The evolution of activity breaks in the nest cycle of annual eusocial bees: a model of delayed exponential growth

BMC Evolutionary Biology BioMed Central Research article Open Access The evolution of activity breaks in the nest cycle of annual eusocial bees: a model of delayed exponential growth Oliver Mitesser*1, Norbert Weissel2, Erhard Strohm3 and HansJoachim Poethke1 Address: 1Forschungsstation 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: 02 June 2006 BMC Evolutionary Biology 2006, 6:45 doi:10.1186/1471-2148-6-45 Received: 25 December 2005 Accepted: 02 June 2006 This article is available from: http://www.biomedcentral.com/1471-2148/6/45 © 2006 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: Social insects show considerable variability not only in social organisation but also in the temporal pattern of nest cycles. In annual eusocial sweat bees, nest cycles typically consist of a sequence of distinct phases of activity (queen or workers collect food, construct, and provision brood cells) and inactivity (nest is closed). Since the flight season is limited to the time of the year with sufficiently high temperatures and resource availability, every break reduces the potential for foraging and, thus, the productivity of a colony. This apparent waste of time has not gained much attention. Results: We present a model that explains the evolution of activity breaks by assuming differential mortality during active and inactive phases and a limited rate of development of larvae, both reasonable assumptions. The model predicts a systematic temporal structure of breaks at certain times in the season which increase the fitness of a colony. The predicted pattern of these breaks is in excellent accordance with field data on the nest cycle of the halictid Lasioglossum malachurum. Conclusion: Activity breaks are a counter-intuitive outcome of varying mortality rates that maximise the reproductive output of primitively eusocial nests. Background Some of the most important components of life history decisions refer to the optimal timing of accumulation of resources and their allocation to growth and reproduction. At any time during its life an organism has not only to spend resources on the conflicting requirements for maintenance, somatic growth, and reproduction, but has also to decide on how much and when resources like food or building material should be accumulated in order to maximise reproductive output. Up to now, theoretical studies on life history strategies of eusocial insects have mainly focused on the first aspect: optimal resource allocation [1-4]. However, the obvious and ample variability in seasonal activity patterns within and between species of eusocial insects requires investigating the optimal timing of resource accumulation too. Seasonal activity patterns vary widely among the species of bees and wasps that have been studied as model organisms for the evolution of sociality in insects [5-7]. Many Page 1 of 12 (page number not for citation purposes) BMC Evolutionary Biology 2006, 6:45 annual Polistes, Vespa, Xylocopa and Allodape species show continuous colony activity during the whole season [811]. This results in a more or less continuous production of offspring as is assumed in the classical model of colony development by Macevicz and Oster (1976). Model predictions have been tested and were met in field data from Polistes and Vespa species [1]. However, the nest cycle of most halictids (e.g. in the genera Lasioglossum and Halictus) is characterized by several discrete broods that are separated by distinct activity breaks [[6,12,13], but see [14] and [15]]. During the solitary founding phase, halictid queens construct nests and supply brood cells with pollen and nectar as provisions for their larvae. After a break of a few weeks, during which the nest is closed and no activity outside the nest can be observed, a first worker brood emerges and starts collecting pollen and nectar to provision the eggs that are usually laid by the queen. Subsequent broods are also separated by breaks during which nests are closed and no outside activity can be observed. Activity breaks can last up to three weeks [[12,16], Weissel et al., submitted]. Usually sexuals emerge in the last brood only, while all other broods consist mainly of workers. There are also species with an intermediate position between continuous growth and discrete broods. In Bombus species, for example, the nest cycle is organized in more or less discrete broods but without activity breaks and nest closure [17]. http://www.biomedcentral.com/1471-2148/6/45 Furthermore one could suppose that activity breaks after the emergence of the first workers just appear when worker mortality is rather high and all workers of a brood have died before emergence of the individuals of a second brood. However, it is clear from field observations that the breaks do not occur simply because all workers of a brood have died. Some workers even survive a complete activity break and continue foraging when the nest is reopened [[16], Weissel and Strohm unpublished]. On the contrary, breaks occur even though there are still some workers alive in a nest, showing that there has to be some advantage of interrupting foraging activity. The well-known colony growth model of Macevicz & Oster (1976) for insect colonies identifies the sequential production of workers first and sexuals just before the ending of the flight season (so called bang-bang reproduction) as the optimal investment strategy to maximize colony fitness. Whereas this model assumes instantaneous occurrence of adult progeny the model that we present accounts for a certain development time of the larvae. The results of our model challenge the assumption that only variation in environmental factors governs the emergence of activity breaks. The model explains the evolution of the observed activity patterns rather by an asymmetric interaction between endogenous and exogenous factors of colony development. Results Due to temperature-dependence of their activity and resource availability, ectothermic organisms, like insects, have to adjust their life history to the seasonal conditions in temperate latitudes. Reproduction and growth must be completed within a limited time span and the unfavourable period has to be bridged by diapause. Variability in biotic and abiotic conditions during the reproductive period has been assumed to cause changes (...truncated)