Abstract
The life cycle of many social insects living in seasonal environments is characterized by a period of (pure) investment into worker brood followed by a phase of pure allocation of resources to the production of sexuals. Researchers have invested some effort to find possible correlates (proximate triggers) of this transition but current empirical knowledge does not provide clear evidence. Utilizing an established theoretical model—modified to account for brood developmental time—we show that a strategy that switches to the production of sexuals at a particular (fixed) date may typically perform better than strategies linking the transition to the status of the colony in terms of attributes like worker or brood number, or the colony’s age. Our results provide rationale why the search for cues triggering the transition in investment has been inconclusive at best and suggests a number of experiments and observations that allow validating our arguments.
Similar content being viewed by others
References
Alaux C, Jaisson P, Hefetz A (2005) Reproductive decision-making in semelparous colonies of the bumblebee Bombus terrestris. Behav Ecol Sociobiol 59:270–277. https://doi.org/10.1007/s00265-005-0035-6
Banks HT, Banks JE, Bommarco R, Laubmeier AN, Myers NJ, Rundlöf M, Tillman K (2017) Modeling bumble bee population dynamics with delay differential equations. Ecol Model 351:14–23. https://doi.org/10.1016/j.ecolmodel.2017.02.011
Beekman M, Van Stratum P (2000) Does the diapause experience of bumblebee queens Bombus terrestris affect colony characteristics? Ecol Entomol 25:1–6. https://doi.org/10.1046/j.1365-2311.2000.00235.x
Beekman M, Lingeman R, Kleijne FM, Sabelis MW (1998) Optimal timing of the production of sexuals in bumblebee colonies. Entomol Exp Appl 88:147–154. https://doi.org/10.1046/j.1570-7458.1998.00356.x
Bourke AFG, Ratnieks FLW (2001) Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae). Proc R Soc B Biol Sci 268:347–355. https://doi.org/10.1098/rspb.2000.1381
Bradshaw WE, Holzapfel CM (2006) Evolutionary response to rapid climate change. Science 312:1477–1478. https://doi.org/10.1126/science.1127000
Deleurance EP (1950) Sur le mécanisme de la monogynie fonctionnelle chez les Polistes (Hyménoptères-Vespides). Comptes Rendus Hebdomadaires des Seances de L’Academie des Sciences 230:782–784
Duchateau MJ, Velthuis HHW (1988) Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107:186–207. https://doi.org/10.1163/156853988X00340
Duchateau MJ, Velthuis HHW, Boomsma JJ (2004) Sex ratio variation in the bumblebee Bombus terrestris. Behav Ecol 15:71–82. https://doi.org/10.1093/beheco/arg087
Gosterit A (2011) Effect of different reproductive strategies on colony development characteristics in Bombus terrestris L. J Apic Sci 55:45–51
Goulson D (2003) Bumblebees. Their behaviour and ecology. Oxford University Press, Oxford
Greene A, Akre RD, Landolt P (1976) The aerial yellowjacket, Dolichovespula arenaria (Fab.): nesting biology, reproductive pro- duction, and behavior (Hymenoptera: Vespidae). Melanderia 26:1–34
Helfrich-Förster C (2004) The circadian clock in the brain: a structural and functional comparison between mammals and insects. J Comp Physiol A 190:601–613. https://doi.org/10.1007/s00359-004-0527-2
Hirata M, Cronin AL, Kidokoro M, Azuma N (2005) Spatio-temporal variation of colony structure and eusociality level of the Japanese sweat bee Lasioglossum (Evylaeus) duplex (Hymenoptera: Halictidae). Ecol Res 20:75–79. https://doi.org/10.1007/s11284-004-0005-x
Holland JG, Guidat FS, Bourke AFG (2013) Queen control of a key life-history event in a eusocial insect. Biol Lett 9:20130056. https://doi.org/10.1098/rsbl.2013.0056
Ikan R, Gottlieb R, Bergmann ED, Ishay J (1969) The pheromone of the queen of the Oriental hornet, Vespa orientalis. J Insect Physiol 15:1709–1712. https://doi.org/10.1016/0022-1910(69)90003-1
Iwasa Y, Levin SA (1995) The timing of life history events. J Theor Biol 172:33–42. https://doi.org/10.1006/jtbi.1995.0003
King D, Roughgarden J (1982) Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theor Popul Biol 22:1–16. https://doi.org/10.1016/0040-5809(82)90032-6
Kreitzman L, Foster R (2010) Seasons of life: the biological rhythms that enable living things to thrive and survive. Profile Books, London. ISBN 978-1-84765-279-9
Lövgren B (1958) A mathematical treatment of the development of colonies of different kinds of social wasps. Bull Math Biophys 20:119–148. https://doi.org/10.1007/BF02477572
Macevicz S, Oster GF (1976) Modeling social insect populations II: optimal reproductive strategies in annual eusocial insect colonies. Behav Ecol Sociobiol 1:265–282
Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B Biol Sci 365:3177–3186. https://doi.org/10.1098/rstb.2010.0148
Mitesser O, Weissel N, Strohm E, Poethke HJ (2006) The evolution of activity breaks in the nest cycle of annual eusocial bees: a model of delayed exponential growth. BMC Evolut Biol 6:45
Mitesser O, Weissel N, Strohm E, Poethke HJ (2007) Adaptive dynamic resource allocation in annual eusocial insects: environmental variation will not necessarily promote graded control. BMC Ecol 7:16. https://doi.org/10.1186/1472-6785-7-16
Muller CB, Schmid-Hempel P (1992) Variation in life-history pattern in relation to worker mortality in the bumble-bee, Bombus lucorum. Funct Ecol 6:48–56. https://doi.org/10.2307/2389770
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Monographs in population biology. Princeton University Press, Princeton
Poethke HJ, Hovestadt T, Mitesser O (2016) The evolution of optimal emergence times: bet hedging and the quest for an ideal free temporal distribution of individuals. Oikos 125:1647–1656. https://doi.org/10.1111/oik.03213
Poitrineau K, Mitesser O, Poethke HJ (2009) Workers, sexuals, or both? Optimal allocation of resources to reproduction and growth in annual insect colonies. Insectes Sociaux 56:119–129. https://doi.org/10.1007/s00040-009-0004-6
Potter NB (1964) A study of the biology of the common wasp, Vespula vulgaris L., with special reference to the foraging behaviour. PhD Thesis, University of Bristol
Reeve HK, Gamboa GJ (1983) Colony activity integration in primitively eusocial wasps: the role of the queen (Polistes fuscatus, Hymenoptera: Vespidae). Behav Ecol Sociobiol 13:63–74. https://doi.org/10.1007/BF00295077
Röseler PF (1967) Untersuchungen über das Auftreten der 3 Formen im Hummelstaat. Zoologisches Jahrbuch, Abt Allgemeine Zoologie, Physiologie der Tiere 74:178–197
Röseler PF (1970) Unterschiede in der Kastendetermination zwischen den Hummelarten Bombus hypnorum und Bombus terrestris. Zeitschrift für Naturforschung 25b:543–548
Röseler PF (1991) Roles of morphogenetic hormones in caste polymorphism in bumble bees. In: Gupta AP (ed) Morphogenetic hormones in arthropods: roles in histogenesis, organogenesis, and morphogenesis. Rutgers University Press, New Brunswick, pp 384–399
Rottler-Hoermann AM, Schulz S, Ayasse M (2016) Nest wax triggers worker reproduction in the bumblebee Bombus terrestris. R Soc Open Sci 3:150599. https://doi.org/10.1098/rsos.150599
Saunders DS (2002) Insect clocks, 3rd edn. Elsevier, Amsterdam
Sharma VK (2003) Adaptive significance of circadian clocks. Chronobiol Int 20:901–919
Shpigler H, Tamarkin M, Gruber Y, Poleg M, Siegel AJ, Bloch G (2013) Social influences on body size and developmental time in the bumblebee Bombus terrestris. Behav Ecol Sociobiol 67:1601–1612. https://doi.org/10.1007/s00265-013-1571-0
Shykoff JA, Muller CB (1995) Reproductive decisions in bumble-bee colonies: the influence of worker mortality in Bombus terrestris (Hymenoptera, Apidae). Funct Ecol 9:106–112. https://doi.org/10.2307/2390096
Smith ML, Ostwald MM, Loftus JC, Seeley TD (2014) A critical number of workers in a honeybee colony triggers investment in reproduction. Naturwissenschaften 101:783–790. https://doi.org/10.1007/s00114-014-1215-x
Spradbery JP (1971) Seasonal changes in the population structure of wasp colonies (Hymenoptera: Vespidae). J Anim Ecol 40:501–523. https://doi.org/10.2307/3259
Verriest EI, Dirr G, Helmke U (2016a) Delayed resource allocation optimization with applications in population dynamics. IFAC PapersOnLine 49:1–6. https://doi.org/10.1016/j.ifacol.2016.07.463
Verriest EI, Dirr G, Helmke U, Mitesser O (2016b) Explicitly solvable bilinear optimal control problems with applications in ecology. In: 22nd international symposium on mathematical theory of networks and systems. University of Minnesota, Minneapolis, pp 538–541
Acknowledgements
We thank two anonymous reviewers for their comments, which helped to improve the manuscript.
Funding
Funding was provided by the German Research Foundation (DFG), Collaborative Research Center SFB 1047 “Insect timing”, Project C6 to TH.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hovestadt, T., Degen, T. & Mitesser, O. Suitable triggers for timing the transition from worker to sexual production in annual eusocial insects. Insect. Soc. 65, 609–617 (2018). https://doi.org/10.1007/s00040-018-0652-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-018-0652-5