Sexual selection in honey bees: colony variation and the importance of size in male mating success
Margaret J. Couvillon
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William O.H. Hughes
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Juan A. Perez-Sato
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Stephen J. Martin
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Gabrielle G.F. Roy
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Francis L.W. Ratnieks
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The Author 2010. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions
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@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
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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
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Laboratory of Apiculture and Social Insects, Department of Biological and Environmental Science, University of Sussex
, Falmer, Brighton BN1 9QG,
UK
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Department of Ecology and Evolutionary Biology, University of Arizona
, 1041 E. Lowell St., Tucson,
AZ 85721-0088, USA
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Institute of Integrative and Comparative Biology, University of Leeds
, Leeds, LS2 9JT,
UK
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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.
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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)