Adaptive dynamic resource allocation in annual eusocial insects: environmental variation will not necessarily promote graded control

BMC Ecology BioMed Central Research article Open Access Adaptive dynamic resource allocation in annual eusocial insects: environmental variation will not necessarily promote graded control Oliver Mitesser*1, Norbert Weissel2, Erhard Strohm3 and HansJoachim Poethke1 Address: 1Field Station Fabrikschleichach, Universität Würzburg, Glashüttenstr. 5, D-96181 Rauhenebrach, Germany, 2Biozentrum (Zoologie III), Universität Würzburg, Am Hubland, D-97074 Würzburg, Germany and 3Institut für Zoologie, Universität Regensburg, Universitätsstr. 31, 93040 Regensburg, Germany Email: Oliver Mitesser* - ; Norbert Weissel - ; Erhard Strohm - ; Hans-Joachim Poethke - * Corresponding author Published: 19 December 2007 BMC Ecology 2007, 7:16 doi:10.1186/1472-6785-7-16 Received: 25 December 2006 Accepted: 19 December 2007 This article is available from: http://www.biomedcentral.com/1472-6785/7/16 © 2007 Mitesser et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: According to the classical model of Macevicz and Oster, annual eusocial insects should show a clear dichotomous "bang-bang" strategy of resource allocation; colony fitness is maximised when a period of pure colony growth (exclusive production of workers) is followed by a single reproductive period characterised by the exclusive production of sexuals. However, in several species graded investment strategies with a simultaneous production of workers and sexuals have been observed. Such deviations from the "bang-bang" strategy are usually interpreted as an adaptive (bet-hedging) response to environmental fluctuations such as variation in season length or food availability. To generate predictions about the optimal investment pattern of insect colonies in fluctuating environments, we slightly modified Macevicz and Oster's classical model of annual colony dynamics and used a dynamic programming approach nested into a recurrence procedure for the solution of the stochastic optimal control problem. Results: 1) The optimal switching time between pure colony growth and the exclusive production of sexuals decreases with increasing environmental variance. 2) Yet, for reasonable levels of environmental fluctuations no deviation from the typical bang-bang strategy is predicted. 3) Model calculations for the halictid bee Lasioglossum malachurum reveal that bethedging is not likely to be the reason for the graded allocation into sexuals versus workers observed in this species. 4) When environmental variance reaches a critical level our model predicts an abrupt change from dichotomous behaviour to graded allocation strategies, but the transition between colony growth and production of sexuals is not necessarily monotonic. Both, the critical level of environmental variance as well as the characteristic pattern of resource allocation strongly depend on the type of function used to describe environmental fluctuations. Conclusion: Up to now bet-hedging as an evolutionary response to variation in season length has been the main argument to explain field observations of graded resource allocation in annual eusocial insect species. However, our model shows that the effect of moderate fluctuations of environmental conditions does not select for deviation from the classical bang-bang strategy and that the evolution of graded allocation strategies can be triggered only by extreme fluctuations. Detailed quantitative observations on resource allocation in eusocial insects are needed to analyse the relevance of alternative explanations, e.g. logistic colony growth or reproductive conflict between queen and workers, for the evolution of graded allocation strategies. Page 1 of 13 (page number not for citation purposes) BMC Ecology 2007, 7:16 Background The optimal allocation of accumulated resources to maintenance, growth, and reproduction is the central topic of life history theory. At any time during its life an organism must decide whether it will allocate available resources to maintenance, to somatic growth (that will allow for larger reproductive potential in the future), or to reproduction. In particular, the existence of a trade-off between growth and reproduction has been well confirmed [1,2]. Much theoretical and field work has been invested to understand the pattern of investment into growth and reproduction and to predict which allocation strategies will maximise an organism's fitness [3-5]. Since the first paper by Cole [6] theoretical analysis of life history strategies has focused on solitary organisms (for reviews see [1,2,4,7]). In contrast, since the eminent work of Macevicz and Oster [8] the evolutionary analysis of nest cycle dynamics in social species has not gained much further attention [9,10]. For social insects the problem of an optimised investment into growth and reproduction mostly concerns the growth of the colony as a whole; how much resources should be allocated to increase worker number and how much to the production of sexuals? As the answer to this problem strongly depends on the time left until the end of the season and as this quantity continuously changes we refer to optimal investment patterns as dynamic strategies. Dynamic allocation strategies in eusocial insects have first been analysed by Macevicz and Oster [8] and Oster and Wilson [11]. Macevicz and Oster [8] analysed the prototype of an annual eusocial colony cycle as exhibited by many vespid wasps, bumble bees and halictid bees and calculated optimal resource allocation strategies for the case of predictable or constant season length [8,12]. When season length is fixed and conditions are constant during the season the predicted optimal investment pattern is a simple "bangbang" strategy with the annual productivity cycle divided into two phases; colonies should start with a phase of pure colony growth, i.e. the exclusive production of workers, and – at some time – abruptly switch to a purely reproductive phase with the exclusive production of male and female sexuals. The optimal moment to switch between the two phases is entirely determined by season length, worker productivity rate, and worker mortality rate. However, already Greene [13] has pointed out that colony development of many annual eusocial insects does not conform to the predicted bang-bang strategy but is characterised by a gradual shift from the production of workers to the production of sexuals. Such "graded control" has been reported in wasps [13-19], bumble bees [20,21] and halictids [22-25]. http://www.biomedcentral.com/1472-6785/7/16 Although sufficiently detailed quantitative data are hardly available, the halictid bee Lasioglossum malachurum can serve as one example of this type of colony dynamics. Recent stud (...truncated)