Adaptive tuning of an extended phenotype: honeybees seasonally shift their honey storage to optimize male production Michael L. Smith * , Madeleine M. Ostwald, Thomas D. Seeley Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, U.S.A. article info Article history: Received 27 November 2014 Initial acceptance 16 December 2014 Final acceptance 30 December 2014 Published online MS. number: A14-00961 Keywords: Apis mellifera breeding season drone comb extended phenotype food storage honeybee nest structure seasonal reproduction social insect Organisms face the challenge of optimally allocating limited resources among investments that promote survival, growth or reproduction. In species whose members build complex nests, this resource alloca- tion problem also applies to the building and use of the nest structure, a critical part of an individual's extended phenotype. Honeybee colonies face an acute problem of properly allocating one nest resource in particular, large cells of drone comb built for rearing drones, between reproduction (rearing drones) and survival (storing honey). Here the trade-off is inescapable, because a drone cell cannot be used simultaneously for drone production and honey storage. We predicted that the workers in a honeybee colony would solve this problem by preferentially using drone comb for producing drones when their mating opportunities are good (spring and early summer) and for honey storage when the drones' mating opportunities are poor (late summer and autumn). To test our prediction, we experimentally tested how drone comb and worker comb were used for honey storage from April to September. In spring and early summer, workers preferentially removed honey from drone comb, making it available for producing drones. In late summer and autumn, workers did not preferentially remove honey from drone comb. This study shows that a honeybee colony is able to fine-tune its extended phenotype by adaptively allocating a key nest resource, its drone comb, between survival and reproduction. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. To maximize its lifetime reproductive success, an organism must optimally allocate its resources among survival, growth and reproduction (Stearns, 1992, page 72). This problem of optimal resource allocation pertains not only to the organism itself, but also to its extended phenotype if it is an organism that builds an external structure (Dawkins, 1982, page 195). For example, a female golden-silk orb weaver spider, Nephila clavipes, must allocate her silk and her time spent building between her web, which enhances her survival and growth, and her eggsac, which is key to her reproduction (Rainer, 2010, page 252). Likewise, a colony of yellow jacket wasps (Vespula spp.), which builds a paper nest containing combs enclosed in a protective envelope, must allocate its building materials and building efforts between small-cell combs for rearing workers, to boost colony survival and growth, and large-cell combs for rearing reproductives, for colony reproduction (Greene, 1991; Spradbery, 1973, page 97). Similarly, a male white-headed buffalo weaver bird, Dinemellia dinemelli, must allocate his time between gathering different nest materials for different purposes: soft grasses for the egg chamber, an investment in reproduction, and hard thorns for defending the nest's top and sides against preda- tors, an investment in survival (Collias & Collias, 1964). So, just as all organisms must fine-tune their physiology to adaptively allocate resources among survival, growth and reproduction, organisms that also build external structures must also fine-tune how they build and use these structures so that their extended phenotypes are adaptively allocated among survival, growth and reproduction. A honeybee colony illustrates especially clearly how trade-offs among survival, growth and reproduction can arise when the sur- vival machinery of a living system includes an architectural struc- ture. Unlike in the structures just mentioned, the beeswax combs that honeybees build can be used to boost survival or reproduction, depending on how the combs are used. A honeybee colony builds two types of comb: drone comb and worker comb (reviewed by Pratt, 2004). The hexagonal cells in drone comb are larger than those in worker comb (wall-to-wall dimension: 6.4 mm versus 5.2 mm) (Martin & Lindauer, 1966; Taber & Owens, 1970). The cells in both types of comb can be used for honey storage as well as brood rearing, but these two uses of a cell are mutually exclusive, so a colony faces a trade-off between survival (honey storage) and reproduction (brood rearing) in using its combs (Fig. 1). How does a * Correspondence: M. L. Smith, Department of Neurobiology and Behavior, Cor- nell University, Ithaca, NY 14853, U.S.A. E-mail address: mls453@cornell.edu (M. L. Smith). Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav http://dx.doi.org/10.1016/j.anbehav.2015.01.035 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Animal Behaviour 103 (2015) 29e33