Ann. Zool. Fennici 41: 789–808 ISSN 0003-455X Helsinki 20 December 2004 © Finnish Zoological and Botanical Publishing Board 2004

Kin recognition in eusocial wasps

George J. Gamboa

Oakland University, Rochester, MI 48309, USA

Received 22 Apr. 2004, revised version received 15 Sep. 2004, accepted 2 June 2004

Gamboa, G. J. 2004: Kin recognition in eusocial wasps. — Ann. Zool. Fennici 41: 789–808.

Greenberg’s landmark publication (Science 206[1979]: 1095–1097) on kin recogni- tion in sweat bees was followed closely by experimental studies of kin recognition in primitively eusocial paper wasps. These early studies of recognition in social wasps concentrated on documenting nestmate recognition ability, which then stimulated interest in the mechanism subserving recognition ability. For the major portion of my review, I summarize our current understanding of kin, brood, and nest recognition abil- ity in social wasps and its underlying mechanism, relying primarily on paper wasps (Polistes) as a model system. In my discussion of the mechanism of recognition, I review our understanding of the perception, expression, and action components of recognition. I also provide a synopsis of the recent recognition studies of two species of Polistes and their congeneric, obligate social parasites. Finally, I discuss our under- standing of the ecology of kin recognition in social wasps and then close my review by contemplating the future directions of kin recognition research.

Introduction trated on documenting recognition ability, which then generated interest in the mechanism of For some inexplicable reason, the serious study recognition. Subsequently, the focus of most of kin recognition did not closely follow the pub- kin recognition studies of social wasps, includ- lication of Hamilton’s (1964a, 1964b) seminal ing recent studies, has been the mechanism that theories on kin selection. It was 15 years later underlies kin/nestmate recognition in wasps of when the landmark publication by Greenberg the primitively eusocial genus, Polistes. There (1979) first triggered intensive kin recognition have been relatively few studies of kin/nestmate research in both vertebrates and invertebrates. recognition in the highly eusocial wasps. Several Greenberg (1979), in a classic study, documented studies of Polistes wasps have examined aspects that sweat bees recognized their relatives using of the ecology, evolution, or adaptiveness of kin odor cues that are at least partly genetically recognition, which has provided an understand- specified (reviewed in Holmes 2004). ing of kin recognition in temperate Polistes The earliest experimental studies of kin rec- that is as complete as that of any other taxon of ognition in social wasps were those of Noonan animals. (1979) and Ross and Gamboa (1981) who exam- In my review, I first summarize the evidence ined nestmate recognition in the paper wasps, for recognition ability in social wasps and then, Polistes fuscatus and P. metricus, respectively. for the major portion of the article, discuss our These early studies of kin recognition concen- current understanding of the mechanism that 790 Gamboa • ANN. ZOOL. FENNICI Vol. 41 subserves this ability. This is followed by a nestmates from non-nestmates. Although nega- synopsis of the recent recognition studies of P. tive results can be due to factors other than a lack dominulus and P. biglumis in association with of recognition ability (Gamboa et al. 1991a), it their obligate social parasites, P. sulcifer and P. is not necessarily adaptive for all social species atrimandibularis, respectively. I then discuss our to manifest or possess kin recognition ability. In understanding of the ecology of kin recognition fact, kin recognition could be maladaptive in cer- and close by contemplating the future directions tain situations (Reeve 1989, Ratnieks & Reeve of kin recognition research in social wasps. 1992, Keller 1997, Bull & Adams 2000). Based primarily on studies of P. fuscatus, all classes of adult females including gynes, Kin recognition ability foundresses, and workers possess nestmate rec- ognition ability (Gamboa 1996). In addition, Adult–adult recognition males can recognize their male and female nest- mates (Shellman-Reeve & Gamboa 1985, Ryan Nestmate recognition, i.e., the differential treat- & Gamboa 1986), although there is presently ment of conspecifics on the basis of colony no definitive evidence that Polistes females can origin, has been documented in at least seven recognize their brothers. However, it would be of the approximately 200 species of Polistes. surprising if females lacked this ability since Although nestmate recognition in Polistes is all classes of adults have the appropriate colony probably widespread, it is not necessarily uni- labels and perceptual systems for nestmate rec- versal. All seven species of Polistes reported to ognition. exhibit nestmate recognition are temperate spe- Social wasps also have the ability to rec- cies. These species include P. metricus, P. fus- ognize some non-nestmate kin. In laboratory catus, P. exclamans, P. carolina and P. annularis studies conducted with blind recognition assays, (Gamboa 1996) as well as the more recently gynes of P. fuscatus treated non-nestmate aunts studied P. biglumis (Lorenzi et al. 1997) and P. and nieces like nestmate sisters, i.e., highly tol- dominulus (Starks et al. 1998). Since most spe- erantly (Gamboa et al. 1987, Gamboa 1988). cies of Polistes are tropical (Reeve 1991), our In blind field studies that involved switching knowledge of nestmate recognition in Polistes is colonies of known relatedness to determine how limited to a minority subset of the genus. resident females treated returning non-nestmate Nestmate recognition has also been reported kin, Bura and Gamboa (1994) found that the in the social wasps, Vespula maculifrons (Ross treatment of non-nestmate kin was highly varia- 1983), Dolichovespula maculata (Ryan et al. ble. Most cousins and nieces (~50%–65%) were 1985), Ropalidia marginata (Venkataraman et al. treated highly intolerantly, i.e., like unrelated 1988), Belonogaster petiolata (Keeping 1990), non-nestmates. However, a minority of cousins Liostenogaster flavolineata, L. vechti, Parisch- and nieces were treated highly tolerantly, i.e., nogaster jacobsoni (Cervo et al. 1996, 2002), like nestmate sisters. Most aunts and non-nest- and Vespa crabro (Ruther et al. 1998, 2002). mate sisters (~80%) were treated like nestmate In all cases, with the exception of male-female sisters while a minority were treated like unre- recognition in a mating context (e.g., Ryan & lated non-nestmates. Unlike the treatment of Gamboa 1986), nestmates of social wasps have non-nestmate kin, resident females were uni- been more tolerant of each other than have non- formly tolerant and uniformly intolerant toward nestmates. female nestmates and unrelated female non-nest- To the best of my knowledge, the only spe- mates, respectively. cies of social wasp that has been studied but I am unaware of any evidence that social not found to display nestmate recognition abil- wasps have the ability to discriminate among ity is Parachartergus colobopterus. Gastreich et nestmates on the basis of relatedness. Queller et al. (1990) conducted both laboratory and field al. (1990) provided evidence that foundresses of recognition bioassays of P. colobopterus and P. annularis lack the ability to make intracolo- found no evidence that females discriminated nial discriminations on the basis of relatedness. ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 791

Using starch gel electrophoresis to determine and subsequent DNA microsatellite analyses to relatedness, they reported that foundresses did determine the maternity of larvae, Strassmann not preferentially found field nests with more et al. (2000) found that foundresses of multiple- closely related nestmates. Their results are espe- foundress associations did not preferentially feed cially compelling since they found no evidence their own larvae. Thus, the laboratory study of of discrimination among former nestmates in a Panek and Gamboa (2000) and the field study of context in which I believe such an ability would Strassmann et al. (2000) both failed to find evi- almost certainly have important fitness conse- dence of intracolonial brood recognition on the quences for foundresses. basis of relatedness. Later, in my discussion of the mechanism of recognition, I discuss a feature of the mechanism that appears to preclude intra- Brood recognition colonial recognition.

Klahn and Gamboa (1983) switched pre-worker, brood-filled combs of P. fuscatus between colo- Comb recognition nies whose queens were former nestmates (sis- ters) and between colonies whose queens were Female P. fuscatus (Ferguson et al. 1987), P. unrelated. Foundresses destroyed the eggs and metricus (Espelie et al. 1990b), Dolichovespula young larvae of unrelated colonies but accepted maculata (Ferguson et al. 1987), P. dominulus the brood of sister colonies. Although foun- (Starks et al. 1998, Lorenzi & Caprio 2000, dresses did recognize brood on the basis of relat- Starks 2003), and P. biglumis (Lorenzi & Caprio edness, it was unknown whether the recognition 2003) can discriminate their own comb or comb cues were associated with the brood, comb, or fragment from that of foreign colonies. Pfen- both. Panek and Gamboa (2000) provided queens nig (1990) reported that P. exclamans workers of P. fuscatus a binary choice of two larvae in a can discriminate between a brood-filled frag- petri dish. Using blind behavioral observations, ment from their own comb and that from another the authors reported that queens discriminated colony although it’s not clear whether workers between their own and unrelated larvae, between recognized the comb, brood, or both. These stud- the larva of a sister and an unrelated larva, ies indicate that the ability to recognize one’s but not between their own larva and that of comb is common in social wasps. Comb recog- their sister. Queens typically bit or ate unrelated nition has typically been documented in those larvae but not their own or sister larvae. Thus, species that have been found to have nestmate queens clearly had the ability to recognize larvae recognition ability. Most nest recognition stud- on the basis of relatedness, and larvae obvi- ies have been laboratory studies, but in a recent ously possessed individually borne recognition study, Starks (2003) found that spring foun- cues. However, the study by Panek and Gamboa dresses of P. dominulus preferentially perched on (2000) did not reveal whether larvae produced or fragments of their natal comb over fragments of acquired their cues. unrelated colonies in a large field enclosure. The findings of Panek and Gamboa (2000) indicated that queens of P. fuscatus lacked the ability to make intracolonial discriminations The mechanism of recognition among larvae on the basis of relatedness since queens failed to discriminate between their own Perception component larvae and those of their sisters. Strassmann et al. (2000), in a blind field study of P. annularis, Kin recognition consists of three components: a species known to possess nestmate recognition perception, expression, and action. The percep- ability (Pfennig et al. 1983b), provided convinc- tion component includes the development of ing evidence that foundresses do not discrimi- a kin template, the sensory processing of rec- nate among larvae on the basis of relatedness. By ognition cues, and the algorithm for matching using videography of foundresses feeding larvae the template and encountered phenotype (Reeve 792 Gamboa • ANN. ZOOL. FENNICI Vol. 41

1989, Gamboa et al. 1991a). Most of the empiri- failed to discriminate nestmates from non-nest- cal studies dealing with the perception compo- mates (Shellman & Gamboa 1982), it wasn’t nent in social wasps have investigated the role, clear whether isolates failed to discriminate timing, and form of learning in the ontogeny because they were deprived of the opportunity to of recognition ability. For a discussion of the learn recognition cues from the nest or because perception component in recognition, see Mateo they were deprived of the opportunity to acquire (2004). cues from the nest, or both. To determine this, Early studies of P. fuscatus and P. carolina isolate nestmate and non-nestmate gynes of P. utilized blind observations to demonstrate that fuscatus were presented to experienced females, manipulating the experiences of young females i.e., females with extensive previous exposure to immediately after eclosion disrupted the devel- their nest and nestmates. In blind observations, opment of recognition ability. For example, Gamboa et al. (1986b) documented that these wasps isolated at eclosion later failed to dis- experienced females discriminated between iso- criminate between nestmates and non-nestmates late nestmates and isolate non-nestmates. Thus, (Shellman & Gamboa 1982). However, exposure isolates clearly possessed recognition cues and of newly eclosed females to their natal comb for their failure to develop recognition ability was at least one hour (but not extensive exposure to because they had been deprived of the oppor- nestmates) was necessary and sufficient for the tunity to learn cues from the nest. Furthermore, development of recognition ability. Furthermore, these results demonstrated that learning was unrelated wasps that had been exposed to dif- restricted to the adult stage and that wasps did ferent fragments of the same unrelated comb not learn their own cues (Gamboa 1996). Venka- (pseudonestmates) treated each other tolerantly, taraman et al. (1988) conducted blind triplet i.e., like nestmate sisters (Shellman & Gamboa observations and reported that Ropalidia mar- 1982, Pfennig et al. 1983a, 1983b). These stud- ginata also learns recognition cues. Wasps that ies demonstrated that newly emerged wasps were had been exposed as adults to their nest and nest- learning recognition cues and that the cues were mates, but not wasps isolated at eclosion, later learned from the comb. Interestingly, exposing a discriminated nestmates from non-nestmates. wasp to its natal nest for more than four hours had The learning of recognition cues in Polistes no effect on its recognition ability indicating that resembles imprinting. Young adults learn rec- learning was complete within four hours after ognition cues from the nest within a few hours emergence. Ross and Gamboa (1981) seques- after emergence and form durable memories of tered individual gynes of P. metricus, which had these cues (Ross & Gamboa 1981, Shellman extensive previous exposure to their nest and & Gamboa 1982, Pfennig et al. 1983a, 1983b, nestmates, from their nest and nestmates for 99 Gamboa et al. 1986b). Since Polistes learn rec- days. They reported that despite this extensive ognition cues from their natal comb, it is dif- isolation, gynes were still able to discriminate ficult to understand how wasps could develop nestmates from non-nestmates, demonstrat- the ability to make intracolonial discriminations ing that the memory of the learned recognition on the basis of relatedness. Presumably, such cue was very durable. Post and Jeanne (1982) discrimination ability would require that wasps found that laboratory overwintered foundresses learn their own recognition cues (self-referent of P. fuscatus preferentially associated with their learning; reviewed in Göth & Hauber 2004) former nestmates in founding a colony regardless rather than the cues of the nest. of whether they had overwintered with them or The ontogeny of recognition ability in with unrelated gynes. Starks (2003) documented Polistes appears to involve the development that foundresses of P. dominulus recognized their of intolerance to unfamiliar cues rather than natal nest after winter diapause. Both of these the development of tolerance to familiar cues. studies clearly show that the memory of recogni- For example, at eclosion female P. fuscatus are tion cues is long lasting. initially highly tolerant of all conspecifics but Although females of P. fuscatus isolated from only later become intolerant of conspecifics with their natal nest and nestmates at emergence later unfamiliar cues (Gamboa et al. 1986a, 1986b). ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 793

Polistes appear to treat conspecifics either visual, tactile, or auditory features of adult nest- tolerantly or intolerantly, and nothing in between. mates. Only chemical cues could potentially be For example, females of P. fuscatus treat non- shared by the comb and nestmates. Pfennig et al. nestmate kin either tolerantly, like nestmates, (1983b) found that females exposed to different or intolerantly, like unrelated non-nestmates fragments of the same unrelated comb shortly (Gamboa et al. 1987, Gamboa 1988, Gamboa after emergence later treated each other as nest- et al. 1991b, Bura & Gamboa 1994). There- mates. These females, pseudonestmates, must fore, females do not exhibit a graded behavio- have learned and acquired common cues from ral response to conspecifics that is proportional the nest fragments in order to later recognize to relatedness. Similarly, Pfennig (1990) and each other. These acquired cues must have been Gamboa et al. (1991b) found that females of P. odors. Finally, Gamboa et al. (1986b) reared exclamans and P. fuscatus were not more toler- colonies of P. fuscatus from egg through adult ant of non-nestmates from nearby colonies (~6– in the laboratory under identical environmental 100 m apart) than non-nestmates from distant conditions, including identical food and nesting colonies (≥ 10 000 m apart). One would assume materials. Females from these laboratory colo- that nearby non-nestmates are more likely to nies failed to discriminate nestmates from non- share environmental and genetic cues than dis- nestmates if they had been recently exposed to tant non-nestmates. The lack of graded behavio- their common environmental odors. Again, these ral responses is consistent with the cue similarity results point to odors, particularly environmental threshold property (Gamboa et al. 1986a, 1986b, odors, as recognition cues. Reeve 1989) in which a wasp matches the tem- Although the laboratory reared females of plate of the learned cues with the cues of the Gamboa et al. (1986b) initially failed to dis- encountered wasp. If there is a sufficient match criminate between nestmates and unrelated non- (or minimum similarity) between the learned and nestmates, after several days of isolation females perceived cue, the encountered wasp is treated did discriminate between nestmates and unre- tolerantly. Otherwise, the wasp is treated intoler- lated non-nestmates. These results indicated that antly. Therefore, tolerance of conspecifics does the recognition odors must have had heritable not increase continuously as a function of increas- components. The authors reasoned that the most ing similarity between the template and encoun- likely explanation for their results was that the tered cue. Unfortunately, we know little about common environmental odors shared by labora- the matching process that wasps use to compare tory colonies had decayed after several days of their template with the encountered phenotype. isolation thereby exposing the wasps’ heritable We also know little about the requisite minimum odors (Gamboa et al. 1986b). similarity between the template and encountered The laboratory study of Gamboa et al. cues that elicits tolerance or acceptance. (1986b) provides evidence that environmental odors from food and/or nesting materials can serve as components of the recognition odor Expression component of recognition in social wasps. Although environmental odors have considerable potential information value The expression component involves the nature as recognition cues (Gamboa et al. 1986a), the and production (or acquisition) of the cues evidence that recognition odors of social wasps (labels) that identify kin (Gamboa 1996). For a have heritable or genetic components is much discussion of the expression component in rec- more extensive and conclusive than the evidence ognition, see Tsutsui (2004). for environmental components of recognition odors. Nevertheless, environmental recognition odors may be important for species that live in The nature of the recognition cue chemically diverse environments (Gamboa et al. 1986a). Since Polistes learn their recognition cues from Although the laboratory study of Gamboa the natal comb, recognition cues cannot be et al. (1986b) provided evidence for a herit- 794 Gamboa • ANN. ZOOL. FENNICI Vol. 41 able component of the recognition odor, it was ognition odors acquired from one’s natal comb possible that their results were due to maternal are similar to those endogenous odors produced rather than genetic effects. However, several by individual wasps. The relative importance of studies later documented recognition between endogenous and acquired odors in Polistes is non-nestmate kin that had different mothers (e.g., unknown. Venkataraman et al. (1988) reported Gamboa 1988, Bura & Gamboa 1994), which that female Ropalidia marginata lack endog- clearly demonstrated that the recognition odor of enous odors and must acquire recognition odors P. fuscatus has a genetic component. from their natal nest. As discussed in consider- The ultimate origin of recognition odors (i.e., able detail elsewhere (Gamboa 1996), the results environmental or genetic) differs from the proxi- of Venkataraman et al. (1988) may have been mate source of recognition odors (i.e., endog- affected by their asymmetric exposures of triplet enous or exogenous). For example, endogenous members. It would be extremely worthwhile to odors could be genetic or environmental (e.g., present isolate nestmates and non-nestmates of environmental odor sources such as food could R. marginata to experienced females in the con- affect the metabolic byproducts of wasps) and text of their nest to determine if isolates possess exogenous odors could be environmental or colony-specific odors independent of exposure genetic (e.g., genetic odors might be deposited to their natal comb. on the nest by the queen and then acquired from the nest). Gamboa et al. (1986b) conducted a reciprocal nest exposure study of P. fuscatus Identification of the recognition odor using blind observations and found that nest- mate recognition could be mediated by endog- In two elegant and convincing studies, Singer enous odors, exogenous (acquired) odors, or and Espelie (1992, 1996) demonstrated that both. Interestingly, wasps that learned both the workers of P. metricus used cuticular hydro- endogenous and exogenous components of their carbons as nestmate recognition cues. Using nestmates’ odor were not more tolerant of each blind triplet observations, the authors found that other than wasps that had learned only one newly emerged wasps that had been exposed component of their nestmates’ odor. Either exog- to their untreated nest, but not wasps exposed enous or endogenous odors were sufficient to to a hexane-washed nest, later discriminated mediate a full recognition response, but the two nestmates from non-nestmates. Newly emerged components were not additive in their effect on wasps that had been exposed to a washed nest in tolerance (Gamboa et al. 1986b). These results which the hydrocarbon extracts had been reap- provided additional support for the cue similar- plied also later discriminated nestmates from ity threshold property (see Gamboa et al. 1986b, non-nestmates. Singer and Espelie (1996) further 1986a, Reeve 1989). reported that experienced females were more There appears to be some confusion as to likely to accept newly emerged nestmates if whether recognition in paper wasps is mediated they had been previously exposed to their natal by endogenous odors, acquired odors, or both. nest with its hydrocarbons intact. This finding For example, in a review of recognition, Sher- indicated that adult wasps had acquired colony man et al. (1997) state that paper wasps use odors, i.e., hydrocarbons, from their natal nest. odors acquired from the comb after eclosion In addition, as had been reported in P. fuscatus, to discriminate nestmates from non-nestmates. Singer and Espelie (1996) provided evidence that Although Polistes can acquire recognition odors P. metricus females do not learn their own odor from the comb, wasps possess a colony-spe- and that learning is restricted to the adult stage. cific odor independent of prior exposure to the They also presented evidence that the ontogeny comb after eclosion. The results of Gamboa of recognition ability in P. metricus, as in P. fus- (1986b), together with the results of Panek et catus, involves the development of intolerance to al. (2001), demonstrate that P. fuscatus utilizes unfamiliar odors rather than the development of endogenous, colony-specific recognition odors tolerance to familiar odors. in nestmate recognition. Presumably, the rec- In a study of nest recognition, Espelie et ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 795 al. (1990) reported that workers of P. metricus cluded that nest hydrocarbons were not as impor- could discriminate between their own nest and tant as a combination of factors, including the a foreign nest when nests were untreated and presence of brood, in nest adoption. They further when hexane-washed nests had their hydrocar- concluded that nest recognition in P. dominulus bon extracts reapplied. However, workers did is probably affected by a variety of complemen- not manifest this ability when presented with tary stimuli rather than solely by isolated stimuli nests that had their hydrocarbons extracted. such as nest hydrocarbons. In a similar study, Layton and Espelie (1995) However, it is possible that the recognition found that workers of P. metricus previously assay utilized by Soleilhavoup et al. (2001), exposed to fragments of their nests displayed nest adoption, does not assess nest recognition different behaviors and nest affinities depending ability. Nest adoption may be affected by the on whether the nests to which they have been presence of brood, and wasps may perceive nests exposed contained hydrocarbons (untreated and with brood as a more valuable resource than an reapplied) or not. The results of these two studies empty nest. In fact, Starks (1998, 2001) has pre- showed that wasps utilize hydrocarbons for nest sented evidence that P. dominulus foundresses recognition and that the cues are learned from preferentially adopt colonies with more mature the nest shortly after eclosion. brood. Nests with brood could provide a food Lorenzi and Caprio (2000) examined nest rec- source for adoptees or provide adoptees a worker ognition in post-worker colonies of P. dominulus force. Both consumption of brood and adoption and P. nimphus. When presented with a choice of of unrelated workers are commonly observed in their own nest and a nearby nest, females of both females that usurp colonies of other conspecific species preferentially rested on their own nest. females (e.g., Klahn & Gamboa 1983). As expected, females of P. dominulus did not Lorenzi et al. (1997) reported that female discriminate between their own and nearby nests P. biglumis had the ability to discriminate dead if the nests had been washed in hexane. Females nestmates from dead non-nestmates unless the of both species discriminated between their own dead wasps had been washed in pentane. How- and nearby nests after the hexane-washed nests ever, when the pentane-washed dead wasps had had their hexane extracts reapplied. Surprisingly, their solvent extracts reapplied, females were female P. nimphus did discriminate between able to discriminate between dead nestmates and their own nest and a nearby nest after the nests non-nestmates. Similarly, Cervo et al. (2002) had been washed in hexane. Lorenzi and Caprio presented dead nestmates and dead non-nest- (2000) suggested that insufficient washing of mates to field colonies of Liostenogaster fla- P. nimphus nests might explain why nests were volineata and found that dead non-nestmates discriminated after being washed with hexane. were treated more aggressively than dead nest- It is not clear whether the results of Lorenzi and mates. However, dead nestmates and non-nest- Caprio (2000) reflect nest and/or brood recogni- mates were treated equally tolerantly if they had tion ability since the authors did not mention been washed in hexane. Dead, solvent-washed, whether they had removed brood from combs non-nestmates treated with nestmate cuticular prior to their tests of nest recognition. extracts were treated more tolerantly than dead, Soleilhavoup et al. (2001) investigated the solvent-washed, non-nestmates treated with non- relative importance of nest hydrocarbons, hydro- nestmate cuticular extracts. carbons from immature brood, and their com- Ruther et al. (2002) used blind behavioral binations on the probability of nest adoption in observations to examine the responses of female laboratory colonies of P. dominulus. The authors Vespa crabro to (1) dead nestmates and non- reported that artificial, plastic nests were likely nestmates, (2) dead nestmates that had extracts to be adopted if the nests contained eggs trans- of heneicosane, tricosane, or (Z)-9-tricosene planted from the original nest or contained a applied, and (3) dead nestmates that had all combination of transplanted eggs, transplanted three compounds applied. The authors found that larvae and pupae, and hydrocarbons from the females were more aggressive to dead non-nest- original comb. Soleilhavoup et al. (2001) con- mates than dead nestmates and that dead nest- 796 Gamboa • ANN. ZOOL. FENNICI Vol. 41 mates with applied hydrocarbons received sig- of six species of social wasps and found that nificantly more aggression than either untreated they differed in the presence or absence of dead nestmates or dead nestmates that had alkenes and methyl-branched alkanes as well their cuticular extracts reapplied. The results of as in the proportions of alkenes, n-alkanes, and Lorenzi et al. (1997), Cervo et al. (2002), and methyl-branched alkanes. In contrast, members Ruther et al. (2002), like those of Singer and of different colonies of the same species tended Espelie (1992, 1996), demonstrated that wasps to have the same cuticular compounds (but dif- were using cuticular hydrocarbons as recogni- ferent relative amounts) and similar proportions tion cues. of classes of compounds. For example, Espelie Pickett et al. (2000) added a novel com- et al. (1994) identified 20 cuticular hydrocarbons pound (pentacosanoic acid methyl ester) to the in P. fuscatus and found that the vast majority of nest material of P. dominulus and then exposed wasps shared the same compounds. females to the manipulated nest. Subsequently, Espelie et al. (1994) postulated that those females preferentially associated with nestmates cuticular hydrocarbons that serve as recognition that had acquired the novel compound demon- pheromones should (1) be colony specific, (2) be strating that wasps can learn and acquire artifi- heritable, (3) not differ markedly between castes cial chemicals as recognition cues and can dis- since the compounds proclaim colony identity, tinguish between chemical profiles that differ by and (4) have a distinctive stereochemistry, which a single compound. The study by Pickett et al. would make them easier for wasps to distinguish. (2000), together with the study by Gamboa et al. Using ANOVA and stepwise discriminant-func- (1986b), also demonstrates the potential impor- tion analyses of the hydrocarbon profiles of 124 tance of environmental odors in kin recognition. wasps from 23 P. fuscatus colonies (including Concurrent with studies demonstrating that 15 sister colonies), Espelie et al. (1994) found paper wasps were utilizing hydrocarbons as rec- that the compounds most efficacious for assign- ognition cues were numerous studies that exam- ing wasps to the correct colony and sister group ined the cuticular hydrocarbon profiles of various primarily were several methyl-branched alkanes. species of social wasps. By using a gas chroma- These methyl-branched alkanes had a distinctive tograph/mass spectrometer (GC/MS), research- stereochemistry and did not differ significantly ers have identified the cuticular compounds and between foundresses and workers. Thus, Espelie their relative amounts for a number of species of et al. (1994) considered these methyl-branched social wasps. These species include Paracharter- hydrocarbons to be leading candidates for kin gus aztecus (Espelie & Hermann 1988), P. metri- recognition pheromones in P. fuscatus. cus (Espelie et al. 1990), P. annularis (Espelie In order to understand which cuticular com- & Hermann 1990), Dolichovespula maculata pounds might serve as recognition cues, Gamboa (Brown et al. 1991), P. dominulus (Bonavita- et al. (1996) switched sister colonies of P. fus- Cougourdan et al. 1991), Vespula squamosa catus in the field and recorded whether aunts (Butts et al. 1991), Vespula maculifrons (Butts accepted or rejected their nieces. The authors et al. 1991), Vespula germanica (Brown et al. then analyzed the cuticular extracts of the 1991), P. biglumis (Lorenzi 1992), P. exclamans females with a GC/MS. A stepwise discriminant (Singer et al. 1992), P. fuscatus (Espelie et al. function analysis (DFA) was conducted to pre- 1994), Vespa crabro (Butts et al. 1995), and dict the behavioral outcomes (accept or reject) Liostenogaster flavolineata (Cervo et al. 2002). on the basis of differences in cuticular hydrocar- In general, investigators have found that the bon profiles. The stepwise DFA was highly sig- cuticular hydrocarbon profiles of social wasps nificant. A 100% correct classification of nieces’ are both species specific and colony specific acceptance or rejection was made on the basis of (Singer et al. 1998). Typically, interspecific dif- differences in 10 cuticular hydrocarbons. This ferences in cuticular hydrocarbons involve dif- was the first evidence of a linkage between dif- ferences in the types, proportions, and classes ferences in cuticular hydrocarbon profiles and of compounds present. For example, Singer et behaviors typically observed in a recognition al. (1998) compared the cuticular hydrocarbons context. ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 797

Gamboa et al. (1996) reported that two of or 48 h old. However, resident females did dis- the three compounds postulated by Espelie et criminate between nestmates and non-nestmates al. (1994) to be prime candidates for recogni- that were 72 h old, which indicated that a wasp’s tion pheromones were ranked highly in their colony signature developed between 2 and 3 discriminant function analysis. However, sev- days of age. Panek et al. (2001) also found that eral other compounds that were ranked highly the cuticular hydrocarbons of young wasps (24 h in the discriminant function analysis were not old) had changed significantly in older wasps (72 compounds postulated to be likely recognition h old) in colony specificity, abundance, and rela- pheromones by Espelie et al. (1994). In addition tive abundance. More specifically, 10 of 13 iden- to demonstrating a linkage between behavior and tified hydrocarbons were found in significantly differences in cuticular hydrocarbons, Gamboa greater abundance in 72 h-old wasps than in 24 et al. (1996) provided evidence that recognition h-old wasps and 6 of the hydrocarbons changed in P. fuscatus involved many compounds rather significantly in relative abundance between the than a few and that recognition was not based on two age classes. These results indicate that wasps the presence or absence of a compound. begin producing an endogenous, recognizable Dani et al. (2001) applied various hydrocar- colony odor at about three days of age. bons known to be part of the cuticular profile of P. dominulus to live workers. These treated work- ers were then introduced to their own colony in The source of cuticular hydrocarbons the laboratory. The application of linear alkanes to introduced workers did not elicit aggression A number of investigators have reported that from nestmates. However, the application of queens of paper wasps stroke the comb with the methyl-branched alkanes and methyl-branched venter of their abdomen. Cervo and Turillazzi alkenes did elicit aggression from nestmates. (1989) reported that when P. gallicus combs were This is the first study to provide direct evidence switched between queens, queens stroked the for- that methyl-branched alkanes and alkenes can eign comb with their gaster, possibly releasing a serve as recognition cues in social wasps. secretion onto the comb. Dani et al. (1992) docu- mented abdominal stroking in P. dominulus and hypothesized that a glandular secretion was being The timing of the expression of the colony applied to the comb. Lorenzi and Cervo (1992) odor and Cervo and Lorenzi (1996) reported that P. biglumis queens of both switched and naturally A number of investigators have reported that usurped colonies exhibited significantly higher newly eclosed social insects can be success- frequencies of abdominal stroking than control fully transferred between conspecific colonies queens. They hypothesized that stroking may (e.g., Litte 1976, Breed et al. 1988, Morel et function to apply the usurper’s odor to the comb, al. 1988, Jeanne et al. 1992, Venkataraman & and that the usurper’s acceptance by subsequently Gadagkar 1993, Lorenzi et al. 1999). One expla- emerging workers may depend on the odor simi- nation for why newly eclosed non-nestmates larity between the comb and the usurper. are treated tolerantly by resident females is that Van Hooser et al. (2002) approximated young adults lack a colony odor and thus are not intraspecific usurpation in P. fuscatus by switch- recognized as foreign conspecifics. Panek et al. ing field nestboxes containing combs between (2001) examined this hypothesis by isolating P. unrelated queens and then they compared the fuscatus wasps at eclosion for various periods of behavior of these alien queens with the behavior time to determine the age at which wasps were of matched, control queens in the field. In blind first recognized as nestmates and non-nestmates observations, the authors found that alien queens by experienced conspecifics. In blind observa- spent significantly more time stroking the comb tions, Panek et al. (2001) reported that mature than control queens. Furthermore, the tolerance resident females did not discriminate between of alien queens by subsequently emerging work- nestmates and non-nestmates that were 1, 24, ers was significantly, positively correlated with 798 Gamboa • ANN. ZOOL. FENNICI Vol. 41 the length of time alien queens had been on the Other recognition functions of cuticular nest prior to worker emergence. These results hydrocarbons were consistent with the hypothesis that abdomi- nal stroking functions to apply the queen’s rec- In an early morphological and behavioral study, ognition pheromone to the nest. Van Hooser et Downing and Jeanne (1983) collected colonies of al. (2002) also observed stroking in workers, P. fuscatus at various phases of the colony cycle although workers stroked much less than queens. and dissected several exocrine glands, includ- Interestingly, Van Hooser et al. (2002) reported ing the Dufour’s gland. Downing and Jeanne that in high resolution video sequences of abdo- (1983) reported that the Dufour’s gland was men stroking, the point of contact between the most active in those females that were involved abdomen and the comb was at or near the open- in aggressive interactions and postulated that the ing to the sting chamber. A large exocrine gland gland might be involved in dominance interac- that opens into the sting chamber, the Dufour’s tions, including differential oophagy. In a later gland, has been hypothesized to be a source of study, Downing (1991) provided evidence that kin recognition pheromones in Polistes. the Dufour’s gland was the source of the cues Dani et al. (1996b) analyzed the cuticular by which queens of P. fuscatus could distinguish hydrocarbons and Dufour’s gland contents of their own eggs from those of subordinates. It is multiple-foundress colonies of P. dominulus. The not clear whether this egg recognition ability is authors found that the cuticle contained the same an example of individual recognition, dominance hydrocarbons as did the Dufour’s gland. How- recognition, or kin recognition. ever, linear alkanes were more abundant in the Sledge et al. (2001a) examined the rela- cuticle than in the Dufour’s gland while dime- tionship between ovarian activity and the pro- thyl-alkanes were more abundant in the Dufour’s portions of cuticular hydrocarbons in queens, gland. Dani et al. (1996b) also reported that the subordinate foundresses, and workers of P. cuticular hydrocarbons and Dufour’s gland con- dominulus. The authors reported that queens and tents were very similar in individuals as well as subordinates were similar in their proportions of among colony members. In a behavioral study, cuticular hydrocarbons immediately after nest Dani et al. (1996a) presented dead, Dufourec- foundation, but at the time of worker emergence, timized, hexane-washed females that had been they had diverged in their chemical profiles. treated with Dufour’s gland extracts to labora- The authors found that the amounts of several tory colonies of P. dominulus. If the donors of hydrocarbons (alkanes) characterized queens, the Dufour’s gland extracts were nestmates of subordinates, and workers. Interestingly, when the colony responding to the introduced dead the authors removed the queen from a colony, wasps, the dead wasps were accepted. However, the replacement queen developed a cuticular if the donors of the Dufour’s gland extracts were signature that was characteristic of the origi- non-nestmates of the colony responding to the nal queen. The authors suggested that cuticular introduced dead wasp, the dead wasps were hydrocarbons are used as cues of ovarian activity attacked. Dani et al. (1996a) concluded that the in P. dominulus. Although Sledge et al. (2001a) secretions of the Dufour’s gland, like epicuticu- have provided compelling evidence that queens, lar lipids, are involved in nestmate recognition. subordinates, and workers have different chemi- Although considerable evidence does sug- cal profiles, there is presently no evidence that gest that the Dufour’s gland is a source of nest/ females utilize these chemical differences for nestmate recognition pheromones, it may not recognition of social status, ovarian activity, or be the only source of these pheromones. Dani any other function. et al. (2003) recently reported that the main Steinmetz et al. (2003) recently investigated compounds found in the sternal gland secretions the origin and composition of the trail pherom- (sampled by contact SPME on the van der Vecht one of Vespula vulgaris and found that an artifi- glands and intersegmental membrane) were the cial trail made from an extract of cuticular lipids same long chain hydrocarbons found on the cuti- was as biologically active as a naturally laid cle and in the Dufour’s gland. trail. Furthermore, chemical analyses revealed ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 799 that natural trail extracts and cuticular extracts et al. 2000). Later in the colony cycle, emerging were very similar. Interestingly, Steinmetz et al. adults (P. dominulus and P. sulcifer) tolerate each (2003) found that trail pheromones of nestmates other, the parasitic queen, and the mixed brood. and non-nestmates were equally effective in elic- In order to understand the mechanism by iting trail following behavior. Thus, the trail which P. sulcifer queens successfully parasitize pheromones did not appear to be colony specific. P. dominulus, Turillazzi et al. (2000) used non- However, it could be that the trail pheromones destructive microextraction procedures to exam- of V. vulgaris are colony specific, and that in the ine the cuticular hydrocarbons of parasites, host context of trail following, acceptance thresholds females, and nests before usurpation and at vari- are more permissive resulting in wasps not mani- ous intervals after usurpation. The authors found festing a discrimination between their own trail that the parasite’s odor began to change within and that of another conspecific colony. If trail 90 min after usurpation and that the chemical pheromones and cuticular hydrocarbons are not profiles of the parasitic queen and host females colony-specific in V. vulgaris, one would assume were very similar within 3 days after usurpa- that V. vulgaris lacks the colony-specific odors tion. The parasitic queen’s odor was also more required for nestmate recognition. similar to the nest odor after usurpation than Finally, it has been suggested that cuticular before. Interestingly, the parasitic queen depos- hydrocarbons may be used to communicate age ited a compound (9,15-dimethyl C29) on the nest and sex. Layton et al. (1994), for example, pre- after usurpation that was unique to the parasite. sented evidence that the cuticular hydrocarbon Turillazzi et al. (2000) also found that the chemi- profiles of queens, workers, and males of P. met- cal profiles of host larvae were more similar to ricus are both distinctive and colony specific. those of the parasite than to host adults. Within two months after usurpation, parasitic larvae displayed a hydrocarbon profile almost identi- Recognition by Polistes invaded cal to P. dominulus larvae from unparasitized by obligate social parasites nests. The parasitic larvae lacked 9,15-dimethyl

C29 although the compound reappeared in the The literature on recognition in Polistes obligate parasitic pupae and parasitic reproductives that social parasitism is extensive, and a thorough emerged later. Turillazzi et al. (2000) postulated consideration of the literature would be more that, after removing the host queen, the parasitic appropriate for a review of social parasitism. queen utilized chemical disguise to enter the My limited discussion will focus on the recent nest. Furthermore, they hypothesized that the literature that examines the two best understood parasitic queen manipulated the odor of the nest, systems, P. dominulus and its obligate parasite, which changed the recognition template formed P. sulcifer, and P. biglumis and its obligate para- by subsequently emerging workers thereby site, P. atrimandibularis. The ability of social inducing them to accept the parasitic queen and parasites to gain access to a colony and then her brood. dupe workers into caring for their offspring is a Sledge et al. (2001b) collected parasitized first-class mystery. field colonies of P. dominulus and placed them in individual laboratory nestboxes. The authors removed parasites (P. sulcifer) and host females P. dominulus and its social parasite P. (P. dominulus) from nestboxes and presented sulcifer them to their own colony or other colonies. Using blind observations, Sledge et al. (2001b) found Turillazzi et al. (1990) reported that P. sulcifer that host females were significantly less aggres- queens either kill or evict queens of their host, P. sive toward parasites from their own nest than dominulus, and then begin stroking the nest with other nests. Similarly, host females were signifi- their abdomen. The parasitic queen also licks cantly less aggressive toward conspecific nest- the bodies of host females and initiates frequent mates than conspecific non-nestmates. Sledge et trophallactic interactions with them (Turillazzi al. (2001b) conducted similar experiments using 800 Gamboa • ANN. ZOOL. FENNICI Vol. 41 hexane-washed, dead wasps to which cuticular workers and reproductives of P. biglumis began extracts had been applied (lures). Host females to eclose, the chemical profiles of the host and were significantly more aggressive toward lures parasitic queens were indistinguishable. with parasite extracts from other nests than lures Bagnères et al. (1996) found that the repro- with parasite extracts from their own nest. The ductive offspring of P. atrimandibularis, which same results were found when host females were are produced late in the colony cycle, had a presented with lures containing extracts of non- chemical profile that was intermediate between nestmate conspecifics and nestmate conspecifics, that of the host and parasitic queen. The off- respectively. Host females were, in addition, spring of the host queen, however, retained their significantly more aggressive toward pieces of characteristic saturated hydrocarbon profile. cotton treated with foreign parasite extracts than Host workers took care of the emerging parasitic cotton treated with resident parasite extracts. reproductives despite the fact that the reproduc- Sledge et al. (2001b) also conducted a prin- tives had a different chemical profile from them. cipal components analysis and a stepwise discri- At the end of the colony cycle, the parasitic minant function analysis of the cuticular profiles queen displayed her preinvasion chemical profile of parasitic and host females. By three days that was rich in alkenes. The authors provided after usurpation, all but one parasitic female was two possible explanations for their findings. The correctly assigned to her colony. By 14 days, first involved a hormonal process in which the all parasitic females were assigned correctly. parasitic queen had the ability to control her Furthermore, the matching of the parasite’s odor metabolic pathway producing hydrocarbons so with the host’s odor after usurpation was due to that she could reproduce the chemical profile of changes in the parasite’s cuticular profile. Sledge the host queen. Alternatively, the parasitic queen et al. (2001b) concluded that their study pro- may have stopped producing hydrocarbons, vided the first compelling evidence that parasites which was accompanied by a degradation of her adopt the colony-specific odors of their hosts. chemical signature followed by the absorption of the host colony’s hydrocarbons. Lorenzi and Bagnères (2002) conducted a Polistes biglumis and its social parasite chemical study of P. biglumis and P. atrimandib- P. atrimandibularis ularis to determine if parasitic queens might use an “odorless strategy”, in addition to chemical Unlike P. sulcifer, the parasitic queen of P. atri- mimicry, to gain access to host colonies. They mandibularis unobtrusively enters a host colony found that the quantity of hydrocarbons in host by adopting a submissive posture and enduring females did not change over the colony cycle, attacks from the host queen (Cervo et al. 1990). but that the quantity of hydrocarbons in para- The host queen and the parasitic queen co-habit sitic females increased throughout the summer. the nest for most of the colony cycle although Female offspring of the parasitic queen (gynes), the parasitic queen typically remains on the which emerged near the end of the colony cycle, nest after the host queen leaves (Bagnères et al. had very low quantities of cuticular hydrocar- 1996). bons. Bagnères et al. (1996), in a revealing chemi- In interspecific comparisons, Lorenzi and cal study, reported that queens of P. biglumis and Bagnères (2002) found that early season para- P. atrimandibularis had distinct cuticular profiles sitic queens had significantly lower quantities before usurpation. The parasitic queen had a of hydrocarbons than host queens, but by the number of unsaturated hydrocarbons (alkenes) end of the season, the parasitic queens actually while the host queen had only saturated hydro- had a greater amount than did the host queens. carbons (alkanes). Soon after invasion, however, The authors postulated that P. atrimandibularis the alkenes disappeared from the cuticle of the queens enhanced their acceptance into host colo- parasite and some of the alkanes characteristic nies by having a hydrocarbon-deficient profile. of P. biglumis began to appear on the parasitic They further hypothesized that a hydrocarbon- queen. Later in the colony cycle, when the deficient profile might facilitate their entry into ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 801 other host nests. After establishing themselves learning of recognition odors impaired leading to on a host nest, queens of P. atrimandibularis a decrease in their recognition efficiency. often rob larvae and pupae from other colonies of P. biglumis and then feed these brood to their own larvae (Lorenzi & Bagnères 2002). The ecology of kin recognition In order to compare the recognition behav- iors of parasitized and non-parasitized workers This section includes discussions of certain of P. biglumis, Lorenzi (2003) presented live, aspects of the action component, i.e., the behav- cooled females to field colonies of P. biglumis. ioral response of an individual that has assessed Using blind behavioral observations, Lorenzi the similarity between its own template and the (2003) reported that workers from non-parasi- encountered phenotype (Reeve 1989, Gamboa tized colonies discriminated conspecific nest- et al. 1991a). It is obvious, however, that the mates from conspecific non-nestmates. Further- behavioral responses of wasps in various kin rec- more, workers were equally aggressive to con- ognition studies have been discussed throughout specific non-nestmates, parasitic queens (P. atri- this review. For a discussion of the action com- mandibularis), and gynes of P. atrimandibularis. ponent, see Liebert and Starks (2004). P. biglumis workers from parasitized colonies also discriminated conspecific nestmates from conspecific non-nestmates as well as their own Adaptiveness of recognition ability parasitic queen from a foreign parasitic queen. Workers from parasitized colonies were equally There have been a number of hypothesized tolerant of nestmate parasitic queens and conspe- advantages for nestmate recognition ability cific nestmates and equally intolerant of foreign in social wasps. These include: (1) prevent- parasitic queens and conspecific non-nestmates. ing usurpation by non-nestmate conspecifics When comparing the behavior of workers (e.g., Gamboa 1996), (2) avoiding colonies of from parasitized and non-parasitized colonies, close relatives as usurpation targets (Gamboa Lorenzi (2003) found that workers of parasit- et al. 1986a), (3) preferentially associating with ized colonies were significantly more tolerant of former nestmates in founding multiple-foundress non-nestmate conspecifics than were workers of colonies (Gamboa et al. 1986a), presumably to non-parasitized colonies. Surprisingly, workers enhance the kin components of associated foun- of parasitized colonies were significantly more dresses, (4) excluding non-nestmates from shar- aggressive toward nestmate conspecifics than ing colony resources such as nectar (Gamboa et were workers of non-parasitized colonies. Fur- al. 1992), (5) minimizing inbreeding (e.g., Ryan thermore, significantly more recognition errors & Gamboa 1986), and (6) preventing brood can- were made by workers from parasitized colo- nibalism by non-nestmates (see Kasuya et al. nies than workers from non-parasitized colonies. 1980). Both acceptance errors and rejection errors were One of the most important ecological pres- more frequent in parasitized colonies. sures favoring nestmate recognition in some Lorenzi (2003) concluded that the differ- North American species of Polistes is, almost ences in tolerance exhibited by parasitized and certainly, intraspecific usurpation. These pres- non-parasitized workers of P. biglumis could not sures can be intense. For example, in a high have been caused by differences in their accept- wasp density habitat, Gamboa (1978) reported ance thresholds. A more permissive acceptance that single-foundress colonies of P. metricus had threshold in parasitized P. biglumis workers as many as eight different queens (i.e., usurp- would result in greater tolerance of both conspe- ers) before the first workers emerged from the cific non-nestmates and conspecific nestmates. colony. Similarly, Michigan field colonies of P. In addition, parasitized workers should exhibit fuscatus had, on average, one usurpation attempt fewer rejection errors but more acceptance per day throughout most of the pre-worker phase errors. Lorenzi (2003) suggested that host work- of the colony cycle (Gamboa et al. 1992). Since ers of parasitized colonies might have had their P. fuscatus usurpers are typically unrelated to 802 Gamboa • ANN. ZOOL. FENNICI Vol. 41 the colonies they usurp (Klahn 1988), usurpers The evidence that non-parasitic species of might use their kin recognition abilities to avoid Polistes rob resources or cannibalize brood of usurping colonies of close relatives. However, other colonies is scanty. Kasuya et al. (1980) Gamboa et al. (1992) and others have reported reported intercolonial cannibalism of brood in that most usurpers are unmarked, indicating the Japanese paper wasp, P. chinensis. I am that they have migrated from other sites. Thus, unaware of any other reports of intercolonial it’s not clear whether usurpers avoid usurping resource or brood theft in temperate Polistes. closely related colonies by dispersing, by rec- Since several temperate species of Polistes have ognizing and avoiding closely related colonies, been observed extensively, including thousands or both. of hours of videography (personal data for P. A number of studies have reported that fuscatus), I believe it is likely that brood and cofoundresses of temperate Polistes are usually resource theft would have been reported if they former nestmates (e.g., West Eberhard 1969, were common occurrences. Klahn 1979, Strassmann 1983). Bornais et al. (1983) documented that foundresses of P. fus- catus preferentially built laboratory nests with Effect of context on recognition former nestmates when given an equal oppor- tunity to found nests with unrelated non-nest- In blind laboratory studies of P. fuscatus, Gamboa mates. These results suggest that P. fuscatus et al. (1991b) reported that resident females foundresses might utilize their nestmate recogni- were significantly more intolerant of unrelated tion ability to associate with former nestmates non-nestmates when they were encountered on in the field. However, temperate and tropical the nest than off the nest. This modulation of species of Polistes tend to be philopatric (Reeve tolerance in different contexts is almost certainly 1991), and thus spring associations of former adaptive since the negative fitness consequences nestmates may be due to philopatry. Nonethe- of encountering an unrelated wasp on one’s nest less, I have recorded foundress associations in P. is presumably greater than encountering an unre- fuscatus consisting of colony-marked nestmates lated wasp away from the nest. As discussed by that have dispersed a considerable distance from Gamboa (1996), there may be little or no advan- their natal nest site. These observations and the tage for displaying aggression toward non-nest- results of Bornais et al. (1983) suggest that both mates encountered away from the nest such as in nestmate recognition ability and philopatry likely the context of foraging. facilitate the association of former nestmates as Starks et al. (1998) examined the effect of cofoundresses. context on recognition in a laboratory study of P. The potential use of nestmate recognition dominulus. Using blind observations, the authors ability for mate choice has received little atten- observed behavioral interactions between dyads tion in social wasps. Ryan and Gamboa (1986) of nestmates, dyads of non-nestmates, and conducted blind laboratory observations of P. triads of two nestmates and a non-nestmate. The fuscatus and reported that males copulated sig- aggression between neighbor non-nestmates and nificantly less often with nestmates gynes than non-neighbor non-nestmates was also compared. non-nestmate gynes. Although these results are Starks et al. (1998) found that non-nestmate suggestive, the authors did not examine whether dyads were not significantly more aggressive the copulations resulted in sperm transfer or than nestmate dyads, but in triads, non-nestmate fertilization. Ross (1983) reported that virgin interactions were significantly more aggressive queens of Vespula maculifrons preferentially than those of nestmates. When these recogni- mated with nestmate males in the laboratory. tion trials were repeated with a fragment of The opposite results for P. fuscatus and V. macu- the nest present, significantly more aggression lifrons are difficult to explain. It is especially was observed in non-nestmates than nestmates difficult to understand why V. maculifrons would in both dyads and triads. Starks et al. (1998) exhibit mating preferences that are consistent also found that in triads, but not in dyads, with inbreeding. significantly more aggression was directed at ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 803 neighbor non-nestmates than non-neighbor non- between queens and workers in colony defense nestmates. These results demonstrated that con- against conspecific intruders. They reported text was modulating the recognition response to that queens were significantly more involved in conspecifics in P. dominulus. More specifically, colony defense than workers. In addition, queens the presence of a nestmate or a familiar nest were significantly less tolerant than workers of fragment, which indicated the proximity of a both returning nestmates and unrelated intruders. colony, affected tolerance in a way that is con- These results and others indicated that queens sistent with the fitness interests of the wasps. and gynes had a more restrictive acceptance Starks et al. (1998) concluded that his results threshold than workers. indicate that context causes adaptive shifts in Gamboa et al. (1991b) reasoned that the the acceptance threshold and thus supports the negative fitness consequences of accepting an optimal acceptance threshold model developed unrelated intruder into the colony are more nega- by Reeve (1989). tive for queens than for workers. Usurpers kill or Ruther et al. (2002) reported that workers of evict resident queens but allow resident workers Vespa crabro leaving the nest on foraging flights to remain on the nest. Workers of usurped colo- were much more aggressive to all classes of dead nies also have a higher probability of becoming wasps than workers returning to the nest. In an a replacement queen than workers of a colony explanation similar to that of Starks et al. (1998), headed by the original queen (Klahn 1988). Ruther et al. (2002) stated that the motivation to Thus, the more restrictive acceptance threshold defend the nest may be higher in departing work- of queens and the less restrictive acceptance ers due to their temporal closeness of contact threshold of workers appear to be consistent with with the chemical and physical clues of the nest. their fitness interests. The unexpected finding that colonies of P. fuscatus are not more aggressive early in the Caste-specific acceptance thresholds colony cycle may be due, in part, to the mech- anism that subserves tolerance. An extremely Gamboa et al. (1991b) investigated whether restrictive acceptance threshold early in the tolerance of conspecifics (nestmates and unre- colony cycle would indeed reduce the chances lated non-nestmates) changed adaptively over of accepting non-nestmates, but it would also the colony cycle in field colonies of P. fuscatus. increase the chances of rejecting nestmates. Since The authors had assumed that females would be the presence of nestmates early in the colony the most aggressive toward non-nestmates early cycle is known to greatly reduce the probability in the colony cycle when conspecific usurpation of successful usurpation (Gamboa 1978, Klahn pressures are severe (e.g., see Gamboa et al. 1988), the optimal setting of the acceptance 1992). When the tolerance of wasps was exam- threshold is likely constrained by the probabili- ined with blind behavioral assays, females did ties of accepting non-nestmates and rejecting the opposite of what had been predicted: females nestmates. Gamboa et al. (1991b) also reported were the most aggressive toward both nestmates that nectar sharing was extensive among late and non-nestmates late in the colony cycle. season nestmates and that nectar consumption Gamboa et al. (1991b) reported that when at this time likely affected winter survivorship, a compared with variances early in the colony time of very high mortality. Sharing nectar with cycle, the variances in tolerance toward nest- non-nestmates may have severe negative fitness mates and non-nestmates were significantly consequences, and thus gynes may be especially higher and lower, respectively, in late season aggressive toward conspecific intruders late in females. These results suggested that the accept- the season. In summary, the fitness interests of ance threshold of late season females (gynes) was queens and workers, as well as the mechanism more restrictive than that of early season females (cue similarity threshold property) that underlies (workers). Subsequently, Fishwild and Gamboa tolerance of conspecifics, appear to explain the (1992) conducted a blind field study of P. fusca- empirical results of Gamboa et al. (1991b) and tus to determine if there was a division of labor Fishwild and Gamboa (1992). 804 Gamboa • ANN. ZOOL. FENNICI Vol. 41

Future directions interest, may shed light on the adaptiveness and evolutionary origins of kin recognition in wasps. Despite the fact that the mechanism of recog- Finally, I believe that the study of the ecology nition has received considerable scrutiny, we of recognition will prove to be the most reward- know relatively little about certain aspects of ing and challenging area of future research. Our the perception component. For example, we understanding of the adaptiveness of kin recog- don’t know if wasps can update their learning nition, the ecological pressures favoring recogni- of recognition odors. One would assume that tion ability, the adaptive modulation of tolerance colony odors change over the colony cycle, in different contexts, and the evolution of kin either because sources of environmental odors recognition is rudimentary. It would be profitable (e.g., nectar, prey, or nesting materials) change to examine nest, brood, and conspecific neighbor or because genetic odors change. Genetic odors recognition in solitary wasps to determine if the might change if many colony members contrib- ancestors of social wasps had the precursors for ute to the comb odor and different adults are on evolving nestmate recognition. It may be that the comb in different phases of the colony cycle. the solitary ancestors of social wasps already We also don’t know if wasps can learn multiple possessed the perception and expression compo- colony odors, perhaps by forming multiple tem- nents of recognition. Indeed, Pfennig and Reeve plates or an expanded template that encompasses (1989, 1993) reported that the solitary cicada more than one colony’s odor. Such knowledge killer wasp can use genetically specified odors to might help us understand the recognition system recognize its nest soil and conspecific neighbors. of parasitized wasps (e.g., P. biglumis) that rec- Many of the questions that address the ecol- ognize both conspecific and parasitic nestmates. ogy of kin recognition will require the study of We also know virtually nothing about the tem- recognition in natural contexts, possibly supple- plate-phenotype matching process that results in mented with laboratory studies. Surprisingly few tolerance/acceptance of conspecifics. kin recognition studies of wasps, particularly As I discussed briefly earlier, kin recognition recent studies, have been field studies. Perhaps has been examined in only a small percentage of it is time to return to the field to learn why social social wasps and these have been mostly temper- wasps have the ability to recognize their relatives ate, primitively eusocial species. Thus, there is and how such a remarkable ability evolved. a great need to study kin/nestmate recognition in tropical and advanced eusocial species. Our understanding of the mechanism underlying kin References recognition in social wasps is based largely on studies of two species of Polistes, P. fuscatus and Bagnères, A. G., Lorenzi, M. C., Dusticier, G., Turillazzi, S. P. metricus. Although present evidence indicates & Clèment, J. L. 1996: Chemical usurpation of a nest by paper wasp parasites. — Science 272: 889–892. that the mechanism underlying recognition is the Bonavita-Cougourdan, A. G., Thèraulaz, G., Bagnères, A. G., same in various species, an insufficient number Roux, M., Pratte, M., Provost, E. & Clèment, J. L. 1991: of species have been examined to conclude that Cuticular hydrocarbons, social organization and ovarian the mechanism reported for Polistes is shared development in a polistine wasp: Polistes dominulus Christ. — Comp. Biochem. Physiol. B 100: 667–680. by all social wasps. It would be particularly Bornais, K. M., Larch, C. M., Gamboa, G. J. & Daily, R. worthwhile to study the mechanism underly- B. 1983: Nestmate discrimination among laboratory ing recognition in Ropalidia marginata and in overwintered foundresses of the paper wasp, Polistes stenogastrine wasps to determine if they con- fuscatus (Hymenoptera: Vespidae). — Can. Entomol. 115: 655–658. form to the Polistes model. Such studies should Breed, M. D., Stiller, T. M. & Moor, M. J. 1988: The ontog- utilize the same rigorous methodologies (i.e., eny of kin discrimination cues in the honey bee Apis blind behavioral assays and large numbers of mellifera. — Behav. Gen. 18: 439–448. colonies to prevent pseudoreplication) that have Brown, W. V., Spradbery, J. P. & Lacey, M. J. 1991: Changes in the cuticular hydrocarbon composition during devel- been used to decipher the recognition mecha- opment of the social wasp, Vespula germanica (F.) nism of Polistes wasps. Recognition studies of (Hymenoptera: Vespidae). — Comp. Biochem. Physiol. non-Polistes wasps, besides being of intrinsic B 99: 553–562. ANN. ZOOL. FENNICI Vol. 41 • Kin recognition in eusocial wasps 805

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