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Platt,T.*, Queller, D. C., and Strassmann, J. E. 2004. Aggression

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Platt,T.*, Queller, D. C., and Strassmann, J. E. 2004. Aggression ANIMAL BEHAVIOUR, 2004, 67, 1e10 doi:10.1016/j.anbehav.2003.01.005 Aggression and worker control of caste fate in a multiple-queen wasp, Parachartergus colobopterus THOMAS G. PLATT, DAVID C. QUELLER & JOAN E. STRASSMANN Department of Ecology and Evolutionary Biology, Rice University (Received 5 June 2002; initial acceptance 21 October 2002; final acceptance 9 January 2003; MS. number: A9376R) Although famously cooperative, social insect colonies harbour considerable potential for genetic conflict among colonymates. This conflict may be expressed behaviourally as aggression by workers. We investigated aggression in 34 colonies of the wasp Parachartergus colobopterus, by evaluating the characteristics of both instigators and victims of aggressive interactions. We estimated genetic relatedness and queen number using DNA microsatellites and found that workers and emerging females should be most in conflict over the caste of the latter when there are many queens on the nest. We found that aggressive interactions are more likely to involve older workers attacking either males or younger workers, and that victim and aggressor females have more ovarian development than randomly sampled colonymates. Moreover, mated females with low levels of ovarian development relative to active queens were also more likely to be aggressors and victims than were randomly sampled females. Aggression among females supports the hypothesis that older workers use aggression towards younger females as a means of policing the development of emerging females into queens. Workers also may use aggression to suppress the reproduction of some mated females. Our findings thus support the hypothesis that genetic conflicts of interest motivate worker aggression in swarm-founding wasp colonies. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Insect societies typically show high degrees of coopera- Epiponini (Strassmann et al. 1991, 1997, 2002; Goodnight tion, with a reproductive division of labour so great that et al. 1996; Herman et al. 2000). they are often viewed as superorganisms (Seeley 1989; Epiponine wasp societies have many complex features: Wilson & Sober 1989; Moritz & Southwick 1992; Ratnieks they have an advanced division of labour, task partition- & Reeve 1992). Kin selection theory has served as ing, alarm and trail pheromones, and large colony sizes a framework for providing insight into the evolution of (Jeanne 1980, 1991, in press; Zucchi et al. 1995). Yet, in this cooperation (Hamilton 1964; Bourke & Franks 1995; contrast with other highly eusocial insects, many epipo- Crozier & Pamilo 1996; Bourke 1997; Queller & Strass- nine wasps have weak caste differentiation (Bourke 1999; mann 1998). It has also provided a framework for O’Donnell 1998; Jeanne, in press). Parachartergus colobop- understanding potential conflicts within these societies, terus colonies typically have large numbers of workers and because colonymates are genetically distinct from one a varying number of singly mated queens, with little or no another and thus have different genetic interests con- morphological caste differences between workers and cerning reproduction (Hamilton 1964; Trivers & Hare queens (Strassmann et al. 1991, 1997, 1998; Goodnight 1976; Ratnieks 1988; Pamilo 1991; Ratnieks & Reeve 1992; et al. 1996). As in some other epiponine societies Queller & Strassmann 1998; Keller & Chapuisat 1999; (Metapolybia azecoides, Synoeca surinama: West-Eberhard Keller & Reeve 1999). Conflicts of interest between 1978, 1981), emerging P. colobopterus females are totipo- colonymates can manifest themselves in a variety of ways tent. They can become either workers or queens (Strass- including oophagy and direct aggression (e.g. Ratnieks & mann et al. 2002). This leads to potential conflict over Visscher 1989; Gobin et al. 1999). Our study focuses caste determination because individuals gain more from on whether genetic conflicts of interest motivate behav- becoming queens than do colonymates (Strassmann 1989; ioural aggression in the well-studied swarm-founding Bourke & Ratnieks 1999; Ratnieks 2001; Reuter & Keller Neotropical wasp, Parachartergus colobopterus, of the tribe 2001). In accord with worker collective interests, new Correspondence: J. E. Strassmann, Department of Ecology and P. colobopterus queens are produced only when queen Evolutionary Biology, Rice University, 6100 Main Street, MS 170, number is low (Strassmann et al. 1991, 2002; Queller Houston, TX 77005, U.S.A. (email: [email protected]). et al. 1993). This raises the question of how totipotent 1 0003e3472/03/$30.00/0 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 2 ANIMAL BEHAVIOUR, 67, 1 females emerging on nests with many queens are kept interaction involved one wasp working its mandibles over from becoming queens themselves when it may be in another in a chewing, snapping or biting action, often their interest to do so. Females attempting to become with the aggressor on top of the victim. Aggressive a queen could be forced to become workers instead (West- interactions also often included the aggressor curving Eberhard 1978, 1981; Herman et al. 2000; Strassmann her gaster and exposing her sting to the victim. The victim et al. 2002), an option not possible when there are fixed sometimes responded by curling over on her side and caste differences, as in Melipona stingless bees, where remaining motionless, even after we pulled the actor off workers slaughter excess queens (Imperatriz-Fonseca & (Strassmann et al. 1997). Sometimes the aggressor dragged Zucchi 1995). the victim to another part of the nest. Each such Eusocial wasp males seldom work or forage; yet they do aggressive interaction typically lasted several seconds, depend on the colony for support. Consequently, the and may be similar to an exaggerated form of biting presence of males on a nest can impose substantial costs behaviour of Polybia wasps (O’Donnell & Jeanne 1995; to social insect colonies (O’Donnell 1999). Moreover, O’Donnell 2001a). Aggressive interactions had a clear workers are more related to female larvae than to adult beginning and most probably would have ended with the males, and thus should favour investing in the former victim running away or flying off the nest had we not over the latter (Hamilton 1972; Trivers & Hare 1976; Starks removed one party (see below). These aggressive acts were & Poe 1997). Workers may use aggression towards males quite stereotyped and did not vary greatly in intensity, to minimize the colony costs they impose and discourage making them a clear class for sampling. We distinguished investment in males. aggression from social grooming by noting that the latter This study examines aggression on a large sample of P. involves one wasp slowly and gently working her mouth- colobopterus colonies. We predicted that males and young parts and mandibles over another wasp’s body while females would be the targets of aggression because of their antennating her and never involves snapping or biting, genetic conflicts with workers. the exposure of the actor’s sting, or the pulling of the recipient to another part of the nest (Strassmann et al. 1997). Also, social grooming does not induce curling in the recipient. We distinguished aggression from solicita- METHODS tion for trophyllaxis by noting that the key feature of the Sampling latter always involves bites directed towards the mandibles of another wasp and seldom extends to generalized We observed 34 P. colobopterus colonies on the campus of aggression with bites directed at the rest of the body the Universidad Central de Venezuela at Maracay, Ven- (Strassmann et al. 1997). ezuela (10(16#N, 67(36#W, altitude 445 m) over 5 days We collected only one of the participants because we (6e10 August 1999) during the rainy season. To sample and could not accurately collect both participants in a single observe the entire nest, we removed the surrounding interaction. Although collecting only one participant envelope of each colony. Removal of the envelope does meant that we had very accurate samples of aggressors not disturb the nest comb because the envelope and the and victims, we could not associate interactants with comb are independently attached to the substrate. Thus, we a particular task (i.e. to determine whether subcategories could observe all areas of the nest for activity and sample of aggressors attacked subcategories of victims). This did wasps from any part of the nest. Following envelope not prove to be a problem because of the strong overall removal, we gave the wasps at least 10 min to resume patterns we found (see Results) and because we were most normal activity before starting observations. interested in comparing victims and aggressors with We were interested in quantifying two aspects of a random sample that, by definition, could not be paired aggressive behaviour: frequency of aggression, and who with particular acts. The random sample consisted of 12 participates in aggressive interactions. To quantify the individuals plucked at random from all areas of the nest aggression level of each colony, we counted all aggressive comb and the substrate surface behind the nest structure. interactions that occurred on the exposed combs for 30 We used this random sample to estimate average re- min (Table 1). We conducted all observations during clear latedness and to provide a baseline for ovarian develop- weather between 0900 and 1600 hours, when the wasps ment and mating status. We stored all individuals and were most active. Our time frame of 30 min to characterize comb parts in 100% ethanol, which is sufficient for aggressive activity of a colony is based on hundreds of accurate assessment of ovarian development and insem- hours of observing these wasps (Strassmann et al. 1991, ination status and for preserving DNA for microsatellite 1997, 1998, 2002; Queller et al. 1993; Herman et al. 2000) genotyping (Strassmann et al. 2002). and on a preliminary study from the previous year in For each colony, we counted the number of adults on the which we watched fewer colonies for periods of 3 h or nest and the number of combs (Table 1).
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