Williams 1975).

Acknowledgements

This project (PRJ-009757) was funded by the AgriFutures™ Honey Bee and Pollination Program, and conducted by Prof. Benjamin Oldroyd and Dr. Nadine Chapman from the Behaviour and Genetics of Social Insects Laboratory, School of Life and Environmental Sciences, at the University of Sydney. We thank Rani Dos Santos Cocenza, Benjamin Blanchard, Lucy Nguyen and Gabriele Buchmann for their contributions to the project.

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Table 2 Observed and expected heterozygosity, probability of a deficit of heterozygotes and the fixation index (FIS) of queens produced by 5 queen producers in early-spring and autumn. NA: No samples were collected from this queen producer at this time point.

Queen Producer

Observed Heterozygosity

Expected Heterozygosity Probability Fixation Index

Early-spring Autumn Early-spring Autumn Early-spring Autumn Early-spring Autumn

1 0.816 0.815 0.739 0.764 0.875 0.072 -0.107 -0.067

2 0.716 0.735 0.694 0.672 0.221 0.697 -0.037 -0.090

3 0.825 0.684 0.660 0.639 1.000 0.830 -0.268 -0.042

4 0.554 NA 0.549 NA 0.684 NA 0.041 NA

5 NA 0.750 NA 0.706 NA 0.715 NA -0.073

Average 0.728 0.746 0.661 0.695 0.695 0.579 -0.093 -0.068

The number of drones a queen mates with can be influenced by the weather, availability of forage, availability of drones and genetic background.

References Boes KE (2010) Honeybee colony drone production and maintenance in accordance with environmental factors: an interplay of queen and worker decisions. Insectes Sociaux 57: 1-9Chapman NC, Cocenza RDS, Blanchard B, Nguyen LM, Lim J, Buchmann G, Oldroyd BP (2018) Genetic diversity in the progeny of commercial Australian queen honey bees (Hymenoptera: Apidae) produced in autumn and early spring. Journal of Economic Entomology doi: 10.1093/jee/toy308Couvillon MJ, Hughes WHO, Perez-Sato JA, Martin SJ, Roy GGF, Ratnieks FLW (2010) Sexual selection in honey bees: colony variation and the importance of size in male mating success. Behavioral Ecology 21: 520-525Free JB, Williams IH (1975) Factors determining the rearing and rejection of drones by the honeybee colony. Animal Behaviour 23: 650-675Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends in Ecology and Evolution 22: 408-413Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the genus Apis. Apidologie 31: 235-248Rousseau A, Fournier V, Giovenazzo P (2015) Apis mellifera (Hymenoptera: Apidae) drone sperm quality in relation to age, genetic line, and time of breeding. Canadian Entomology 147: 702-711Tarpy DR, Nielsen R, Nielsen DI (2004) A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Sociaux 51: 203-204Tarpy DR, vanEngelsdorp D, Pettis JS (2013) Genetic diversity affects colony survivorship in honey bee colonies. Naturwissenschaften 100: 723-728

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Quick Facts

• Genetically diverse colonies have increased health, survival and productivity

• An effective mate number (mₑ; Box 1) above 7 has been suggested to determine if queens are adequately mated

• Early-spring queens mated with 15.5 males on average

• Mid-autumn queens mated with 13.6 males on average

• mₑ in spring was 10.6

• mₑ in autumn was 9.0

• 92.8% of spring queens had mₑ >7

• 33.8% of autumn queens had mₑ <7

• The average number of colonies contributing drones in spring was 120.5, while in autumn it was 112.0

• Management practices should be used to increase drone availability in autumn

• Queens were not inbred

Contact

Ben Oldroyd Behaviour and Genetics of Social Insects Laboratory University of Sydney 02 9351 7501 benjamin.oldroyd@sydney.edu.au

Nadine Chapman Behaviour and Genetics of Social Insects Laboratory University of Sydney 02 9351 2267 Nadine.Chapman@sydney.edu.au

AgriFutures Australia Project No.: PRJ-009757 AgriFutures Australia Publication No.: 18/077