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Molina, Y. & S. O'donnell. 2009. Worker Reproductive Competition

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Molina, Y. & S. O'donnell. 2009. Worker Reproductive Competition Insect. Soc. 56 (2009) 14 – 20 0020-1812/09/010014-7 Insectes Sociaux DOI 10.1007/s00040-008-1027-0 Birkhuser Verlag, Basel, 2008 Research article Worker reproductive competition affects division of labor in a primitively social paperwasp (Polistes instabilis) Y. Molina and S. ODonnell Animal Behavior Program, Department of Psychology, Box 351525, University of Washington, Seattle, WA 98195 USA, e-mail: [email protected] Received 6 June 2008; revised 11 August 2008; accepted 12 August 2008. Published Online First 23 September 2008 Abstract. Social insects are premier models for studying Introduction the evolution of self-organization in animal societies. Primitively social species may be informative about the The shift from centralized to distributed social organiza- early stages of social evolution and transitions in self- tion is one of the major transitions in the evolution of organization. Previous worker removal studies in Polistes social behavior (Bourke, 1999; Jeanne, 2003). Social instabilis paper wasps suggested that dominant but non- organization in primitively eusocial species, such as egglaying workers play an important role in regulating independent founding (IF) paper wasps, often depends rates of task performance by inducing foraging in sub- on physical aggression from queens (Reeve, 1991; Ga- ordinates.ACHTUNGRE We extend previous worker removal studies by dagkar, 2001). Queen aggression suppresses direct repro- quantifying changes in individuals behavior following duction in workers, and also promotes helping behavior removals, and by measuring associations between behav- (Gamboa et al., 1990; Premnath et al., 1996; ODonnell, ioral change and individuals reproductive capacity (ovary 1998b; Bruyndonckx et al., 2006). Inducing helping development). Workers changed their rates of aggressive behavior may further reduce reproductive competition behaviors more than queens following the dominant for the queens. For example, foraging precludes subordi- worker removals. Increases in workers rates of aggressive nates from egglaying (Keeping, 1992; Powell and Tschin- behaviors were correlated with decreases in their foraging kel, 1999). In some species, queens are the most active rates. Changes in individual rates of social aggression were individuals in colonies (Reeve, 1991; ODonnell, 1998b). associated with their reproductive capacity: worker fe- Queen control of workers task performance appears to males with well-developed ovaries increased their rates of be an effective mode of social organization in small aggression. Further changes in rates of aggression after the colonies. Reproductive competition may have been the dominant workers were returned also depended on ovary primary mechanism to establish and regulate division of development. These patterns suggest that task perform- labor in the early stages of social evolution. ance and potential fecundity are linked in workers, and In contrast, reproductive competition does not appear that worker interactions play a strong role in regulating to influence task performance in more derived, larger task performance. We conclude that worker reproductive societies, such as swarm-founding paper wasps, honey competition may have influenced the evolution of colony bees, and ants (Cole, 1981; Robinson, 1987; Bourke, 1988; organization in social insects. Robinson et al., 1989; ODonnell, 2001). Social inter- actions regulate task performance and even worker Keywords: Polistes instabilis, dominance, foraging, poly- reproduction (e.g., worker policing), but do not necessa- ethism, social organization, social evolution. rily reflect reproductive dominance (Wenseleers et al., 2004a; Wenseleers and Ratnieks, 2006). This suggests that a transition from centralized to distributed control of task performance has accompanied the evolution of larger insect colonies (Gordon, 1996; Bourke, 1999; Fewell, 2003; Ratnieks et al., 2006). Insect. Soc. Vol. 56, 2009 Research article 15 Although IF wasps have served as models for the stage where worker aggression, rather than queen study of queen control, non-egglaying workers in some aggression, is important in task allocation among workers. primitively eusocial species affect each others task Our present study tests the hypothesis that worker performance (Chandrashekara and Gadagkar, 1992; reproductive competition regulates task performance in ODonnell, 1998a,b; Jha et al., 2006). For example, some primitively social species. Previous studies on the workers initiate most of the aggressive interactions and paperwasp Polistes instabilis suggested that workers, influence foraging activity in Ropalidia marginata (Chan- rather than queens, were regulating colony-wide foraging drashekara and Gadagkar, 1992; Premnath et al., 1996) rates (ODonnell, 1998a; Jha et al., 2006). We predicted and worker-worker interactions appear to regulate for- that P. instabilis colonies would resemble self-organized aging rates in Polistes instabilis (ODonnell, 1998a). The societies, in which worker interactions regulate division of relationship between task decisions and reproductive labor. We further predicted that worker competition over competition in workers from primitively eusocial species opportunities for direct reproduction would determine may provide important information about evolutionary workers roles. We extend previous research by quantify- transitions in social organization. ing individual changes in rates of social aggression and There is often a dominance hierarchy among IF foraging behavior, and correlating these behavioral paperwasp non-reproductive workers (Mischocyttarus: changes to workers reproductive capacity. Queens Markiewicz and ODonnell, 2001; Polistes: Pardi, 1948; should not manage colony activity, specifically not Reeve, 1991; Strassmann et al., 2004; Ropalidia: Prem- engaging in significantly more dominance interactions nathACHTUNGRE et al., 1996), which correlates positively with ovarian than the workers (ODonnell, 1998a; Jha et al., 2006). In development and negatively with foraging rates (Gam- contrast to more derived societies (Robinson, 1987; boa et al., 1990; Rçseler, 1991; Markiewicz and ODon- Robinson et al., 1989; ODonnell, 2001), we expected nell, 2001). Worker competition can persist in more worker effects on task performance to be related to their advanced insect societies: worker dominance hierarchies reproductive physiology. form following queen loss in many advanced eusocial If worker competition affects task performance, we species (Wenseleers et al., 2004b). Dominant female expected the following patterns. First, increased social workers compete among each other to replace lost or aggression and increased foraging activity would be missing reproductives (Strassmann and Meyer, 1983; opposing responses to nest mate removals. The workers Hughes and Strassmann, 1988; Kardile and Gadagkar, with better chances of replacing the queen should exhibit 2003; Strassmann et al., 2004), and reproductive com- greater rates of aggressive interactions post-removal, and petition may influence many worker-worker interactions. should also forage at lower frequencies. Second, repro- In some species such as P. instabilis, the worker hierarchy ductive physiology would correspond to individuals predicts which female will become a replacement queen behavioral responses to dominant worker removal. (Hughes and Strassmann, 1988). Non-reproductive work- Workers ovary size and increased social aggression ers may increase their chances for direct reproduction by should be positively correlated (Pardi, 1948; West- inducing others to forage. Social aggression by workers, Eberhard, 1969; Rçseler et al., 1980; Strambi, 1985). even before they can reproduce, could suppress the We discuss the implications of our findings for individu- ovarian development of potential competitors and help als direct and indirect reproductive fitness in P. instabilis secure future direct fitness (Jeanne, 1991). colonies. We also develop further hypotheses for the Despite extensive research on queen removal and evolution of the relationship between social aggression replacement (Polistes: Hughes and Strassmann, 1988; and task performance. Strassmann et al., 2004; Ropalidia: Kardile and Gadag- kar, 2003), few manipulative studies have examined the effects of dominant workers on nest mate task perform- Materials and methods ance. Understanding the role of worker dominance in IF paper wasps may be especially useful in understanding Study site and subject colonies the shift in social organization from central control to distributed management of task performance (Schneider The majority of P. instabilis colonies at our site are established at the beginning of the rainy season (e.g., the middle of May; Hunt et al., et al., 1998; Schneider and Lewis, 2004; ODonnell, 2001, 1999). Data were collected from 27 June to 24 July 2005 from seven 2006). One possible evolutionary pathway from central- post-worker emergence Polistes instabilis colonies. Colony sizes ranged ized (queen) to distributed (worker) control is the from 8 to 29 adult females, with all brood stages present throughout the changing role of worker reproductive competition in study (eggs to pupae; Table 1). The nests were observed in situ near CaÇas in Guanacaste Province, Costa Rica (10826N; 85807W; affecting task performance. Interactions among non- ODonnell, 1998a). Nests were located at heights of 0.5 to 2.5 m ovipositing but reproductively capable workers may have above the ground in vegetation or on the
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