Behav Ecol Sociobiol (2007) 61:1877–1883 DOI 10.1007/s00265-007-0427-x

ORIGINAL PAPER

Dispersal decisions and predispersal behavior in Polistes paper ‘workers’

Elizabeth A. Tibbetts

Received: 5 December 2006 /Revised: 4 May 2007 /Accepted: 7 May 2007 /Published online: 26 May 2007 # Springer-Verlag 2007

Abstract Social insects are popular models for studying internal state and nest environment to optimize their the evolution of cooperation. Casteless taxa where individ- behavioral strategies. uals have the flexibility to either nest alone or cooperate are particularly valuable for understanding the causes and Keywords Cooperation . Relatedness . Ecological consequences of cooperative behavior. For example, some constraints . Cooperative breeding . Caste . Plasticity ‘workers’ from Polistes paper wasp nests disappear from their natal colony soon after pupal emergence and nest independently. However, little is known about dispersal Introduction behavior. In this paper, I compare predispersal behavior of who leave their natal colony soon after emergence Social insect colonies appear to be paradigms of coopera- with behavior of individuals who remain on the natal tion, as many individuals forgo independent reproduction to colony as true workers. I found that P. dominulus females help rear the offspring of others. Consequently, social with short nest tenure behave much like gynes (reproduc- insects have provided an important model for understand- tive-destined offspring produced at the end of the season), ing the evolution of cooperative behavior. Even within the as wasps with short nest tenure are behaviorally selfish most cooperative social groups, the reproductive interests while on the natal colony. They spend a smaller proportion of group members are not completely aligned. Group of their time foraging and a larger proportion of their time members can sometimes attain higher inclusive fitness by resting than workers with long nest tenure. In addition, I rearing their own offspring instead of cooperating (Hamilton assessed the factors that may favor early dispersal. Nest 1964a, b; Ratnieks et al. 2006). As a result, individuals may environment strongly influenced dispersal; large colonies try to maximize their fitness by dispersing to nest had a smaller proportion of females with short nest tenure. independently instead of remaining on the natal colony. Queen turnover also increased dispersal behavior perhaps Species with the flexibility to cooperate versus nest because queen turnover reduces relatedness between a independently provide some of the best models for colony’s current and future offspring, thereby reducing the understanding the circumstances that favor cooperation. kin-selected benefits of cooperation. Therefore, casteless In general, the overall benefits of cooperating versus social insects exhibit a surprising degree of reproductive independent breeding influence reproductive strategies flexibility. Individuals may use information about their (Emlen 1991; Koenig et al. 1992; Choe and Crespi 1997). Kin-selected benefits of remaining with the natal colony play an important role. Individuals are often less likely to Communicated by K. Ross help unrelated individuals (Griffin and West 2003), so they E. A. Tibbetts (*) may disperse when changes in group membership reduce Department of Ecology and Evolutionary Biology, their relatedness to subsequent offspring (Klahn 1988; University of Michigan, Emlen 1995; Strassmann 1996 but see Keller 1997). 830 N. University, Ann Arbor, MI 48109-1048, USA Individuals may also use information about their internal e-mail: [email protected] state to optimize cooperative decisions, although little real 1878 Behav Ecol Sociobiol (2007) 61:1877–1883 research has explicitly tested this possibility. Individuals natal colony within a few days of pupal emergence are differ in overall phenotypic and genetic constitution (i.e., pursuing independent reproduction (Reeve et al. 1998; quality), with some individuals having higher survival, Starks 2001). Therefore, I compared the behavior of fertility, and dominance status than other individuals Polistes dominulus females with short versus long nest (Sheldon 1994; Jennions et al. 2001; Hunt et al. 2004; tenure. If the majority of short tenure females are leaving Tibbetts and Dale 2004). Variation in these factors may their natal colony to pursue independent reproduction, I influence the relative costs and benefits of dispersing versus predicted that short tenure females will invest less in nesting independently as well as individuals’ reproductive helping behavior while on their natal colony. In particular, decisions (Komdeur 2006). short tenure females are expected to spend less time In social insects, the decision to nest alone versus remain foraging than long tenure females. Alternatively, if short with the natal group is often considered from the tenure females do not behave more selfishly than long perspective of constraints on independent reproduction. tenure females, many of the short tenure females could Some social insects are infertile and cannot nest alone merely be dying. (Wheeler 1986). Other individuals are fertile, but their This study also assessed the nest and individual reproductive options may be limited by ecological factors characters associated with tenure length. Specifically, I (Emlen 1991; Koenig et al. 1992; Nonacs and Reeve 1995). examined the relationship between tenure and queen For example, the first brood of offspring in annual social turnover, nest size, and individual quality. If short nest insect colonies is often considered nonreproductive workers tenure is part of an early dispersal strategy, I predicted that who forgo reproduction to help rear future generations of tenure length will be influenced by the relative benefits of reproductive females (gynes) and males (Wilson 1971). cooperating versus dispersing. Although constraints play an important role in the reproductive behavior of social insects, species that lack clear morphological castes may have surprising levels of reproductive flexibility. For example, some of the first Materials and methods emerging (‘worker’) offspring on Polistes wasp nests leave their natal colony and immediately found new nests or Behavior before dispersal usurp previously established nests (Strassmann 1981; Page et al. 1989; Queller et al. 1997; Hagiwara and Kojima Research was conducted on queen-right Polistes dominulus 2002). Some ‘worker’ Halictid and Polistes wasps colonies in rural and semirural areas surrounding Ithaca, leave their natal colony to enter early diapause and found NY. Although P. dominulus are native to Europe, they have nests the following year (Yanega 1989; Reeve et al. 1998). been studied extensively in Europe and North America and There has been less detailed field observation of individual their genetic diversity and behavior appear similar in both behavior in other primitively eusocial taxa, although first- locations (Pardi 1948; Mead et al. 1995; Cervo et al. 2000; brood offspring in Ropalidia, Belonogaster, and Stenogas- Tibbetts and Reeve 2000; Cant and Field 2001; Johnson trine wasps are also thought to be capable of independent and Starks 2004). Nests were videotaped for behavioral reproduction (Gadagkar 1991; Turillazzi 1991). analysis during late June and early July 2004. The goal was Examples of reproductive flexibility are widespread, but to compare the behavior of a pair of early females from questions about dispersal behavior remain. For example, are each colony. The pairs consisted of individually marked dispersal decisions influenced by the relative costs and females from the same nest who were approximately the benefits of remaining with the natal colony versus same age. One female had a short nest tenure (<8 days) and dispersing? Are individuals who leave the natal nest one female had a long nest tenure (=>8 days). During behaviorally distinct before dispersal? Behavioral compar- videotaping, the future tenure of each female was not isons between more versus less cooperative individuals can known. Consequently, multiple videos were taken. Later, help clarify the broader behavioral consequences of cooper- 17 tapes that contained paired long and short tenure ative decisions. The costs of helping (Schmid-Hempel and individuals were chosen for behavioral analysis. The Wolf 1988; O’Donnell and Jeanne 1992) are expected to fraction of time each wasp spent resting, inspecting cells, produce a tradeoff between current helping behavior and and foraging was scored. Resting time included time spent future reproductive success (Cant and Field 2001). Conse- inactive on the front of the nest as well as time spent out of quently, individuals with future reproductive options may sight behind the nest. All behavior was scored by an invest less in current helping behavior. observer who did not know the nest tenure of the focal In this paper, I use Polistes wasps as a model to perform wasps. After square-root transformation, the behavioral data a detailed analysis of early dispersal behavior. Previous conformed to the assumption of normality using the work suggests that many Polistes ‘workers’ who leave their Shapiro-Wilk test for normality (all p>0.05). Paired t-tests Behav Ecol Sociobiol (2007) 61:1877–1883 1879 were used to compare the behavior of long versus short spots on their clypeus, while wasps with small ‘brokenness’ tenure wasps within each colony. numbers have smaller, fewer, and smoother spots. All dispersal analyses consider the first cohort of emerging ‘workers’ on each colony. We defined the first Factors that influence early dispersal cohort as wasps who eclosed within 20 days after the first individual eclosed on a colony. For example, if the P. dominulus nests were followed over the entire 2004 first individual on a nest eclosed on July 1, the first cohort season. After nest founding, foundresses were marked with encompasses all the individuals emerging between July 1 individually identifiable paint marks. During the preworker and July 20. Focusing on the first cohort ensures that all phase, nests were censused every 7 days to assess queen wasps in the dispersal analyses would be traditionally turnover. Nests were always censused early in the morning considered ‘worker destined’ offspring. July 20 was used when all colony members were present and wasps were as the cutoff for population-wide dispersal analyses cool and inactive. After workers eclosed on the most because first workers on most nests emerged between advanced colony (June 15), each nest was censused every June 25 and July 1. The data conformed to the assumption 2–3 days. Later in the season, from July 20 to late August, of normality using the Shapiro-Wilk test for normality (all colonies were censused every 6 days. At each census, p>0.05). Dispersal analyses were performed using para- newly eclosed wasps were marked with individually metric statistical tests. identifiable enamel paint marks and weighed with a balance accurate to 0.002 g. Wasps that emerged between June 15 and July 20 were also photographed for facial pattern Results analysis. During each census, the identifications of all previously marked resident adults were recorded. Behavior before dispersal The detailed census data were used to calculate early females’ first and last day on a nest. A female’s first day on A pair of short and long tenure workers were observed the nest was calculated as halfway between the census day within each of 17 nests. Short and long tenure workers were before the female was observed on the nest and the census observed during the same 2 h and were of similar age at day the female was first marked. A female’s last day on the observation (t17=1.07, p=0.30). Nevertheless, there were nest was calculated as halfway between the census day the significant differences in their behavior. Wasps with short female was last seen on the nest and the census day where tenures spent a larger fraction of their time resting than its permanent absence began. Tenure was calculated as the those with long tenures (Fig. 1, t17=2.90, p=0.010). Wasps difference between a female’s last and first days. In with short tenure also spent a smaller fraction of their time analyses, tenure length was square root transformed for foraging than those with long tenure (Fig. 2, t17=2.65, p= normality. Colony size was measured by counting the 0.017). There was no difference in the proportion of time number of cells in each nest on July 1 (a few days after first spent cell inspecting between short and long tenure workers worker emergence). (t17=0.13, p=0.89). In total, wasps spend over 99% of their P. dominulus facial patterns are a condition-dependent time resting, foraging, or inspecting cells. Therefore, each signal of dominance (Tibbetts and Dale 2004; Tibbetts behavioral result is not independent; time spent resting 2006; Tibbetts and Curtis 2007), so individual facial versus foraging is likely to directly tradeoff. patterns were assessed to determine the relationship between individual quality and cooperation. Facial patterns were measured using the methods of Tibbetts and Dale (2004). Briefly, the variable area of the clypeus was converted into a 30h×60l pixel bitmap. At each of the 60 horizontal points along the clypeus, the number of black pixels on each vertical column was counted. The resulting data provides information about the amount of black at each point along the horizontal gradient of the clypeus. Then, I calculated the standard deviation of the black pigment deposition in the central part of the clypeus. This number provides information about the amount and position of black pigment on the clypeus, particularly the Fig. 1 Proportion of time long versus short tenure individuals spent amount of disruption or ‘brokenness’ of the black pattern. resting (+SE). Within a nest, short tenure individuals spend more time Wasps with high ‘brokenness’ numbers have multiple, large resting than long tenure individuals (t17=1.07, p=0.010) 1880 Behav Ecol Sociobiol (2007) 61:1877–1883

Fig. 2 Proportion of time long versus short tenure individuals spent foraging (+SE). Within a nest, long tenure individuals spend more Fig. 4 Nests with queen turnover had a higher proportion of offspring time foraging than short tenure individuals (t17=2.65, p=0.017) with a short nest tenure than nests without queen turnover (t31=3.25, p=0.004) Factors that influence early dispersal patterns are a condition-dependent signal of dominance in Generally, larger nests had offspring with longer tenure. P. dominulus (Tibbetts and Dale 2004; Tibbetts 2006; There is a significant, positive relationship between the Tibbetts and Curtis 2007), so facial patterns were used as a square-root transformed mean tenure of the first cohort of measure of individual quality. Within each nest, there was offspring from a colony and the number nest cells in that no relationship between the facial patterns of long and short colony (Fig. 3, R2=0.23, f=8.7, p=0.006, n=31). Nests tenure individuals (t =0.9, p=0.38). However, the high with more cells had workers with longer tenure. 31 level of dispersal in nests with queen turnover could Tenure was strongly influenced by the presence or potentially overwhelm any effect of individual character- absence of the original queen. Although a new individual istics on dispersal. Consequently, separate analyses were always took over as the dominant reproductive following performed in nests with and without queen turnover. Within queen disappearance, nests whose queen disappeared nests where the dominant queen remained on the colony before 20 July had a larger proportion of short tenure through July (good nests), short tenure individuals had offspring than nests whose queen remained after 20 July higher quality facial patterns than long tenure individuals (Fig. 4, t =2.85, p=0.01). July 20 was used as a 31 (t =1.77, p=0.094). Within nests where the queen dis- population-wide cutoff for ‘worker-destined’ offspring, 19 appeared (bad nests), there was no relationship between although these results are not sensitive to specific cutoff facial pattern and tenure (t =0.9, p=0.39). There was no date, as any date within the month of July yields similar 12 relationship between body weight and nest tenure. Overall, results. Colonies with queen turnover also had offspring short tenure and long tenure workers within each nest were with shorter square-root transformed mean tenure than similarly sized (t =0.03, p=0.97). There was also no colonies lacking queen turnover (t =3.25, p=0.004). 31 31 difference in the weight of short and long tenure individuals The characteristics of short and long tenure individuals within ‘good’ nests lacking queen turnover (t =0.23, p= within each nest were compared to assess the influence of 19 0.82) or ‘bad’ nests with queen turnover (t =0.34, p=0.74). individual characteristics on behavioral strategies. Facial 12

Discussion

Behavior prior to dispersal

The first brood of offspring from social insect colonies are usually considered workers who remain on their natal colony as nonreproductive helpers until death. However, some of the first brood of Polistes offspring disappear from their natal colony soon after eclosion. For example, Pardi (1948, cited in Mead et al. 1995) found that 45% of Fig. 3 Relationship between colony size and the nest tenure of ‘worker’ P. dominulus in Italy disappeared from their natal offspring that eclosed during the first 20 days of offspring production. Larger nests had offspring with longer nest tenure (R2=0.23, f=8.7, colony within 10 days of emergence. These early females n=31, p=0.006) with short nest tenure may be pursuing alternative Behav Ecol Sociobiol (2007) 61:1877–1883 1881 behavioral strategies. Some early females have been probability of nest inheritance spend less time foraging than observed to disperse from the natal colony, enter early other individuals (Cant and Field 2001; Field et al. 2006). diapause, and emerge the following year to found a nest (personal observations; Reeve et al. 1998; Starks 2001). Factors that influence dispersal Others found new nests or usurp previously established nests (personal observations; Strassmann 1981; Page et al. The patterns of early worker dispersal suggest the relative 1989; Queller et al. 1997; Hagiwara and Kojima 2002). benefits of helping versus dispersing influence early However, most of ‘workers’ who disappear from their natal females’ nesting strategies. Colony-level factors seemed to colony within a few days of eclosion are never located. have the strongest effect, although individual factors may Consequently, it has been difficult to assess whether many also play a role. short tenure females are pursuing an alternative reproduc- Queen turnover influences early female nest tenure; tive strategy or whether most are merely dying. colonies with queen turnover had a larger proportion short- In this paper, we use behavioral observations on the natal tenure offspring than colonies without queen turnover. nest to show Polistes ‘workers’ with short nest tenure are Queen turnover reduces relatedness between a colony’s behaviorally distinct before dispersal. Short tenure females current and future offspring thereby reducing the kin-selected are relatively uncooperative, spending more time resting benefits of cooperation (Hamilton 1964a, b; Strassmann and less time foraging than long tenure females. The 1996). In addition, nests may suffer a general productivity significant early behavioral differences between short and decline following the loss of a queen (Klahn 1988; long tenure females suggest that many individuals with Strassmann 1996; Strassmann et al. 2004). It is difficult to short nest tenure are pursuing selfish, alternative behavioral assess the relative importance of these factors on dispersal strategies, rather than dying prematurely. Of course, it is behavior, as both could decrease the benefits of coopera- unlikely that all short tenure individuals disperse; some tion. Previous work suggests that small differences in premature death is expected in every population. In the relatedness may not influence Polistes dispersal behavior, field, it is not possible to determine the exact fate of every as Reeve et al. (1998) found that dispersal was more individual, so all wasps who disappear from the natal common in single-queen than multi-queen P. fuscatus colony soon after emergence are pooled in the behavioral colonies. However, many cooperative breeders appear to analysis. Pooling could decrease our ability to detect a preferentially help kin (e.g., Reyer 1984; Komdeur 1994; behavioral difference between long and short tenure wasps. Griffin and West 2003; but see Keller 1997; Strassmann However, the significant overall behavioral difference 1996), so further experiments that directly assess the effect between short and long tenure females indicates the two of kinship on dispersal could be quite interesting. groups are behaviorally distinct on average; most short Nest size was also correlated with the proportion of short tenure females are dispersing rather than dying prematurely. tenure offspring; smaller nests had a relatively larger Gynes and early females with a short nest tenure have fraction of short tenure offspring. Large, mature nests are strikingly similar behavior on the natal colony. Both avoid more likely to survive until gyne production, so worker the risk and energetic expense associated with foraging investment in large nests is more likely to be realized (Schmid-Hempel and Wolf 1988; O’Donnell and Jeanne though successful gyne production (Queller 1989; Reeve 1992) and spend more time resting (Gadagkar 1991; Reeve et al. 1998). The lower probability of nest failure in large 1991; Keeping 1992). The behavioral similarities between nests may increase the relative benefits of cooperation and gynes and early dispersers make intuitive sense, as both increase the proportion of individuals who stay and help. must conserve energy for independent reproduction. Help- Reeve et al. (1998) found a similar relationship between ing is energetically costly and can increase the risk of injury colony size and nest tenure in P. fuscatus paper wasps. and predation (Schmid-Hempel and Wolf 1988; O’Donnell In addition to colony-level factors like kinship and and Jeanne 1992; Nielsen 2001). There is a tradeoff between colony size, individual factors may also influence cooper- current and future reproductive success, such that current ative decisions. The role of individual factors in cooperative investment in helping behavior decreases the potential for decisions has not been studied in detail, although individuals future independent fitness gains (West-Eberhard 1981; Cant differ in a range of ways, including their dominance, survival, and Field 2001). Consequently, individuals with higher immune function, fertility, condition, etc. (Andersson 1994; probability of independent breeding are predicted to invest Sheldon 1994; Jennions et al. 2001; Hunt et al. 2004; less in helping their current colony (Cant and Field 2001). Tibbetts and Dale 2004). All these factors could influence For example, hopeful reproductives in Ropalidia marginata the probability of successful, independent nest foundation wasps have been termed ‘sitters’ because they spend most as well as the benefits of different nesting strategies of their time resting and do not forage (Gadagkar 1991). In (Komdeur 2006). One way to quickly assess individual Polistes and Stenogastrine wasps, individuals with higher characteristics and their effect on cooperation is to use 1882 Behav Ecol Sociobiol (2007) 61:1877–1883 quality signals as an indicator of their bearer’s overall Instead, individual Polistes incorporate information about phenotypic and genetic constitution. For example, in P. individual and colony status to pursue strategies that dominulus, an individual’s facial pattern is a signal of maximize their reproductive potential. quality that is related to their agonistic abilities (Tibbetts and Dale 2004) and condition (Tibbetts and Curtis 2007). In Acknowledgment Thanks to J. Shorter for videotape analysis, M. this study, there was no relationship between offspring Tyner for help with facial pattern analysis and data entry, as well as B. facial pattern and dispersal behavior, suggesting that Daley, K. Ross, and two anonymous reviewers for helpful comments individual quality did not have a strong effect on on the manuscript. This manuscript complies with the laws of the cooperative decisions in P. dominulus. However, within United States. nests lacking queen turnover, the mean advertised quality P. dominulus who dispersed was higher than the mean advertised quality of P. dominulus who did not disperse, References although this difference was not statistically significant (p=0.09). Therefore, further research with a larger sample could be quite useful to rigorously test whether wasps with Andersson M (1994) Sexual selection. Princeton University Press, Princeton greater dominance potential are less likely to forgo Cant MA, Field J (2001) Helping effort and future fitness in cooperative independent reproduction (West-Eberhard 1969). In gener- animal societies. Proc R Soc Lond B Biol Sci 268:1959–1964 al, additional research on quality signals in a variety of Cervo R, Zacchi F, Turillazzi S (2000) Polistes dominulus (Hyme- contexts may help broaden our understanding of quality noptera, ) invading North America: some hypotheses for its rapid spread. Insectes Soc 47:155–157 and its role in social behavior. Choe J, Crespi B (1997) The evolution of social behavior in insects The dispersal data suggest that both individual and and arachnids. Cambridge University Press, Massachusetts colony characteristics influence reproductive strategies in Emlen ST (1991) Evolution of cooperative breeding in birds and the Polistes. The results support much of what is known mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell Scientific, Oxford, about caste in primitively eusocial insects. First, there is no UK, pp 301–337 strict preimaginal caste bias, as environment after pupal Emlen ST (1995) An evolutionary theory of the family. Proc Natl eclosion has a strong influence in reproductive strategies Acad Sci USA 92:8092–8099 (review in O’Donnell 1998). Caste flexibility allows newly Field J, Cronin A, Bridge C (2006) Future fitness and helping in social queues. Nature 441:214–217 eclosed workers to optimize their reproductive strategies by Gadagkar R (1991) Belonogaster, Mischocyttarus, Parapolybia, and using information about the social environment in repro- independent-founding Ropalidia. In: Ross KG, Matthews RW (eds) ductive decisions. Although there is caste flexibility, all The social biology of wasps. Comstock, Ithaca, NY, pp 149–190 individuals do not have identical reproductive capabilities. Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636 Early environment influences adult quality and the costs Hagiwara Y, Kojima J (2002) Reproductive options for first brood and benefits of different strategies (Lindstrom 1999; “workers” emerging in orphan nests of Polistes nipponensis Metcalfe and Monaghan 2001; Tibbetts and Curtis 2007). (, Vespidae). Insectes Soc 49:191–195 Therefore, preimaginal factors likely influence caste deci- Hamilton WD (1964a) Genetical evolution of social behaviour I. J Theor Biol 7:17–52 sions, although castes are not rigidly fixed before eclosion Hamilton WD (1964b) Genetical evolution of social behaviour II. J (Solis and Strassmann 1990; Hunt 1991). The cooperative Theor Biol 7:1–16 decisions of primitively eusocial insects have a lot in Hunt JH (1991) Nourishment and the evolution of the social Vespidae. common with those of cooperatively breeding vertebrates In: Ross KG, Matthews RW (eds) The social biology of wasps. Comstock Publishing, London, pp 426–450 (Sherman et al. 1995; Lacey and Sherman 2005). Both Hunt J, Bussiere LF, Jennions MD, Brooks R (2004) What is genetic groups integrate information about individual character- quality? Trends Ecol Evol 19:329–333 istics and ecology to make decisions about cooperation Jennions MD, Moller AP, Petrie M (2001) Sexually selected traits and (Emlen 1991; Koenig et al. 1992; Choe and Crespi 1997). adult survival: a meta-analysis. Quart Rev Biol 76:3–36 Johnson RN, Starks PT (2004) A surprising level of genetic diversity Such similarities across divergent taxa may help broaden in an invasive wasp: Polistes dominulus in the northeastern our understanding of the factors that influence cooperative United States. Ann Entomol Soc Am 97:732–737 behavior. Keeping MG (1992) Social organization and division of labor in Overall, Polistes display a surprising degree of repro- colonies of the Polistine Wasp, Belonogaster petiolata. Behav Ecol Sociobiol 31:211–224 ductive flexibility. Behavioral data suggest that some early Keller L (1997) Indiscriminate altruism: unduly nice parents and females do not help at their natal colony. These noncoop- siblings. Trends Ecol Evol 12:99–103 erative females likely disperse from their natal colony to Klahn J (1988) Intraspecific comb usurpation in the social wasp pursue independent reproduction. Colony size and queen Polistes fuscatus. Behav Ecol Sociobiol 23:1–8 Koenig WD, Pitelka FA, Carmen WJ, Mumme RL, Stanback MT turnover influence dispersal behavior. Therefore, early (1992) The evolution of delayed dispersal in cooperative emerging Polistes are not strongly constrained by ecology. breeders. Quart Rev Biol 67:111–150 Behav Ecol Sociobiol (2007) 61:1877–1883 1883

Komdeur J (1994) The effect of kinship on helping in the cooperative Schmid-Hempel P, Wolf T (1988) Foraging effort and life-span of breeding Seychelles Warbler (Acrocephalus sechellensis). Proc R workers in a social insect. J Anim Ecol 57:509–521 Soc Lond B Biol Sci 256:47–52 Sheldon BC (1994) Male phenotype, fertility, and the pursuit of Komdeur J (2006) Variation in individual investment strategies among extrapair copulations by female birds. Proc R Soc Lond B Biol social animals. Ethology 112:729–747 Sci 257:25–30 Lacey EA, Sherman PW (2005) Redefining : concepts, Sherman PW, Lacey EA, Reeve HK, Keller L (1995) The eusociality goals and levels of analysis. Ann Zool Fenn 42:573–577 continuum. Behav Ecol 6:102–108 Lindstrom J (1999) Early development and fitness in birds and Solis CR, Strassmann JE (1990) Presence of brood affects caste mammals. Trends Ecol Evol 14:343–348 differentiation in the social wasp, Polistes exclamans Viereck Mead F, Gabouriaut D, Habersetzer C (1995) Nest-founding (Hymenoptera, Vespidae). Funct Ecol 4:531–541 behavior induced in the first descendants of Polistes domi- Starks PT (2001) Alternative reproductive tactics in the paper wasp nulus Christ (Hymenoptera, Vespidae) colonies. Insectes Soc Polistes dominulus with specific focus on the sit-and-wait tactic. 42:385–396 Ann Zool Fenn 38:189–199 Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow Strassmann JE (1981) Evolutionary implications of early male and now, pay later? Trends Ecol Evol 16:254–260 satellite nest production in Polistes exclamans colony cycles. Nielsen MG (2001) Energetic cost of foraging in the Behav Ecol Sociobiol 8:55–64 Rhytidoponera aurata in tropical Australia. Physiol Entomol Strassmann JE (1996) Selective altruism towards closer over more 26:248–253 distant relatives in colonies of the primitively eusocial wasp, Nonacs P, Reeve HK (1995) The ecology of cooperation in wasps— Polistes. In: Turillazzi S, West-Eberhard MJ (eds) Natural causes and consequences of alternative reproductive decisions. history and evolution of paper-wasps. Oxford University Press, Ecology 76:953–967 NY, pp 190–201 O’Donnell S (1998) Reproductive caste determination in eusocial Strassmann JE, Fortunato A, Cervo R, Turillazzi S, Damon JM, wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43:323– Queller DC (2004) The cost of queen loss in the social wasp 346 Polistes dominulus (Hymenoptera: Vespidae). J Kansas Entomol O’Donnell S, Jeanne RL (1992) Lifelong patterns of forager behavior Soc 77:343–355 in a tropical swarm-founding wasp—effects of specialization and Tibbetts EA (2006) Badges-of-status in worker and gyne Polistes activity level on longevity. Anim Behav 44:1021–1027 dominulus wasps. Ann Zool Fenn 43:575–582 Page RE, Post DC, Metcalf RA (1989) Satellite nests, early males, and Tibbetts EA, Curtis TR (2007) Rearing conditions influence quality plasticity of reproductive behavior in a paper wasp. Am Nat signals but not individual identity signals in Polistes wasps. 134:731–748 Behav Ecol 18:602–607 Pardi L (1948) Ricerche sui Polistini. 11. Sulla durata della Tibbetts EA, Dale J (2004) A socially enforced signal of quality in a permanenza delle feminine nel nido e sull’ accrescimento della paper wasp. Nature 432:218–222 societa in Polistes gallicus (L.). Atti della Societa Toscana di Tibbetts EA, Reeve HK (2000) Aggression and resource sharing Scienze Naturali 55:1–15 among foundresses in the social wasp Polistes dominulus: Queller DC (1989) The evolution of eusociality—reproductive head testing transactional theories of conflict. Behav Ecol Sociobiol starts of workers. Proc Natl Acad Sci USA 86:3224–3226 48:344–352 Queller DC, Peters JM, Solis CR, Strassmann JE (1997) Control of Turillazzi S (1991) The Stenogastrinae. In: Ross KG, Matthews reproduction in social insect colonies: individual and collective RW (eds) The social biology of wasps. Comstock, Ithaca, relatedness preferences in the paper wasp, Polistes annularis. NY, pp 74–98 Behav Ecol Sociobiol 40:3–16 West-Eberhard M (1969) The social biology of Polistine wasps. Misc Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in Publ Mus Zool Univ Mich 140:1–101 insect societies. Annu Rev Entomol 51:581–608 West-Eberhard MJ (1981) Intragroup selection and the evolution of Reeve HK (1991) Polistes. In: Ross KG, Matthews RW (eds) The insect societies. In: Alexander RD, Tinkle DW (eds) Natural social biology of wasps. Comstock Publishing Associates, Ithaca, selection and social behaviour: recent research and new theory. pp 99–148 Chiron, New York, pp 3–17 Reeve HK, Peters JM, Nonacs P, Starks PT (1998) Dispersal of first Wheeler DE (1986) Developmental and physiological determinants of “workers” in social wasps: causes and implications of an caste in social Hymenoptera—evolutionary implications. Am Nat alternative reproductive strategy. Proc Natl Acad Sci USA 128:13–34 95:13737–13742 Wilson EO (1971) The insect societies. Belknap, New York Reyer HU (1984) Investment and relatedness—a cost benefit analysis Yanega D (1989) Caste determination and differential diapause of breeding and helping in the Pied Kingfisher (Ceryle rudis). within the 1st brood of Halictus rubicundus in New York Anim Behav 32:1163–1178 (Hymenoptera, Halictidae). Behav Ecol Sociobiol 24:97–107