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Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality
Journal of Insect Physiology 57 (2011) 995–999
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Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys
Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality Elizabeth A. Tibbetts *, Stephanie Levy, Kellie Donajkowski Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 17 February 2011 Received in revised form 15 April 2011 Accepted 18 April 2011
Regulatory pathways in solitary species provide the raw materials for the evolution of sociality. Therefore, comparing the mechanisms that mediate reproductive plasticity in social species and their solitary ancestors can provide insight into the evolutionary origin of sociality. In many solitary insects, the effect of juvenile hormone (JH) on fertility is mediated through the fat body; individuals in good physical condition show a stronger fertility response to JH than individuals in poor physical condition. Here, we test whether a similar, condition-dependent JH response mediates fertility in workers of the primitively eusocial Polistes dominulus wasps. We test how body weight, JH, and adult nutrition influence worker ovarian development. Both JH-treatment and adult nutrition dramatically increased ovarian development. Body weight also influenced ovarian development, as large workers developed more eggs than smaller workers. Body weight and fat are strongly linked in P. dominulus workers, so these results suggest that the fat-dependent JH responsiveness common in solitary insects is conserved in social wasps. The simple, ancestral relationship between reproductive investment and physical condition may facilitate cooperation by allowing workers to adaptively allocate energy into reproduction based on their probability of successfully becoming a queen. ß 2011 Elsevier Ltd. All rights reserved.
Keywords: Sociality Vitellogennin Division of labor Caste Developmental plasticity Phenotypic plasticity Ovarian groundplan
1. Introduction The evolution of sociality has long interested biologists (Lin and Michener, 1972; Wilson, 1971). Much research has focused on the selective costs and benefits of sacrificing independent reproduction to help rear the offspring of others (Andersson, 1984; Sherman et al., 1995). Less is known about the evolutionary origin of reproductive sacrifice within social groups and the physiological mechanisms that mediate variation in reproduction among group members. It can be difficult to study the evolutionary origin of a behavior such as sociality. One valuable method is testing the mechanisms that underlie social behavior and comparing them with mechanisms found in solitary ancestors (Amdam et al., 2004; Hunt et al., 2007; West-Eberhard, 1996). Identifying the parallels between regulatory pathways present in social species and their solitary ancestors can provide insight into the origin of sociality, as the pathways present in solitary species provide the raw materials for social evolution. One hypothesis for the origin of sociality is the ‘ovarian groundplan hypothesis’, which posits that the ovarian cycle in solitary insects provides the basis for social evolution (West-
* Corresponding author. E-mail address: [email protected] (E.A. Tibbetts). 0022-1910/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2011.04.016
Eberhard, 1996; West-Eberhard, 2003). This hypothesis proposes that social and solitary insect behavior may be linked by juvenile hormone (JH) responsiveness. Specifically, reproductive plasticity in social insects may have originated via modification of the nutrition-dependent endocrine responsiveness that occurs in solitary insects (West-Eberhard, 1996). Many solitary insects show a nutrition-dependent response to juvenile hormone, JH. Fat body responds to JH by producing the yolk protein vitellogenin, so individuals in good physical condition develop more eggs in response to JH than individuals in poor physical condition (Engelmann, 1983; Nijhout, 1994; Wyatt and Davey, 1996). If the condition-dependent endocrine responsiveness that mediates reproductive plasticity in solitary species also regulates reproduction in social insects, individual condition is predicted to influence reproduction of social insect workers. However, this prediction has not been experimentally tested. Although the role of JH responsiveness in the reproductive sacrifice of workers has not been tested, previous work suggests that condition-dependent JH response may influence reproduction in nest founding queens. P. dominulus foundresses form cooperative associations where the dominant foundress is the primary reproductive. Subordinate foundresses act much like workers; they forage and typically do not reproduce (Reeve, 1991; Ro¨seler, 1991). The effect of JH on foundress fertility varies with individual condition. Large foundresses with facial patterns advertising high quality respond to JH by increasing their fertility, while small
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foundresses with facial patterns advertising low quality do not increase their fertility in response to JH (Tibbetts and Izzo, 2009). Body weight and advertised quality are associated with foundress dominance rank and reproduction (Reeve, 1991; Tibbetts and Dale, 2004), so these results indicate that the condition-dependent endocrine responsiveness of foundresses may be an adaptation that facilitates resource investment. Does a similar, conditiondependent mechanism mediate reproductive plasticity among workers? We tested whether condition-dependent hormonal response mediates reproductive plasticity among P. dominulus workers. Specifically, we tested how adult feeding, body weight, and treatment with the JH analog methoprene influence worker reproductive potential. In addition, we confirmed that weight is associated with physical condition in P. dominulus workers by measuring the relationship between body weight and fat content. 2. Methods 2.1. Study system Polistes wasps provide an interesting model for studying the evolution of sociality because there is plasticity in reproductive behavior within each caste that parallels the plasticity between castes. For example, some nest-founding Polistes paper wasp foundresses become the reproductive dominant, while others take a subordinate role and do not reproduce. Subordinate foundresses act much like workers. They care for the dominant’s offspring instead of reproducing independently (Reeve, 1991; WestEberhard, 1969). There is similar reproductive plasticity within paper wasp workers. Most workers care for the dominant’s offspring and do not reproduce. However, some workers take over their natal nest or disperse to reproduce independently (Page et al., 1989; Strassmann, 1981; Tibbetts, 2007; Tibbetts and Huang, 2010). Polistes are a primitively eusocial taxa that lacks discrete morphological castes, so the phenotypes of queens and workers overlap (O’Donnell, 1998; Tibbetts, 2006; Toth et al., 2009). As a result, defining the caste of a particular individual can be challenging. Definitions of ‘queen’ and ‘worker’ may vary across studies. For this study, we define workers as females that eclose from their nest in late June and July before the cohort of reproductive males. In temperate species, like P. dominulus, the first broods to eclose on a nest are typically non-reproductive foragers, workers. Early eclosing females can develop active ovaries and reproduce independently in the same year (O’Donnell, 1998; Solis and Strassmann, 1990) or they may enter early diapause and found nests the following year (Reeve et al., 1998; Tibbetts, 2007). As a result, they are sometimes called ‘undifferentiated females’ instead of ‘workers’. However, the vast majority of early eclosing females in temperate species become non-reproductive foragers, so we will use the term ‘worker’ for simplicity. Females that eclose later in the season are idle females in reproductive diapause (idle females or gynes) (Mead et al., 1995; O’Donnell, 1998; Solis and Strassmann, 1990). Gynes mate, overwinter, and emerge the following year as nest founding females. Different factors may influence gyne reproduction, as individuals are in reproductive diapause (Hunt, 2007; Hunt et al., 2007). Therefore, this study does not examine gynes.
a natural day/night cycle that matched the outdoors and were kept at 25 8C. Nests were checked daily for worker eclosion from pupation. Individuals used in the experiment eclosed between June 25 and July 28, 2009. At eclosion, each new worker was removed from her nest, weighed, and placed in a individual deli cup with sugar and water. Individuals were removed on the day of eclosion to reduce the effects of nest social environment on reproduction. Workers were randomly assigned to treatment groups and experimental treatment of workers started the day after pupal eclosion. Workers experienced both a hormone treatment and a diet treatment. 123 individuals from 19 nests were included in the analysis. 2.2.1. Hormone treatment Half the workers were treated with 5 mg methoprene in 1 ml acetone three times a week for two weeks. The other half the workers were treated with 1 ml acetone alone three times a week for two weeks as a control. Methoprene and acetone were topically applied to the thorax. Methoprene is a JH analog and previous studies using similar methods have shown that methoprene has behavioral and physiological effects similar to those of JH (Giray et al., 2005; O’Donnell and Jeanne, 1993; Robinson and Vargo, 1997). Further, methoprene acts in ways similar to JH at the cellular level (Ashok et al., 1998; Parthasarathy and Palli, 2009; Shemshedini and Wilson, 1990). The timing and amount of hormone treatment was chosen because it parallels previous work on reproduction in P. dominulus foundresses (Tibbetts and Izzo, 2009). 2.2.2. Diet treatment Half the workers received no caterpillars, while the other half were given B. mori caterpillars three times a week during the treatments. Most of an adult wasps’ diet is sugar, so the caterpillar treatment provided ad lib caterpillars. Workers typically ate some of each caterpillar, but did not entirely consume each caterpillar. In sum, workers received one of four treatments: caterpillars and methoprene, caterpillars and acetone control, no caterpillars and methoprene, no caterpillars and acetone control. After two weeks, individuals were sacrificed and their ovarian development was assessed. The total length of all eggs was used as the measurement of ovarian development because this measure effectively captures variability across individuals. 2.3. Fat analysis The relationship between worker weight and fat content was measured using workers that pupated in the wild. Adult workers were weighted on a scale accurate to 0.001 g three times and the average was used as the final weight. Then, abdominal fat was assessed using ether extraction, as most available fat body is in the abdomen (Arrese and Soulages, 2010). Abdomens were placed in fat free paper thimbles (Whatman), dried at 80 8C for three days, and weighed on a balance accurate to 0.0001 g. After weighing, the abdomens were extracted in diethyl ether for 24 h, washed in fresh diethyl ether, and dried for another 3 days at 80 8C. Following the second drying, abdomens were weighed again. Fat content was calculated from the difference between the dry mass and the dry fatless mass post extraction. 49 workers from 19 nests were included in this analysis.
2.2. Experimental procedures 2.4. Statistical analysis Single foundress P. dominulus nests were collected from the wild in June. The nest and foundress were transplanted into boxes in the lab and provided with water, sugar, and an ad lib diet of Bombyx mori and Galleria mellonella caterpillars. Nests experienced
Data were analyzed in SPSS v. 17. Data were analyzed using a mixed linear model. The dependent variable was ovarian development, which was log transformed prior to analysis. The
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fixed independent variables were hormone treatment, diet treatment, eclosion date, and weight at eclosion. Nest of origin was included as a random effect to account for any similarity within workers from the same nest. Non-significant interactions were removed from the final model, though the interaction data are reported below. 3. Results In general, larger workers, individuals treated with JH, and those fed caterpillars as adults developed more eggs than smaller individuals, those given no caterpillars, or individuals treated with acetone (Figs. 1 and 2). There was also a significant interaction between adult diet and weight because there was a stronger relationship between body size and ovarian development in
10
Ovarian development
JH
6
4
2
0
No Caterpillars
Caterpillars
Fig. 1. Mean (+SE) ovarian development (total egg length) in workers that experienced the following treatments: fed no caterpillars as adults and treated with acetone (black) or JH analog methoprene (grey); fed caterpillars as adults and treated with acetone (black) or JH analog methoprene (grey).
JH
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Ovarian development
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individuals fed caterpillars as adults than individuals given no caterpillars. Eclosion date had no effect on ovarian development, as predicted because these analyses are confined to workers. Worker egg development was influenced by hormone treatment (F1,106 = 78.8, p < 0.001), adult diet (F1,115 = 4.5, p = 0.037), body weight at eclosion (F1,115 = 4.4, p = 0.038), and the interaction between adult diet and weight at eclosion (F1,115= 6.8, p = 0.01). However, worker egg development was not associated with eclosion date (F1,112 = 0.43, p = 0.51), the interaction between adult diet and eclosion date (F1,107 = 2.7, p = 0.1), the interaction between hormone treatment and adult diet (F1,108 = 1.6, p = 0.20), the interaction between hormone treatment and weight (F1,99 = 0.83, p = 0.36), the interaction between hormone treatment and eclosion date (F1,97 = 1.8, p = 0.18), or the interaction between adult weight and eclosion date (F1,110 = 0.65, p = 0.42). Worker weight at eclosion was positively associated with fat content, as larger workers had more fat than smaller workers (F7.6,15.6 = 15.6, p < 0.001). 4. Discussion
Control 8
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Weight (g) Fig. 2. Relationship between ovarian development (total egg length) and weight in P. dominulus workers fed caterpillars as adults.
Ovarian development varied with worker weight, with larger workers having more developed eggs than smaller workers (Fig. 2). Worker weight is positively associated with fat body, so these results suggest that endocrine responsiveness in paper wasp workers may be mediated through the fat body. The fat-dependent endocrine responsiveness in paper wasps parallels previous work in solitary taxa (Engelmann, 1983; Nijhout, 1994; Wyatt and Davey, 1996) and suggests that reproductive plasticity in social wasps may have originated via the fat-dependent endocrine responsiveness present in a solitary ancestor (West-Eberhard, 1996). These results support the ovarian groundplan hypothesis for the origin of sociality and add to a growing body of research that uses the mechanisms underlying social insect behavior to understand the origin of sociality (Amdam et al., 2004; Hunt et al., 2007; Toth et al., 2007; West-Eberhard, 1996). One challenge of using the phenotype of solitary ancestors as a window into the evolutionary origin of sociality is that there is little agreement about the evolutionary history of social behavior. In particular, there are questions about number of times that sociality originated in wasps and which solitary groups are most closely related to social species (Hines et al., 2007; Pickett and Carpenter, 2010). Fortunately, interpretation of this study does not depend on precise evolutionary relationships. Solitary insects commonly show a condition-dependent ovarian response to JH (Engelmann, 1983; Nijhout, 1994; Wyatt and Davey, 1996). Our results indicate that this mechanism is evolutionarily conserved in the social Polistes and this ancestral mechanism may provide a simple method to optimize resource allocation in social species. Nevertheless, future work confirming phylogenetic relationships in the Vespidae, as well as additional information about the behavior of closely related solitary species would be quite important to understand the origin of sociality. Worker fertility was strongly influenced by access to supplemental caterpillars during adulthood. Adult workers fed sugar alone has less developed ovaries than adult workers fed supplemental caterpillars. Fat and protein are important components of egg development, so it isn’t surprising that adult nutrition had such a strong effect on ovarian development (Wheeler, 1996). However, good adult nutrition alone wasn’t sufficient to induce ovarian development, as body weight and hormone treatment also influenced worker fertility. The role of adult nutrition in reproduction could be a mechanism that allows workers to incorporate social information into their reproductive decisions. Many of the social factors thought to influence worker reproduction are associated with
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adult nutrition. For example, workers on nests without brood exhibit more reproductive-like characteristics than workers on nests with brood (Mead et al., 1995; Solis and Strassmann, 1990). Further, some workers that engage in energetically expensive foraging behavior may be less likely to become reproductive than non-foragers (O’Donnell, 1996; Strassmann and Meyer, 1983; West-Eberhard, 1969). Therefore, nutritionally taxing tasks like foraging and brood care may reduce adult nutritional condition (O’Donnell and Jeanne, 1995), thereby inhibiting worker reproduction. In contrast, workers that do not participate in demanding nest work remain in good condition and have reproductive-like physiological responses. Previous studies have indicated that adult nutrition influences worker reproductive potential (Gadagkar et al., 1988; Hunt, 2006; Hunt, 2007). The results of this study provide direct, experimental evidence that adult nutrition mediates worker reproduction. There has been longstanding interest in the factors that influence caste in primitively eusocial taxa. Some studies suggest that adult social context is the primary factor influencing caste, while others suggest that caste is mediated by developmental environment such that individuals are strongly caste biased prior to eclosion. Alternatively, both social environment and early development may play a role in general reproductive strategy (reviewed in O’Donnell, 1998). The results of this study suggest that both factors are important. Adult nutrition influences reproduction, indicating that caste is not completely determined by early development. However, early environment is important, as it influences the reproductive strategy that individuals pursue. Well-fed larvae develop into large, high quality adults (Gadagkar et al., 1991; Hunt, 1991; Hunt, 2007; Karsai and Hunt, 2002; Tibbetts, 2010) and these individuals are more likely to invest in reproduction than small, low quality adults (Tibbetts and Izzo, 2009). As Polistes are a primitively eusocial group, the relationship between condition and reproductive investment is probabilistic rather than deterministic. Early development influences the costs and benefits of different strategies, thereby influencing individual reproductive strategies. In addition, adult nutrition plays an important role in initiating worker reproduction after eclosion. The condition-dependent effect of JH on ovarian development parallels previous work in nest-founding queens (Tibbetts and Izzo, 2009), suggesting that the same, simple mechanism mediates cooperation and reproductive plasticity across castes. Workers and foundresses appear to lie along a continuum. In both, large individuals show increased ovarian development when treated with JH, while small individuals do not. Workers are typically smaller than foundresses and have lower reproductive potential (Judd et al., 2010; Toth et al., 2009), but our results suggest that there is no qualitative difference in worker reproductive potential. The relationship between worker size and reproduction suggests that the queen could manipulate the reproductive strategies of her offspring to encourage worker behavior. The queen controls worker nutrition, so she may also control adult body size and reproductive strategies (West-Eberhard, 1969). Future work exploring the factors that influence worker size will be useful to address this hypothesis in more detail. The condition-dependent fertility of paper wasps helps clarify how JH can have multifaceted effects within social insects. JH is a well-known gonadotropin that increases fertility in many social and non-social insects (Nijhout, 1994). In addition, JH increases foraging behavior among some social insects, including Polistes workers (Giray et al., 2005; O’Donnell and Jeanne, 1993; Shorter and Tibbetts, 2009). Reproduction and foraging are often thought to be on opposite ends of the behavioral spectrum, so how can the same hormone mediate such different behaviors? Queens are typically larger and in better physical condition than workers, so one hypothesis is that response to JH is mediated through
individual condition. The ‘split function hypothesis’ proposes that JH promotes reproductive maturation, with its specific effect varying with individual condition. When individuals are in good physical condition, JH promotes egg production and aggressive behaviors. When individuals are in poor physical condition, JH promotes maturation from oviposition associated activities like cell construction to foraging aspects of maternal behavior (Giray et al., 2005; West-Eberhard, 1996). Our results are consistent with this hypothesis, as JH responsiveness is influenced by individual condition. Although our results are consistent with the split function hypothesis, additional research will be important to test this hypothesis in additional social contexts. For this study, we removed workers from their nest immediately after eclosion to standardize social environment. In the wild, reproductive plasticity is influenced by social factors including the presence of the queen and the behavior of other workers. Workers may not become fertile on a queenright nest, regardless of their size or hormone level. Therefore, physical condition is likely to be one important factor among multiple factors that influences worker reproductive plasticity. Overall, reproductive plasticity in paper wasp workers is influenced by JH, adult nutrition, and body size. Our results suggest that workers may use variation in endocrine response to optimize resource allocation such that only large individuals that are able to successfully dominate rivals invest in reproduction. Fatdependent JH responsiveness is common among non-social insects, so these results suggest that the reproductive plasticity involved in social cooperation may be an evolutionarily conserved mechanism. Acknowledgements Thanks to H. Hoffmann and C. Wangen for research assistance. M.J. West-Eberhard and J. Hunt provided helpful feedback on an earlier version of this manuscript. References Amdam, G.V., Norberg, K., Fondrk, M.K., Page, R.E., 2004. Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. In: Proc. Natl. Acad. Sci. U.S.A.101, pp. 11350–11355. Andersson, M., 1984. The evolution of eusociality. Ann. Rev. Ecol. Syst. 15, 165–189. Arrese, E.L., Soulages, J.L., 2010. Insect fat body: energy, metabolism, and regulation. Ann. Rev. Entomol. 55, 207–225. Ashok, M., Turner, C., Wilson, T.G., 1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. In: Proc. Natl. Acad. Sci. U.S.A.95, pp. 2761–2766. Engelmann, F., 1983. Vitellogenesis controlled by juvenile hormone. In: Downer, R.G.H., Laufer, H. (Eds.), Endocrinology of Insects. Alan Liss, New York, pp. 259– 270. Gadagkar, R., Bhagavan, S., Chandrashekara, K., Vinutha, C., 1991. The role of larval nutrition in preimaginal biasing of caste in the primitively eusocial wasp Ropalidia marginata (Hymenoptera, Vespidae). Ecol. Entomol. 16, 435–440. Gadagkar, R., Vinutha, C., Shanubhogue, A., Gore, A.P., 1988. Pre-imaginal biasing of caste in a primitively eusocial insect. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 233, 175–189. Giray, T., Giovanetti, M., West-Eberhard, M.J., 2005. Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. In: Proc. Natl. Acad. Sci. U.S.A.102, pp. 3330–3335. Hines, H.M., Hunt, J.H., O’Connor, T.K., Gillespie, J.J., Cameron, S.A., 2007. Multigene phylogeny reveals eusociality evolved twice in vespid wasps. In: Proc. Natl. Acad. Sci. U.S.A.104, pp. 3295–3299. Hunt, J.H., 1991. Nourishment and the evolution of the social Vespidae. In: Ross, K.G., Matthews, R.W. (Eds.), The Social Biology of Wasps. Cornell University Press, Ithaca, NY, pp. 426–450. Hunt, J.H., 2006. Evolution of castes in Polistes. Annales Zoologici Fennici 43, 407– 422. Hunt, J.H., 2007. The Evolution of Social Wasps. Oxford University Press, New York. Hunt, J.H., Kensinger, B.J., Kossuth, J.A., Henshaw, M.T., Norberg, K., Wolschin, F., Amdam, G.V., 2007. A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies. In: Proc. Natl. Acad. Sci. U.S.A.104, pp. 14020–14025.
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Reproductive plasticity in Polistes paper wasp workers and the evolutionary origins of sociality Elizabeth A. Tibbetts *, Stephanie Levy, Kellie Donajkowski Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 17 February 2011 Received in revised form 15 April 2011 Accepted 18 April 2011
Regulatory pathways in solitary species provide the raw materials for the evolution of sociality. Therefore, comparing the mechanisms that mediate reproductive plasticity in social species and their solitary ancestors can provide insight into the evolutionary origin of sociality. In many solitary insects, the effect of juvenile hormone (JH) on fertility is mediated through the fat body; individuals in good physical condition show a stronger fertility response to JH than individuals in poor physical condition. Here, we test whether a similar, condition-dependent JH response mediates fertility in workers of the primitively eusocial Polistes dominulus wasps. We test how body weight, JH, and adult nutrition influence worker ovarian development. Both JH-treatment and adult nutrition dramatically increased ovarian development. Body weight also influenced ovarian development, as large workers developed more eggs than smaller workers. Body weight and fat are strongly linked in P. dominulus workers, so these results suggest that the fat-dependent JH responsiveness common in solitary insects is conserved in social wasps. The simple, ancestral relationship between reproductive investment and physical condition may facilitate cooperation by allowing workers to adaptively allocate energy into reproduction based on their probability of successfully becoming a queen. ß 2011 Elsevier Ltd. All rights reserved.
Keywords: Sociality Vitellogennin Division of labor Caste Developmental plasticity Phenotypic plasticity Ovarian groundplan
1. Introduction The evolution of sociality has long interested biologists (Lin and Michener, 1972; Wilson, 1971). Much research has focused on the selective costs and benefits of sacrificing independent reproduction to help rear the offspring of others (Andersson, 1984; Sherman et al., 1995). Less is known about the evolutionary origin of reproductive sacrifice within social groups and the physiological mechanisms that mediate variation in reproduction among group members. It can be difficult to study the evolutionary origin of a behavior such as sociality. One valuable method is testing the mechanisms that underlie social behavior and comparing them with mechanisms found in solitary ancestors (Amdam et al., 2004; Hunt et al., 2007; West-Eberhard, 1996). Identifying the parallels between regulatory pathways present in social species and their solitary ancestors can provide insight into the origin of sociality, as the pathways present in solitary species provide the raw materials for social evolution. One hypothesis for the origin of sociality is the ‘ovarian groundplan hypothesis’, which posits that the ovarian cycle in solitary insects provides the basis for social evolution (West-
* Corresponding author. E-mail address: [email protected] (E.A. Tibbetts). 0022-1910/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jinsphys.2011.04.016
Eberhard, 1996; West-Eberhard, 2003). This hypothesis proposes that social and solitary insect behavior may be linked by juvenile hormone (JH) responsiveness. Specifically, reproductive plasticity in social insects may have originated via modification of the nutrition-dependent endocrine responsiveness that occurs in solitary insects (West-Eberhard, 1996). Many solitary insects show a nutrition-dependent response to juvenile hormone, JH. Fat body responds to JH by producing the yolk protein vitellogenin, so individuals in good physical condition develop more eggs in response to JH than individuals in poor physical condition (Engelmann, 1983; Nijhout, 1994; Wyatt and Davey, 1996). If the condition-dependent endocrine responsiveness that mediates reproductive plasticity in solitary species also regulates reproduction in social insects, individual condition is predicted to influence reproduction of social insect workers. However, this prediction has not been experimentally tested. Although the role of JH responsiveness in the reproductive sacrifice of workers has not been tested, previous work suggests that condition-dependent JH response may influence reproduction in nest founding queens. P. dominulus foundresses form cooperative associations where the dominant foundress is the primary reproductive. Subordinate foundresses act much like workers; they forage and typically do not reproduce (Reeve, 1991; Ro¨seler, 1991). The effect of JH on foundress fertility varies with individual condition. Large foundresses with facial patterns advertising high quality respond to JH by increasing their fertility, while small
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foundresses with facial patterns advertising low quality do not increase their fertility in response to JH (Tibbetts and Izzo, 2009). Body weight and advertised quality are associated with foundress dominance rank and reproduction (Reeve, 1991; Tibbetts and Dale, 2004), so these results indicate that the condition-dependent endocrine responsiveness of foundresses may be an adaptation that facilitates resource investment. Does a similar, conditiondependent mechanism mediate reproductive plasticity among workers? We tested whether condition-dependent hormonal response mediates reproductive plasticity among P. dominulus workers. Specifically, we tested how adult feeding, body weight, and treatment with the JH analog methoprene influence worker reproductive potential. In addition, we confirmed that weight is associated with physical condition in P. dominulus workers by measuring the relationship between body weight and fat content. 2. Methods 2.1. Study system Polistes wasps provide an interesting model for studying the evolution of sociality because there is plasticity in reproductive behavior within each caste that parallels the plasticity between castes. For example, some nest-founding Polistes paper wasp foundresses become the reproductive dominant, while others take a subordinate role and do not reproduce. Subordinate foundresses act much like workers. They care for the dominant’s offspring instead of reproducing independently (Reeve, 1991; WestEberhard, 1969). There is similar reproductive plasticity within paper wasp workers. Most workers care for the dominant’s offspring and do not reproduce. However, some workers take over their natal nest or disperse to reproduce independently (Page et al., 1989; Strassmann, 1981; Tibbetts, 2007; Tibbetts and Huang, 2010). Polistes are a primitively eusocial taxa that lacks discrete morphological castes, so the phenotypes of queens and workers overlap (O’Donnell, 1998; Tibbetts, 2006; Toth et al., 2009). As a result, defining the caste of a particular individual can be challenging. Definitions of ‘queen’ and ‘worker’ may vary across studies. For this study, we define workers as females that eclose from their nest in late June and July before the cohort of reproductive males. In temperate species, like P. dominulus, the first broods to eclose on a nest are typically non-reproductive foragers, workers. Early eclosing females can develop active ovaries and reproduce independently in the same year (O’Donnell, 1998; Solis and Strassmann, 1990) or they may enter early diapause and found nests the following year (Reeve et al., 1998; Tibbetts, 2007). As a result, they are sometimes called ‘undifferentiated females’ instead of ‘workers’. However, the vast majority of early eclosing females in temperate species become non-reproductive foragers, so we will use the term ‘worker’ for simplicity. Females that eclose later in the season are idle females in reproductive diapause (idle females or gynes) (Mead et al., 1995; O’Donnell, 1998; Solis and Strassmann, 1990). Gynes mate, overwinter, and emerge the following year as nest founding females. Different factors may influence gyne reproduction, as individuals are in reproductive diapause (Hunt, 2007; Hunt et al., 2007). Therefore, this study does not examine gynes.
a natural day/night cycle that matched the outdoors and were kept at 25 8C. Nests were checked daily for worker eclosion from pupation. Individuals used in the experiment eclosed between June 25 and July 28, 2009. At eclosion, each new worker was removed from her nest, weighed, and placed in a individual deli cup with sugar and water. Individuals were removed on the day of eclosion to reduce the effects of nest social environment on reproduction. Workers were randomly assigned to treatment groups and experimental treatment of workers started the day after pupal eclosion. Workers experienced both a hormone treatment and a diet treatment. 123 individuals from 19 nests were included in the analysis. 2.2.1. Hormone treatment Half the workers were treated with 5 mg methoprene in 1 ml acetone three times a week for two weeks. The other half the workers were treated with 1 ml acetone alone three times a week for two weeks as a control. Methoprene and acetone were topically applied to the thorax. Methoprene is a JH analog and previous studies using similar methods have shown that methoprene has behavioral and physiological effects similar to those of JH (Giray et al., 2005; O’Donnell and Jeanne, 1993; Robinson and Vargo, 1997). Further, methoprene acts in ways similar to JH at the cellular level (Ashok et al., 1998; Parthasarathy and Palli, 2009; Shemshedini and Wilson, 1990). The timing and amount of hormone treatment was chosen because it parallels previous work on reproduction in P. dominulus foundresses (Tibbetts and Izzo, 2009). 2.2.2. Diet treatment Half the workers received no caterpillars, while the other half were given B. mori caterpillars three times a week during the treatments. Most of an adult wasps’ diet is sugar, so the caterpillar treatment provided ad lib caterpillars. Workers typically ate some of each caterpillar, but did not entirely consume each caterpillar. In sum, workers received one of four treatments: caterpillars and methoprene, caterpillars and acetone control, no caterpillars and methoprene, no caterpillars and acetone control. After two weeks, individuals were sacrificed and their ovarian development was assessed. The total length of all eggs was used as the measurement of ovarian development because this measure effectively captures variability across individuals. 2.3. Fat analysis The relationship between worker weight and fat content was measured using workers that pupated in the wild. Adult workers were weighted on a scale accurate to 0.001 g three times and the average was used as the final weight. Then, abdominal fat was assessed using ether extraction, as most available fat body is in the abdomen (Arrese and Soulages, 2010). Abdomens were placed in fat free paper thimbles (Whatman), dried at 80 8C for three days, and weighed on a balance accurate to 0.0001 g. After weighing, the abdomens were extracted in diethyl ether for 24 h, washed in fresh diethyl ether, and dried for another 3 days at 80 8C. Following the second drying, abdomens were weighed again. Fat content was calculated from the difference between the dry mass and the dry fatless mass post extraction. 49 workers from 19 nests were included in this analysis.
2.2. Experimental procedures 2.4. Statistical analysis Single foundress P. dominulus nests were collected from the wild in June. The nest and foundress were transplanted into boxes in the lab and provided with water, sugar, and an ad lib diet of Bombyx mori and Galleria mellonella caterpillars. Nests experienced
Data were analyzed in SPSS v. 17. Data were analyzed using a mixed linear model. The dependent variable was ovarian development, which was log transformed prior to analysis. The
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fixed independent variables were hormone treatment, diet treatment, eclosion date, and weight at eclosion. Nest of origin was included as a random effect to account for any similarity within workers from the same nest. Non-significant interactions were removed from the final model, though the interaction data are reported below. 3. Results In general, larger workers, individuals treated with JH, and those fed caterpillars as adults developed more eggs than smaller individuals, those given no caterpillars, or individuals treated with acetone (Figs. 1 and 2). There was also a significant interaction between adult diet and weight because there was a stronger relationship between body size and ovarian development in
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Fig. 1. Mean (+SE) ovarian development (total egg length) in workers that experienced the following treatments: fed no caterpillars as adults and treated with acetone (black) or JH analog methoprene (grey); fed caterpillars as adults and treated with acetone (black) or JH analog methoprene (grey).
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individuals fed caterpillars as adults than individuals given no caterpillars. Eclosion date had no effect on ovarian development, as predicted because these analyses are confined to workers. Worker egg development was influenced by hormone treatment (F1,106 = 78.8, p < 0.001), adult diet (F1,115 = 4.5, p = 0.037), body weight at eclosion (F1,115 = 4.4, p = 0.038), and the interaction between adult diet and weight at eclosion (F1,115= 6.8, p = 0.01). However, worker egg development was not associated with eclosion date (F1,112 = 0.43, p = 0.51), the interaction between adult diet and eclosion date (F1,107 = 2.7, p = 0.1), the interaction between hormone treatment and adult diet (F1,108 = 1.6, p = 0.20), the interaction between hormone treatment and weight (F1,99 = 0.83, p = 0.36), the interaction between hormone treatment and eclosion date (F1,97 = 1.8, p = 0.18), or the interaction between adult weight and eclosion date (F1,110 = 0.65, p = 0.42). Worker weight at eclosion was positively associated with fat content, as larger workers had more fat than smaller workers (F7.6,15.6 = 15.6, p < 0.001). 4. Discussion
Control 8
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Weight (g) Fig. 2. Relationship between ovarian development (total egg length) and weight in P. dominulus workers fed caterpillars as adults.
Ovarian development varied with worker weight, with larger workers having more developed eggs than smaller workers (Fig. 2). Worker weight is positively associated with fat body, so these results suggest that endocrine responsiveness in paper wasp workers may be mediated through the fat body. The fat-dependent endocrine responsiveness in paper wasps parallels previous work in solitary taxa (Engelmann, 1983; Nijhout, 1994; Wyatt and Davey, 1996) and suggests that reproductive plasticity in social wasps may have originated via the fat-dependent endocrine responsiveness present in a solitary ancestor (West-Eberhard, 1996). These results support the ovarian groundplan hypothesis for the origin of sociality and add to a growing body of research that uses the mechanisms underlying social insect behavior to understand the origin of sociality (Amdam et al., 2004; Hunt et al., 2007; Toth et al., 2007; West-Eberhard, 1996). One challenge of using the phenotype of solitary ancestors as a window into the evolutionary origin of sociality is that there is little agreement about the evolutionary history of social behavior. In particular, there are questions about number of times that sociality originated in wasps and which solitary groups are most closely related to social species (Hines et al., 2007; Pickett and Carpenter, 2010). Fortunately, interpretation of this study does not depend on precise evolutionary relationships. Solitary insects commonly show a condition-dependent ovarian response to JH (Engelmann, 1983; Nijhout, 1994; Wyatt and Davey, 1996). Our results indicate that this mechanism is evolutionarily conserved in the social Polistes and this ancestral mechanism may provide a simple method to optimize resource allocation in social species. Nevertheless, future work confirming phylogenetic relationships in the Vespidae, as well as additional information about the behavior of closely related solitary species would be quite important to understand the origin of sociality. Worker fertility was strongly influenced by access to supplemental caterpillars during adulthood. Adult workers fed sugar alone has less developed ovaries than adult workers fed supplemental caterpillars. Fat and protein are important components of egg development, so it isn’t surprising that adult nutrition had such a strong effect on ovarian development (Wheeler, 1996). However, good adult nutrition alone wasn’t sufficient to induce ovarian development, as body weight and hormone treatment also influenced worker fertility. The role of adult nutrition in reproduction could be a mechanism that allows workers to incorporate social information into their reproductive decisions. Many of the social factors thought to influence worker reproduction are associated with
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adult nutrition. For example, workers on nests without brood exhibit more reproductive-like characteristics than workers on nests with brood (Mead et al., 1995; Solis and Strassmann, 1990). Further, some workers that engage in energetically expensive foraging behavior may be less likely to become reproductive than non-foragers (O’Donnell, 1996; Strassmann and Meyer, 1983; West-Eberhard, 1969). Therefore, nutritionally taxing tasks like foraging and brood care may reduce adult nutritional condition (O’Donnell and Jeanne, 1995), thereby inhibiting worker reproduction. In contrast, workers that do not participate in demanding nest work remain in good condition and have reproductive-like physiological responses. Previous studies have indicated that adult nutrition influences worker reproductive potential (Gadagkar et al., 1988; Hunt, 2006; Hunt, 2007). The results of this study provide direct, experimental evidence that adult nutrition mediates worker reproduction. There has been longstanding interest in the factors that influence caste in primitively eusocial taxa. Some studies suggest that adult social context is the primary factor influencing caste, while others suggest that caste is mediated by developmental environment such that individuals are strongly caste biased prior to eclosion. Alternatively, both social environment and early development may play a role in general reproductive strategy (reviewed in O’Donnell, 1998). The results of this study suggest that both factors are important. Adult nutrition influences reproduction, indicating that caste is not completely determined by early development. However, early environment is important, as it influences the reproductive strategy that individuals pursue. Well-fed larvae develop into large, high quality adults (Gadagkar et al., 1991; Hunt, 1991; Hunt, 2007; Karsai and Hunt, 2002; Tibbetts, 2010) and these individuals are more likely to invest in reproduction than small, low quality adults (Tibbetts and Izzo, 2009). As Polistes are a primitively eusocial group, the relationship between condition and reproductive investment is probabilistic rather than deterministic. Early development influences the costs and benefits of different strategies, thereby influencing individual reproductive strategies. In addition, adult nutrition plays an important role in initiating worker reproduction after eclosion. The condition-dependent effect of JH on ovarian development parallels previous work in nest-founding queens (Tibbetts and Izzo, 2009), suggesting that the same, simple mechanism mediates cooperation and reproductive plasticity across castes. Workers and foundresses appear to lie along a continuum. In both, large individuals show increased ovarian development when treated with JH, while small individuals do not. Workers are typically smaller than foundresses and have lower reproductive potential (Judd et al., 2010; Toth et al., 2009), but our results suggest that there is no qualitative difference in worker reproductive potential. The relationship between worker size and reproduction suggests that the queen could manipulate the reproductive strategies of her offspring to encourage worker behavior. The queen controls worker nutrition, so she may also control adult body size and reproductive strategies (West-Eberhard, 1969). Future work exploring the factors that influence worker size will be useful to address this hypothesis in more detail. The condition-dependent fertility of paper wasps helps clarify how JH can have multifaceted effects within social insects. JH is a well-known gonadotropin that increases fertility in many social and non-social insects (Nijhout, 1994). In addition, JH increases foraging behavior among some social insects, including Polistes workers (Giray et al., 2005; O’Donnell and Jeanne, 1993; Shorter and Tibbetts, 2009). Reproduction and foraging are often thought to be on opposite ends of the behavioral spectrum, so how can the same hormone mediate such different behaviors? Queens are typically larger and in better physical condition than workers, so one hypothesis is that response to JH is mediated through
individual condition. The ‘split function hypothesis’ proposes that JH promotes reproductive maturation, with its specific effect varying with individual condition. When individuals are in good physical condition, JH promotes egg production and aggressive behaviors. When individuals are in poor physical condition, JH promotes maturation from oviposition associated activities like cell construction to foraging aspects of maternal behavior (Giray et al., 2005; West-Eberhard, 1996). Our results are consistent with this hypothesis, as JH responsiveness is influenced by individual condition. Although our results are consistent with the split function hypothesis, additional research will be important to test this hypothesis in additional social contexts. For this study, we removed workers from their nest immediately after eclosion to standardize social environment. In the wild, reproductive plasticity is influenced by social factors including the presence of the queen and the behavior of other workers. Workers may not become fertile on a queenright nest, regardless of their size or hormone level. Therefore, physical condition is likely to be one important factor among multiple factors that influences worker reproductive plasticity. Overall, reproductive plasticity in paper wasp workers is influenced by JH, adult nutrition, and body size. Our results suggest that workers may use variation in endocrine response to optimize resource allocation such that only large individuals that are able to successfully dominate rivals invest in reproduction. Fatdependent JH responsiveness is common among non-social insects, so these results suggest that the reproductive plasticity involved in social cooperation may be an evolutionarily conserved mechanism. Acknowledgements Thanks to H. Hoffmann and C. Wangen for research assistance. M.J. West-Eberhard and J. Hunt provided helpful feedback on an earlier version of this manuscript. References Amdam, G.V., Norberg, K., Fondrk, M.K., Page, R.E., 2004. Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. In: Proc. Natl. Acad. Sci. U.S.A.101, pp. 11350–11355. Andersson, M., 1984. The evolution of eusociality. Ann. Rev. Ecol. Syst. 15, 165–189. Arrese, E.L., Soulages, J.L., 2010. Insect fat body: energy, metabolism, and regulation. Ann. Rev. Entomol. 55, 207–225. Ashok, M., Turner, C., Wilson, T.G., 1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. In: Proc. Natl. Acad. Sci. U.S.A.95, pp. 2761–2766. Engelmann, F., 1983. Vitellogenesis controlled by juvenile hormone. In: Downer, R.G.H., Laufer, H. (Eds.), Endocrinology of Insects. Alan Liss, New York, pp. 259– 270. Gadagkar, R., Bhagavan, S., Chandrashekara, K., Vinutha, C., 1991. The role of larval nutrition in preimaginal biasing of caste in the primitively eusocial wasp Ropalidia marginata (Hymenoptera, Vespidae). Ecol. Entomol. 16, 435–440. Gadagkar, R., Vinutha, C., Shanubhogue, A., Gore, A.P., 1988. Pre-imaginal biasing of caste in a primitively eusocial insect. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 233, 175–189. Giray, T., Giovanetti, M., West-Eberhard, M.J., 2005. Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. In: Proc. Natl. Acad. Sci. U.S.A.102, pp. 3330–3335. Hines, H.M., Hunt, J.H., O’Connor, T.K., Gillespie, J.J., Cameron, S.A., 2007. Multigene phylogeny reveals eusociality evolved twice in vespid wasps. In: Proc. Natl. Acad. Sci. U.S.A.104, pp. 3295–3299. Hunt, J.H., 1991. Nourishment and the evolution of the social Vespidae. In: Ross, K.G., Matthews, R.W. (Eds.), The Social Biology of Wasps. Cornell University Press, Ithaca, NY, pp. 426–450. Hunt, J.H., 2006. Evolution of castes in Polistes. Annales Zoologici Fennici 43, 407– 422. Hunt, J.H., 2007. The Evolution of Social Wasps. Oxford University Press, New York. Hunt, J.H., Kensinger, B.J., Kossuth, J.A., Henshaw, M.T., Norberg, K., Wolschin, F., Amdam, G.V., 2007. A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies. In: Proc. Natl. Acad. Sci. U.S.A.104, pp. 14020–14025.
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