Sexual selection in honey bees: colony variation and the importance of size in male mating success

Behavioral Ecology, May 2010

Sexual selection is a dominant force in the evolution of many animals and can be particularly significant in species that mate in aerial swarms characterized by strong male–male competition. However, such mating biology, typical of many social insects, is also quite challenging to study. Here, we investigate sexual selection in the honey bee that has 2 distinct male morphs (normal sized and small). Males mate only once and females return to their nest after mating, making it possible to measure the lifetime fitness of both sexes. We allowed known numbers of normal-sized males from 6 colonies and small males from another 6 colonies to compete for natural matings with experimental virgin queens. We then determined the mating success of males by genotyping the offspring of these queens. Colonies differed by an order of magnitude in the intrinsic mating success of their males, confirming that the reproductive fitness of honey bee colonies is highly variable. Small males achieved approximately half as many matings as expected given their number of flights and, in addition, had a significantly smaller share of paternity per mating than normal-sized males. Interestingly, the flight activity of small males suggested that they may compensate for their lower competitiveness by flying outside the most competitive mating period in the afternoon. The lower fitness of small males shows that sexual selection is strong in honey bees and contributes to inclusive fitness dynamics that favor worker cooperation within their societies.

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Sexual selection in honey bees: colony variation and the importance of size in male mating success

Margaret J. Couvillon 0 1 4 6 William O.H. Hughes 0 1 5 6 Juan A. Perez-Sato 0 1 2 6 Stephen J. Martin 0 1 6 Gabrielle G.F. Roy 0 1 6 Francis L.W. Ratnieks 0 1 3 6 0 The Author 2010. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions , please 1 @leeds.ac. uk . Margaret J. Couvillon and William O.H. Hughes contributed equally to this work. Received 11 June 2009 ; revised 11 January 2010; accepted 17 January 2010 2 Colegio de Postgraduados Campus Cordoba, Km 348 Carretera Federal Cordoba-Veracruz , Congregacio n Manuel Leon Amatlan de los Reyes, Cordoba, Veracruz, C.P. 94946, Mexico 3 Laboratory of Apiculture and Social Insects, Department of Biological and Environmental Science, University of Sussex , Falmer, Brighton BN1 9QG, UK 4 Department of Ecology and Evolutionary Biology, University of Arizona , 1041 E. Lowell St., Tucson, AZ 85721-0088, USA 5 Institute of Integrative and Comparative Biology, University of Leeds , Leeds, LS2 9JT, UK 6 Department of Animal and Plant Sciences, University of Sheffield , Sheffield, S10 2TN, UK Sexual selection is a dominant force in the evolution of many animals and can be particularly significant in species that mate in aerial swarms characterized by strong male-male competition. However, such mating biology, typical of many social insects, is also quite challenging to study. Here, we investigate sexual selection in the honey bee that has 2 distinct male morphs (normal sized and small). Males mate only once and females return to their nest after mating, making it possible to measure the lifetime fitness of both sexes. We allowed known numbers of normal-sized males from 6 colonies and small males from another 6 colonies to compete for natural matings with experimental virgin queens. We then determined the mating success of males by genotyping the offspring of these queens. Colonies differed by an order of magnitude in the intrinsic mating success of their males, confirming that the reproductive fitness of honey bee colonies is highly variable. Small males achieved approximately half as many matings as expected given their number of flights and, in addition, had a significantly smaller share of paternity per mating than normal-sized males. Interestingly, the flight activity of small males suggested that they may compensate for their lower competitiveness by flying outside the most competitive mating period in the afternoon. The lower fitness of small males shows that sexual selection is strong in honey bees and contributes to inclusive fitness dynamics that favor worker cooperation within their societies. - Ca common and significant feature of the biology of animals ompetition between males for matings with females is (Andersson 1994; Alcock 2005). It can be particularly extreme when the operational sex ratio is male biased (Clutton-Brock and Parker 1992), as is the case in the many insect species in which large numbers of males form swarms within which there is intense competition to mate with females (Thornhill and Alcock 1983). In this competitive arena, females may select males directly precopulation, but more commonly do so indirectly, by mating with males that are faster, more agile, or more persistent fliers. Females, in addition, may select males postcopulation, again directly or indirectly (Eberhard 1996). Female selection precopulation may result in larger males that are more powerful fliers if selection is based on flight speed or persistence, smaller males if selection is based on agility, or both strategies in some species (Neems et al. 1992; Pitnick et al. 2009). Many social insects, specifically ants, termites, and some bees, provide classic examples of such swarm-based mating biology. In some, obligate monogamy combined with a sex ratio close to 1:1 makes sexual selection weak (Boomsma et al. 2005; Boomsma 2007). In other species, though, in which the operational sex ratio is highly male biased or males are capable of remating, sexual selection is likely to be particularly strong (Heinze and Holldobler 1993; Heinze and Tsuji 1995; Boomsma et al. 2005). However, studying sexual selection in social insects is notoriously difficult, and the evidence is consequently limited. Matings often take place in midair and are stimulated by precise environmental conditions, making controlled matings impossible. Furthermore, females (queens) normally disperse after mating, making it difficult or impossible to quantify the fitness of the partners postmating. One exception to this is the honey bee (Apis mellifera). The act of mating is instantaneously fatal to honey bee males, so their fitness is linked completely to that of a single queen, and queens return to their natal nest after mating. As a result, the subsequent fitness of both partners can be readily determined (Gary 1963; Winston 1995; Koeniger, Koeniger, Gries, and Tingek 2005). Honey bee males (drones) gather in distinct dro (...truncated)


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Margaret J. Couvillon, William O.H. Hughes, Juan A. Perez-Sato, Stephen J. Martin, Gabrielle G.F. Roy, Francis L.W. Ratnieks. Sexual selection in honey bees: colony variation and the importance of size in male mating success, Behavioral Ecology, 2010, pp. 520-525, 21/3, DOI: 10.1093/beheco/arq016