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The Challenge Hypothesis in an Insect: Juvenile Hormone Increases During Reproductive Conflict Following Queen Loss in Polistes Wasps

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The Challenge Hypothesis in an Insect: Juvenile Hormone Increases During Reproductive Conflict Following Queen Loss in Polistes Wasps vol. 176, no. 2 the american naturalist august 2010 The Challenge Hypothesis in an Insect: Juvenile Hormone Increases during Reproductive Conflict following Queen Loss in Polistes Wasps Elizabeth A. Tibbetts1,* and Zachary Y. Huang2 1. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109; 2. Department of Entomology, Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, Michigan 48824 Submitted November 10, 2009; Accepted March 31, 2010; Electronically published June 1, 2010 within wild populations (Ketterson et al. 1996; Ball and abstract: The challenge hypothesis was proposed as a mechanism Balthazart 2008). for vertebrates to optimize their testosterone titers by upregulating testosterone during periods of aggressive competition. Here we test In vertebrates, much research on the context depen- key predictions of the challenge hypothesis in an independently dence of hormonal actions has focused on social modu- evolved endocrine system: juvenile hormone (JH) in a social insect. lation of the steroid hormone testosterone (T). T is often We assess how social conflict influences JH titers in Polistes dominulus associated with benefits such as increased competitiveness, wasps. Aggressive conflict was produced by removing the queen from fertility, and mating success, but high T titers are also some colonies (experimental) and a low-ranked worker from other associated with costs such as reduced immune function colonies (control). Queen removal produced competition among and survival (Wingfield et al. 2001; Adkins-Regan 2005). workers to fill the reproductive vacancy. Workers upregulated their JH titers in response to this social conflict; worker JH titers were Individuals are hypothesized to mitigate these trade-offs higher in queenless than in queenright colonies. Furthermore, JH by upregulating T titers during times of aggressive com- titers were associated with an individual’s ability to dominate rivals; petition (Wingfield et al. 1990). This hypothesis, termed the worker that took over as the replacement queen had a substan- the challenge hypothesis, has received empirical support tially higher JH titer than did other workers. Finally, JH titers were across a range of taxa and competitive contexts. Many positively associated with aggression in queenless colonies, but there vertebrates upregulate T titers during periods of social was no relationship between JH and aggression in stable, queenright competition (Hirschenhauser and Oliveira 2006; Goy- colonies. Overall, these results match key predictions of the challenge mann et al. 2007). The variation in T titers across contexts hypothesis and parallel much of the work on testosterone in verte- brates. Social modulation of hormone titers is not confined to a means that it is difficult to understand T’s actions without particular endocrine system but is likely to be an adaptive feature studying its effects in multiple contexts. For example, the of endocrine systems across diverse taxa. strength of the relationship between T and dominance or aggression varies with the extent of social competition. Keywords: challenge hypothesis, juvenile hormone, testosterone, ag- There is typically a strong correlation between T and dom- gression, dominance, competition. inance or aggression during times of aggressive competi- tion, but there may be no relationship during periods of social stability (Wingfield et al. 1990; Adkins-Regan 2005). Introduction Although there has been extensive research on verte- Studying endocrine systems in multiple contexts is im- brate endocrine systems, much less is known about en- portant for understanding how hormones coordinate be- docrine regulation in invertebrates. Both vertebrates and invertebrates have complex social behaviors, but their en- havior and physiology as well as how selection acts on docrine systems have evolved independently. As a result, endocrine systems in the wild (Zera 2007). As a result, vertebrate and invertebrate hormones have different struc- researchers are focusing more attention on the factors that tures and work in different physiological backgrounds influence interindividual variation in hormone titers as (Nijhout 1994; Adkins-Regan 2005). Comparing the fac- well as the role of social context in endocrine variation tors that influence endocrine variation across indepen- * Author for correspondence; e-mail: [email protected]. dently evolved taxa can provide insight into the evolution Am. Nat. 2010. Vol. 176, pp. 000–000. ᭧ 2010 by The University of Chicago. of endocrine systems. Similarities in endocrine responses 0003-0147/2010/17602-51724$15.00. All rights reserved. suggest that there has been convergent evolution of en- DOI: 10.1086/653664 docrine systems and indicate that the hypotheses devel- 000 The American Naturalist oped for vertebrates reflect adaptive solutions to problems mann et al. 2004; Bocher et al. 2008). Despite extensive faced by diverse taxa. work on worker takeover in social insects, the physiological The insect hormone juvenile hormone (JH) is a key factors associated with queen replacement have not been hormone that provides a good model for studying en- addressed. docrine variation in wild invertebrates. It is a versatile JH titers were examined in wild nests of Polistes domin- hormone that influences multiple aspects of insect behav- ulus paper wasps. JH plays an important role in mediating ior and physiology including metamorphosis, diapause, dominance and aggression among Polistes queens (Ro¨seler sexual behavior, migration, parental care, and caste de- et al. 1984; Ro¨seler 1991; Tibbetts and Izzo 2009; E. A. velopment (Nijhout 1994). JH can also function as a go- Tibbetts, M. Izzo, and Z. Y. Huang, unpublished data). nadotropin and is associated with fertility (Barth et al. Among workers, nothing is known about the role of JH 1975; Robinson and Vargo 1997). In many social insects, in dominance and aggression; previous work focused on JH mediates age-related division of labor among workers the role of JH in modulating age-based division of labor (Robinson and Vargo 1997; Giray et al. 2005; Shorter and (Giray et al. 2005; Shorter and Tibbetts 2009). Polistes are Tibbetts 2009). primitively eusocial insects that lack discrete castes JH provides a particularly good comparison with work (O’Donnell 1998), so workers compete to fill the repro- on T, as JH has some effects that parallel those of T. For ductive vacancy left after queen loss (Strassmann et al. example, both JH and T are associated with life-history 2004). Here we compare the JH titers and behavior of trade-offs. In the endocrine systems of both vertebrates workers in queenright colonies with the JH titers and be- and invertebrates, high hormone titers are often associated havior of workers in colonies following queen loss. We with benefits, such as increased fertility and dominance, test whether workers upregulate JH during the period of as well as costs, such as reduced immune function (Nijhout competition following queen loss. Furthermore, we test 1994; Wingfield et al. 2001; Rantala et al. 2003; Adkins- whether JH titer is associated with the individual who takes Regan 2005; Amdam et al. 2007). Given the costs and over as the replacement queen following queen loss. Fi- benefits associated with high JH titers, insects may benefit nally, we test whether there is a stronger relationship be- by using social information to modulate their JH titers. tween JH and aggression within queenless colonies than In this study, we test three key predictions of the chal- within queenright colonies. lenge hypothesis in an insect model. The challenge hy- pothesis critically predicts that (1) individuals upregulate Methods their endocrine titers during periods of aggressive com- petition and (2) high endocrine titers are associated with Colonies used in this study were located at the University increased reproductive success in competitive contexts. of Michigan botanical garden in Ann Arbor, Michigan. The challenge hypothesis also predicts that (3) aggression Soon after nest foundation in mid-May, all nest-founding will be more strongly associated with endocrine titers dur- queens were marked with individual-specific paint marks. ing periods of heightened aggressive competition than dur- Only single-foundress nests that contained their original ing periods of low conflict (Wingfield et al. 1990; Goymann queen were used in this experiment. Workers emerged et al. 2007). Promising work has provided some support between the end of June and early July. The experiment for the challenge hypothesis in insects, as JH may increase began in mid-July 2008, when nests contained at least six during social competition (Scott 2006a; Kou et al. 2008). workers. Before the experiment, all workers on each nest However, less is known about the other predictions of the were marked with unique paint marks to allow for indi- challenge hypothesis in taxa lacking T (Scott 2006b; vidual identification. On day 1, the queen was removed Trumbo 2007). from half of the colonies (experimental) and a low-ranked We test predictions of the challenge hypothesis by as- worker was removed from the other half of the colonies sessing hormonal response during an important compet- (control). Removals were performed early in the morning, itive context within social insects: queen replacement. In when all colony members were cool and inactive, to avoid social-insect colonies there is intense competition to be- disturbing the nest. The collected queens
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