Ann. Zool. Fennici 43: 550–563 ISSN 0003-455X Helsinki 29 December 2006 © Finnish Zoological and Botanical Publishing Board 2006

The result of an arms race: the chemical strategies of social parasites

Maria Cristina Lorenzi

Department of and Human Biology, University of Turin, Via Accademia Albertina 13, I-10123 Turin, Italy (e-mail: [email protected])

Received 17 Dec. 2005, revised version received 27 Nov. 2006, accepted 2 May 2006

Lorenzi, M. C. 2006: The result of an arms race: the chemical strategies of Polistes social para- sites. — Ann. Zool. Fennici 43: 550–563.

The ability of social to discriminate between nestmates and aliens on the basis of scent has been the selective pressure favoring the evolution of chemical strategies to facilitate integration into host nests by social parasites, i.e., by organisms which rely on the nests and workers of others to rear their brood. As a result of the coevolu- tionary arms race, obligate social parasites of Polistes wasps have evolved complex mechanisms of mimicry. Social parasites mimic host chemical signatures at the level of species, colony, and possibly rank. Social parasites possess diluted recognition cues and apply compounds to the host nests that may result in host manipulation. The origin and evolutionary pathway to host/parasite chemical similarity is discussed by making comparisons with the tactics used by facultative social parasites, and with the develop- ment of the cuticular signature in free-living species.

Introduction to their parasitic lifestyle focus on deception, i.e., the ability to break the recognition code of When organisms of one species depend exclu- hosts to penetrate host colonies (Holldobler & sively on organisms of another species — as Wilson 1990). Such studies have documented occurs with parasites and their hosts — recipro- that social parasite odors match the odors of the cal selective pressures may result in the evolu- host species (Dettner & Liepert 1994, Lenoir et tion of matching traits. For example, this may al. 2001). The analysis of the chemical adapta- result in evolutionary trajectories where the tions of social parasites is fecund, and papers antagonists in the arms race are selected to have described the subtle mechanisms leading to exhibit progressively more complex adaptations host mimicry, which occur soon after host nest that facilitate , on one hand, and allow entrance or even before their first encounter. hosts to limit parasite exploitation on the other However, research has rarely focused on the (Davies et al. 1989, Thompson 1994, 2005). In origin and evolution of deceptive mechanisms social insects, the close coevolutionary relation- used by social parasites. To this aim, the social ships between social parasites and their hosts has wasps of the genus Polistes may represent a led parasites to evolve a number of mechanisms model system, mainly because the number of to overcome host barriers to colony invasion. species of obligate social parasites within the Most of the studies on social parasite adaptations genus is limited to only three, all of which share ANN. ZOOL. FENNICI Vol. 43 • The chemical strategies of Polistes social parasites 551 a similar parasitic lifestyle. As a result, the sce- whose chemical signatures match the learned nario of obligate parasitic strategies is relatively template and attack those which differ. simple in Polistes wasps. In contrast, facultative Recognition mechanisms are particularly social parasitism is widespread in the genus (see well-known in Polistes wasps, due to the studies Cervo & Dani 1996) and involves both intra- and by Gamboa and co-workers (reviewed in Gamboa inter-specific parasitic strategies, possibly cover- [1996, 2004]). Pfennig et al. (1983) documented ing a wide spectrum of integration mechanisms. abilities of Polistes wasps to develop recogni- The combined effect is that the Polistes genus tion within four hours after emergence, and that offers the possibility to identify potential inter- this process occurs correctly only if wasps spend mediate steps and prerequisites in the evolution their first hours on their nests or on fragments of the adaptations to parasitic life. of their nests. When newly emerged wasps per- The aim of this paper is to review the chemi- ceive nest paper odor they are later able to match cal adaptations of Polistes wasp social parasites, the learned template with the “odor” of the cue to treat them as adaptive parasitic traits, and bearer (Pfennig et al. 1983, Gamboa et al. 1986). to highlight their complexity (level of species, Thus the comb has a central role in the process colony, rank). I will analyze the mechanisms of learning recognition odors in Polistes wasps. involved in adopting cuticular signatures that As in other social insects, recognition cues in match those of hosts, the timing and schedule for Polistes paper wasps are complex species-spe- this process, and — by making comparisons with cific blends of hydrocarbons which cover the the tactics used by facultative social parasites cuticle (epicuticular hydrocarbons) and and with the ontogeny of chemical signature in the surface of the comb (Lorenzi et al. 1996, free-living Polistes species — investigate the Singer 1998). Epicuticular blends are similar possible origin and evolutionary pathways to within members of the same colony (Lorenzi et host/parasite chemical similarity. Throughout the al. 1996, Singer 1998), and between the comb paper, the focus will be on the parasite queens, and the resident wasps (Singer et al. 1998). In rather than on their brood, i.e. on those individu- social wasps, the epicuticular layer is gener- als that enter uninfested colonies, force hosts ally a blend of methylated, branched and linear into tolerating them and later into caring for hydrocarbons; their variations in quality usually their brood, get colony control, and live in host identify the species, their variations in quantity colonies for months. The knowledge of these within a fixed composition identify the colony to processes would permit the development of a which insects belong. scenario of the evolution of social parasitism in As a result, each colony (comb and adults) Polistes social wasps. has a unique chemical signature, which allows chemical nestmate/non-nestmate discrimination. In social wasps, recognition experiments have The barrier to invasion by aliens: shown that epicuticular hydrocarbons are suf- nestmate recognition in Polistes ficient to allow correct nestmates/non-nestmate free-living species discriminations (Dani et al. 1996, Lorenzi et al. 1997, Cervo et al. 1996, Ruther et al 1998; but Within social groups of , insect colonies also Lahav et al. [1999] in ants). are particularly well-demarcated social units. Thus research confirms that Polistes wasps Social insects usually make almost no mistakes have sophisticated recognition abilities. This is in distinguishing between colony members and the reason why it is surprising to observe in the non-members, and strictly limit the admittance wild that all intruder wasps are promptly rejected into their colonies to nestmates. This sophisti- from alien conspecific colonies, but social para- cated ability depends mainly on chemorecep- sites, which belong to alien species or colonies, tion. As a general rule, social insects learn their can infiltrate host colonies. Although most stud- colony odor rapidly after emergence and from ies on nestmate recognition have been accom- that moment they are able to recognize nestmates plished on only seven Polistes species (Gamboa from non-nestmates. They tolerate individuals 2004), there is no reason to think that the host 552 Lorenzi • ANN. ZOOL. FENNICI Vol. 43 species (P. dominulus, P. gallicus, P. biglumis, may coincide with the end of active colony P. nimphus and P. associus) of obligate social life (Cervo, 1990, Lorenzi et al. 1992). When parasites do not exhibit recognition abilities. And parasites have taken over host colonies, they indeed, evidence exists that two of the host spe- participate in colony life, i.e. they lay eggs and cies discriminate colony members from non-nest- inspect cells but they also interact with hosts, mates (P. biglumis: Lorenzi et al. [1997], Lorenzi receive food from them, and behave as dominant [2003]; P. dominulus: Dani et al [1996], Starks et individuals, without overt rebellion from hosts al. [1998], and indirectly, Sledge et al. [2001b]). (but see Dapporto et al. 2004). This indicates The contrast between the ability of paper that the parasites use long term strategies to wasps to discriminate between nestmates and trick hosts, and that adaptations to parasitic life aliens, and that of obligate parasites to deceive are even more complex than in parasitic birds host barriers with intruders, has stimulated much (Davies et al. 1989). Indeed, insect social para- research aimed at elucidating the adaptations of sites exhibit adaptations in both immature stages social parasites to their lifestyle. which develop in host nests (see Cervo 2006) and adult parasite females which enter host colo- nies and live there for months. Adult parasite The wasp social parasites females exhibit morphological traits (thickened cuticle and robust mandibles, for example) which Polistes wasps have three species of obligate favor overcoming the physical defense that hosts social parasites that share a distribution area oppose when parasites enter host nests (Cervo (Mediterranean and Caspian basin, Cervo 1994). However, in Polistes as in the other social [2006]), and an ancestor (Choudary et al. 1994), insect parasites, one of the most intricate, intrigu- but use different main hosts (Scheven, 1958, ing and most studied adaptations is the range Cervo & Dani 1996, Fanelli et al. 2001). In addi- of chemical strategies employed by parasites, tion, they have similar lifestyles. Parasite females which have the function of achieving integration enter the host nests after natural nest foundation with resident hosts, tricking hosts into tolerating by the host foundresses, usually before the emer- usurpers and into allocating colony resources to gence of the host brood (Scheven 1958, Cervo parasites. et al. 1990a, Turillazzi et al. 1990, Mead 1991, Zacchi 1995, Zacchi et al. 1996). However, Polistes parasites employ different — either non- Parasites intercept the host violent or aggressive — behavioral strategies for chemical code of recognition: usurpation (Cervo et al. 1990a, Cervo & Dani chemical strategies of integration 1996). After having defeated their hosts with a violent attack or with a sneaking strategy, para- Social parasites overcome species-specific differ- sites subdue subordinate females and subdue or ences in recognition cues by chemical adaptations chase out the legitimate resident queen. Each defined as mimicry or camouflage of host odor parasite queen controls a single host colony, (reviewed by Dettner & Liepert [1994], Lenoir possibly up to the end of the colony cycle. Once et al. [2001], Howard & Blomquist [2005]), i.e. they are established in the invaded colonies, by exhibiting a chemical resemblance with hosts. parasite “queens” begin egg-laying and domi- When the process of resemblance is attained, nate resident hosts. In Polistes obligate parasites, parasites exhibit epicuticular profiles with host- parasite eggs develop either into gynes or males: specific compounds in host-specific proportions, no parasite workers are produced. Thus, para- possibly passing through a blank state or chemi- sites rely on the comb and the workforce of host cal insignificance (Lenoir et al. 2001). species for reproduction. In contrast to bird brood parasites, which lay eggs in host nests and leave, insect social para- Mimicry at the level of species sites enter host colonies and establish themselves there for long periods, which, in Polistes wasps, In all three species of obligate parasites of ANN. ZOOL. FENNICI Vol. 43 • The chemical strategies of Polistes social parasites 553

Polistes wasps, parasites integrate within host host colony chemical signature (Sledge et al. colonies by chemically mimicking the hosts 2001b, Lorenzi et al. 2004a), so that each para- (here, mimicry is used as a general term for sitic female is accepted as a nestmate by host chemical resemblance, without referring to the residents, but is rejected in other colonies of the origin of the compounds involved, Dettner & same host species (Sledge et al. [2001b] for P. Liepert [1994]). Indeed, Bagnères et al. (1996) sulcifer; Lorenzi [2003] for P. atrimandibula- described that P. atrimandibularis females are ris, where recognition of parasites as nestmates chemically quite distinct from their P. biglumis was tested in the field). Besides Polistes social hosts before host nest invasion — at that time, parasites, mimicry of individual host colony’s their cuticular hydrocarbon blend contains para- odor was rarely documented (i.e. in the butterfly site-specific compounds, the alkenes, which are Maculinea rebeli, a social parasite of ants, Akino lacking in the hosts. After host nest invasion, et al. [1999]; and in a myrmecophilus spider, chemical analyses show that alkenes decrease Elgar & Allan [2004]) although it is probably a in the parasite epicuticular profiles and that the common feature in parasites that deceive hosts parasite cuticle becomes enriched with those whom exhibit nestmate recognition abilities. compounds abundant in the host chemical sig- nature. One month after invasion, when the host brood emerges, parasite females are chemically Mimicry at the level of rank indistinguishable from their hosts (Table 1). Similar patterns occur in the other Polistes Colony-specific matching of host cuticular odors social parasites. For instance, the matching proc- may not be all accomplished by social para- esses of epicuticular hydrocarbons in P. sul- sites. Dapporto et al. (2004) documented that cifer begin soon after entering the host nests P. sulcifer female parasites exhibit the chemical (Turillazzi et al. 2000) and P. semenowi matches profile of the alpha rather than that of the beta their host colonies 2–4 weeks after entering them female after invading P. dominulus nests (even (Lorenzi et al. 2004a). In all three cases, mim- when the alpha female was removed before icry is accurate; parasites lose, where present, parasite invasion). This deception, if it is such, is parasite-specific hydrocarbons and acquire host- complete, and host workers use only visual cues specific hydrocarbons (Table 1). to unmask their parasites. The “dominant cuticular profiles” may be used by subordinate foundresses and by workers Mimicry at the level of colony as indicators of egg-laying capacity of the domi- nant individuals (Sledge et al. 2001a). This may Polistes obligate social parasites also match the ensure the acceptance of an egg-layer by workers

Table 1. Chemical mimicry in Polistes obligate social parasites. ? = no data available; – individuals not present.

Similarity between parasite and hosts

Before Soon after host After co-inhabiting End of colony host nest nest invasion with hosts (host cycle (parasite invasion workers emerge) brood emerge)

P. atrimandibularis (1 Parasite females no no (but less yes no divergent than before) Parasite adult brood – – – no P. sulcifer (2 Parasite females no yes* yes ? P. semenowi (3 Parasite females no ? yes ?

* Host workers can emerge either before or soon after host nest invasion (Cervo 1990). Data from: 1) Bagnères et al. 1996; 2) Turillazzi et al. 2000; 3) Lorenzi et al. 2004. 554 Lorenzi • ANN. ZOOL. FENNICI Vol. 43

(Dapporto et al. 2004), as the removal of alpha scarcity in recognition cues could be the result of females causes competition over reproduction in specific selective pressures operating on social Polistes colonies (reviewed in Reeve 1991). The parasites. exhibition of an alpha profiles by parasites may Polistes atrimandibularis social parasites thus favor parasite control over host reproduc- have only about 20%–60% of the amount of tion (which occurs in Polistes, Cervo & Lorenzi epicuticular hydrocarbons of their P. biglumis [1996]). hosts for most of their life (Lorenzi & Bagnères However, evidence that subordinate foun- 2002). The deficiency in epicuticular hydrocar- dresses and workers use the alpha cuticular pro- bons with respect to hosts is extreme in parasite file as a signal is still lacking (Dapporto et al queens when they invade host nests (the amount 2004). If it is found, it will be further confirma- in parasites is 22% of the amount in their hosts, tion that acute discrimination abilities by hosts Table 2), but significant differences with the have created severe selection pressures for para- amount of their hosts are maintained during the sites that mimic hosts in the smallest details. whole colony cycle. Only at the end of colony cycle, when parasite queens stop egg laying and their similarity with the host vanishes (Bagnères Concealing identity via a blank state et al. 1996), does the quantity of parasite queens’ cuticular lipids increase (and largely exceeds that In the two species of Polistes social parasites of the hosts). At the end of colony cycle, when where specific analyses were done, usurping parasite brood emerge, parasite female adult off- females were poor in cuticular hydrocarbons spring (which will behave as parasite queens next with respect to their hosts (Lorenzi & Bagnères summer) were significantly poorer in epicuticular 2002, Lorenzi et al. 2004a). This peculiarity was lipids than their hosts. In this parasite species, the previously noted in ant social parasites (Lenoir scarcity of cuticular hydrocarbon is a consistent et al. 2001), but may be a general property property of adult females, with the only excep- of social parasites’ chemical signatures. Indeed, tion of old queens at the end of their life. authors often report that parasites possess cuticu- Data available for P. semenowi show a simi- lar chemical profiles “simpler” than those of their lar pattern (Lorenzi et al. 2004a) (Table 2). Para- hosts, but quantitative data on cuticular lipids are site females possessed only 40% of the amount not often available, or the sampling method do of epicuticular hydrocarbons of their P. dominu- not allow the quantification of the total cuticular lus hosts before entering host nests but had 60% lipids per insect (e.g. Turillazzi et al. 2000). two–four weeks after invasion. The critical role of epicuticular hydrocarbons During winter, parasites and hosts possibly is that of limiting dehydration (Gibbs 1998, hibernate in different habitats, as parasites per- Howard & Blomquist 2005). Social parasites form altitudinal migration and hibernate up in share the same habitat with their hosts, and even the mountains at elevations higher than their the same colony, and thus probably have similar hosts (Cervo & Dani 1996). Dehydration risks, physiological hydration requirements. Given that however, increase with altitudes. Thus overwin- social parasites possess lower quantities of epi- tered parasites, which abandon their high-moun- cuticular hydrocarbons than their hosts, parasite tain hibernacula and search for host nests in

Table 2. Variation in the total quantity of hydrocarbons in Polistes obligate social parasites.

Parasite species Mean amount of hydrocarbons (% with respect to hosts)

at host-nest invasion mid-colony cycle end of colony cycle

P. atrimandibularis * Parasite females 22% 58% 290% (old queens) 70% (adult female offspring) P. semenowi ** Parasite females 40% 60%

* with respect to P. biglumis (Lorenzi & Bagnères 2002). ** with respect to P. dominulus (Lorenzi et al. 2004a). ANN. ZOOL. FENNICI Vol. 43 • The chemical strategies of Polistes social parasites 555 lowland or at lower altitudes, should exhibit do not reject non-nestmate dead wasps when they even larger amount of cuticular hydrocarbons have had their hydrocarbons removed by solvent- than their hosts. Which selective pressures may washing (Dani et al. 1996, Lorenzi et al. 1997, have instead favored such a scarcity of cuticular Sledge et al. 2001). Here, the lack of recognition lipids? cues inhibits aggressive responses by residents. Possessing small amounts of epicuticular However, notwithstanding the minimum compounds might facilitate the acquisition of amount of cuticular compounds, parasite queens host odors after nest invasion (Lorenzi et al. are recognized and attacked by host residents at 2004b), if the cuticle more easily absorbs exog- nest invasion. Moreover, they exhibit the poten- enous compounds when the lipid layer is less tial dilution of recognition cues even after reach- abundant. Indeed, newly emerged wasps are ing complete mimicry with host colonies. These poor in cuticular lipids, and acquire hydrocar- two observations partially counter the hypothesis bons from the nest or the artificial environment that parasites conceal their identity by means of a in the first hours after emergence (Panek et al. dilution of recognition cues. Perhaps the amount 2001, Lorenzi et al. 2004b). In the same way, the of hydrocarbons required to be fully “chemi- total amount of hydrocarbons increases in para- cally invisible” is even smaller than the amount sites after the invasion of host colonies (Lorenzi possessed by parasites, and the quantity of rec- & Bagnères 2002, Lorenzi et al. 2004a), but it ognition cues they have only help parasites par- never reaches 100% of the amount detectable tially inhibit host aggressive reactions or to avoid in hosts (Table 2). Thus, it is possible that the detection. This hypothesis needs further analyses. scarcity of lipids favors the acquisition of com- It is possible that chemical mimicry operates with pounds from host nests in social Polistes para- a deficiency in recognition cues to limit identifi- sites, but available information does not fully cation of parasites as intruders into host colonies, support this hypothesis. thus facilitating the integration process and mini- The scarcity of cuticular lipids in social par- mizing fatal discrimination by hosts. asites may be used to conceal identity. This hypothesis was initially formulated to explain a similar phenomenon in social parasites of ants The timing of mimicry (Lenoir et al. 2001). The concept is that, as cutic- ular lipids constitute chemical signatures in rec- A few species-specific peculiarities may be found ognition processes, a dilution of such cues may in the pathways that lead Polistes obligate parasites render the identification of a cue bearer more dif- to match the chemical signature of their hosts. ficult. In the case of social parasites, a dilution of The epicuticular profile of P. semenowi recognition cues may favor acceptance by hosts. female parasites was not qualitatively much dif- In favor of this hypothesis is the observation that ferent from that of its P. dominulus hosts before young wasps (which possess poor quantities of host nest invasion (Lorenzi et al. 2004a). No hydrocarbons) have free access in alien colo- parasite-specific compounds were found in this nies soon after emergence, but are rejected later, species and parasites needed no more than fif- when the amount of their cuticular hydrocarbons teen days to match the profile of the individual has increased (Lorenzi et al. 1999, Panek et al. host colony that they invaded. 2001, Lorenzi et al. 2004b). Newly emerged Before P. sulcifer invaded nests of the host P. atrimandibularis females are not an excep- species P. dominulus, a single parasite-specific tion, and they are tolerated by host residents in compounds was found on their epicuticular alien parasitized nests during their first hours of layer, although large differences distinguished life (but rejected from un-parasitized nests, sug- the profiles of hosts and parasites. Specifically, gesting that, although poor in recognition cues, the odor of the parasite was simpler than that of they possessed parasite-specific compounds that the host, lacking a number of compounds that were unfamiliar to wasps from non-parasitized were present in the host profile. As early as 90 nests) (Lorenzi et al. 1999). Also in favor of this min after host-nest invasion, the first variation hypothesis, is the observation that resident wasps in the parasite epicuticular blends began, and the 556 Lorenzi • ANN. ZOOL. FENNICI Vol. 43 parasite cuticle became enriched in host-specific contain parasite-specific hydrocarbons (Bagnères compounds. Major changes were completed by et al. [1996], in large amounts in P. atrimandibu- 3 days after host nest invasion, and at that point, laris male brood, Lorenzi et al. [1996], Turillazzi the differences between parasite’s and host’s et al. [2000]), although the adult parasite’s brood odors were not larger than those between the inhabits host colonies and hosts tolerate them. hosts themselves (Turillazzi et al. 2000). Species-specific profiles probably favor mate In the field-collected samples of P. atri- searching and identification, but also make para- mandibularis, the profiles of the parasites were sites detectable in host colonies. qualitatively different from that of its P. biglu- In P. atrimandibularis, recognition tests mis hosts before host nest invasion and showed showed that newly emerged parasite females entire classes of parasite-specific compounds were accepted in any parasitized colony, but (Bagnères et al. 1996). Within 6 days after host were rejected in non-parasitized colonies of the nest invasion, the chemical signatures of the host species (Lorenzi et al. 1999), although parasites began to converge with those of the they were only accepted in their natal host colo- hosts: unsaturated hydrocarbons, which were the nies when they matured (Lorenzi 2003). Thus, parasites-specific compounds, disappeared from parasite offspring emerge with parasite-specific the cuticle and host-specific compounds began to labels (which cause rejection from non-parasit- be present. However, although changes occurred ized colonies), but without colony-specific labels soon after nest usurpations, the complete match- (allowing acceptance in any parasitized colonies) ing of the host recognition cues required about (Lorenzi et al. 1999) which they acquire later 30 days so that it was reached when host workers (Lorenzi 2003). However, the parasite brood is began to emerge from invaded nests (Bagnères et accepted in natal colonies notwithstanding the al. 1996, M. C. Lorenzi unpubl. data). fact that they possess parasite-specific hydrocar- Available data suggest that in the three spe- bons. These contradictory results can be under- cies of social parasites, the larger the difference stood because Polistes wasps learn their colony in the chemical profile of parasites and hosts, the odors from the nests. Parasites manipulate colony longer it takes parasites to match the recognition odors by supplementing the paper nest surface cues of their hosts. However, selective forces with parasite-specific compounds (Lorenzi & may modulate the speed of the host-matching Bagnères 1996, Lorenzi et al. 1996, Turillazzi et processes. In all three species of social parasites, al. 2000). When host workers emerge in parasit- mimicry is reached approximately when workers ized colonies, they experience the supplemented emerge from colonies (Table 1), suggesting that colony odor and later accept emerging parasite mimicry may be crucial to control host work- brood with parasite-specific labels, as well as ers. Host worker emergences can occur soon nestmate hosts with host-specific labels (Lorenzi after host nest invasion in P. semenowi and P. et al. 1996). Here, contamination of host colo- sulcifer, but a month later in P. atrimandibularis nies by parasite-specific cues mediates parasite (Cervo 1990, Lorenzi et al. 1992). At least in P. acceptance by hosts. atrimandibularis, parasites completely subdue host foundresses without matching their chemi- cal profiles (Bagnères et al. 1996). How are chemical adaptations attained?

Integration without mimicry (the peculiar Behavioral mechanisms case of old parasite queens and their adult brood) Specific behaviors are possibly involved in the variation of the lipid layer of the cuticle. Both Surprisingly, chemical resemblance with hosts P. sulcifer and P. semenowi parasites stroke their it is not the only chemical strategy that ensures abdomens on the nest surface soon after enter- acceptance by hosts. The chemical profiles of the ing the host nest (Turillazzi et al. [1990], Zacchi adult brood of P. atrimandibularis and P. sulcifer [1995], but see also Cervo & Dani [1996] for ANN. ZOOL. FENNICI Vol. 43 • The chemical strategies of Polistes social parasites 557 the same behavior in Polistes facultative para- wasps and used for rejection of aliens from home sites). In social wasps, nest paper is covered by colonies. The compounds acquired by parasites a hydrocarbon layer similar to that of resident after nest invasion are candidates to be perceived wasps (Lorenzi et al. 1996, Singer et al. 1998), by resident wasps and used as cues contributing so that physical contact between parasite cuticle to the acceptance of nestmates. As such, these and nest hydrocarbons may favor the transfer analyses are expected to clarify the recognition of odors between wasps and comb. In parasites process. However, variation in the chemical com- which quickly mimic host odors, like P. sul- position of parasite epicuticular hydrocarbons are cifer and P. semenowi, stroking may favor fast so large that it is difficult to distinguish between acquisition of host hydrocarbons from the comb them. For example, Lorenzi et al. (2004a) in P. surfaces. Indeed, stroking is rarely performed by semenowi listed the hydrocarbons acquired by P. atrimandibularis, where mimicry is achieved parasites 15–30 days after entrance in the nest of over an extended period. the host species P. dominulus. During this period, Besides stroking, social parasites lick their the parasites exhibit about 20 new hydrocar- hosts and eat eggs and immature host brood bons on their cuticles, all branched hydrocarbons (Turillazzi et al. 1990, Cervo et al. 1990b). These (except three linear alkanes) of 25 to 35 carbon behaviors may favor ingestion and accumulation each. As these hydrocarbons were already present of host hydrocarbons by the parasites, contribut- in the chemical signature of hosts before usurpa- ing — possibly with biochemical modification tion, they may have been acquired from hosts or within the parasites — to matching the chemical nests. Currently, the variation is too large to give signature of hosts. However, no studies have spe- clues to the nature of the chemicals involved in cifically addressed the problem of the origin of the identification process. The only consistent the compounds involved in the process of mim- finding is that all three parasite species become icry. The question remains open as to whether enriched in long-chain compounds after host nest Polistes social parasites acquire host-specific usurpation (P. atrimandibularis: Lorenzi & Bag- compounds passively from hosts, biosynthesize nères unpubl. data, P. semenowi: Lorenzi et al. them, or if both processes occur. A halt in the pro- 2004a; P. sulcifer: Dapporto et al. 2004) and duction of parasite-specific compounds, as well that high quantities of long-chain hydrocarbons as the absorption of colony-specific compounds, distinguish dominant P. dominulus females from were both supposed to occur in P. atrimand- workers (Dapporto et al. 2004). ibularis (Bagnères et al. 1996) and in P. sulcifer (Turillazzi et al. 2000, Sledge et al. 2001b). Other adaptations to parasitic life: manipulation of host recognition Hydrocarbons involved in the variation abilities? of the chemical signature In Polistes colonies parasitized by social para- The analysis of chemical variation in the hydro- sites, resident hosts may encounter nestmates carbon blend should theoretically help in the with two different recognition labels: namely, identification of the compounds (or classes of nestmate hosts and parasite queens with host- compounds) directly involved in the nestmate specific cuticular odors, and adult parasite brood recognition process. In honeybees only particular with parasite-specific cuticular odors. Recogni- hydrocarbons within the cuticular chemical pro- tion tasks of host workers may thus be more file are used as recognition cues (Breed 1998) and complex than in un-parasitized colonies. Indeed, the same may occur in social wasps (Espelie et al. less efficient recognition abilities in parasitized 1990, Dani et al. 2001, Lorenzi et al. 2004b). In nests were documented in P. biglumis colo- social parasites, the compounds which are present nies parasitized by P. atrimandibularis (Lorenzi on the parasites before usurpation, but disap- 2003). Similar results were obtained in ants, pear later (parasite-specific hydrocarbons), are where workers from polygynous ant colonies candidates for compounds perceived by resident were less discriminant towards aliens than work- 558 Lorenzi • ANN. ZOOL. FENNICI Vol. 43 ers from monogynous colonies (Sundström 1997, has been completed (Bagnères et al. 1996). This Starks et al. 1998, Vander Meer & Alonso 2002). variation occurs in adult individuals and indi- A tendency to make recognition errors may also cates that the chemical signatures of parasites are be seen in P. biglumis and P. nimphus colonies dynamic in both their qualitative and quantitative usurped by conspecific females (M. C. Lorenzi composition. Free-living adult Polistes wasps do et al. unpubl. data). Here, usurped workers do not change individual chemical signatures when not attack alien females significantly more often they leave the nest to forage or when they visit than their foundresses or usurpers. The common alien colonies to steal food (behavioral evidence variable in all those studies is the fact that nests documents that they are accepted into their col- were usurped or have multiple queens. It is pos- onies after performing these activities, M. C. sible that in such colonies two recognition labels Lorenzi [unpubl. data]). Moreover, free-living coexisted, thus making the process of learning of Polistes wasps maintain their species-specific recognition cues more complex and making the chemical signature even when they live in para- ability to discriminate between nestmates and sitized colonies with parasite brood or when their non-nestmates less efficient. nest paper is covered by unsaturated parasite-spe- Parasites and usurpers, as non-related colony cific compounds (chemical evidence, Bagnères et members, may benefit from impaired host rec- al. [1996], in P. biglumis). Indeed, adult Polistes ognition abilities (see Keller 1997) and might wasps of free-living species do not change their actively scramble recognition cues by deposit- cuticular patterns when they are experimen- ing appropriate chemicals on host combs. The tally exposed to hydrocarbons (behavioral and tainting of the nest surface with parasite-specific chemical evidence, Lorenzi et al. [2004b], in P. compounds was reported in P. atrimandibula- dominulus). In contrast, newly emerged wasps ris (Lorenzi et al. 1996, Lorenzi & Bagnères, of free-living species do change their epicuticu- 1996) and in P. sulcifer (Turillazzi et al. 2000). lar chemical composition drastically after emer- Here, parasite cuticles contained alkenes (in P. gence. Polistes dominulus females emerge with atrimandibularis) or 9,15-dimethyl C29 (in P. sul- a chemical profile which is poor in recognition cifer) before usurpations, and these compounds cues and within 3 days the quantity of cuticular were found on nest paper after usurpation (while hydrocarbons triples. Moreover, soon after emer- their amount decreased drastically in parasites). gence, the cuticle of young wasps absorbs hydro- In this case, the transfer of chemical cues may carbons when exposed to alien nests (Lorenzi et serve to remove or alter information about kin- al. 1999) or to natural quantities of hydrocarbons ship. Research on the variation of nest odor in (Lorenzi et al. 2004b). In this respect, the epi- parasitized and usurped colonies has rarely been cuticle of newly emerged wasps resembles that performed, but in many cases the experimental of mature parasites: both are poor in recognition procedures that document mimicry by parasites cues and both absorb hydrocarbons from the or usurpers cannot exclude the possibility that environment (for free-living species: Panek et al. parasites or usurpers do not deposit chemicals [2001], Lorenzi et al. [2004b]; for Polistes social on invaded nests. Indeed, studies that analyze parasites: Lorenzi & Bagnères [2002], Lorenzi et this aspect prove that invaded combs are con- al. [2004a]; for a review of the same phenomenon taminated by the intruders’ odors (Lorenzi & in ants: Lenoir et al. [2001]). Here, the ontogeny Bagnères 1996, Lorenzi et al. 1996, Turillazzi et of chemical signatures gives insight into the pos- al. 2000). sible origin of mimicry in social parasites.

A property of adult parasite Chemical strategies of facultative cuticular signature: plasticity social parasites: acquisition of host colony odor or marking host Polistes social parasites vary their chemical sig- combs? nature until it matches that of their hosts, but var- iation still occurs after the matching of the nests In Polistes wasps, the foundresses of the free- ANN. ZOOL. FENNICI Vol. 43 • The chemical strategies of Polistes social parasites 559 living species are able to behave as facultative 1994). In our view, the ability of P. nimphus to social parasites (Cervo & Dani 1996). In the field, usurp heterospecific colonies, the fact that they data on the success of usurpation by facultative possess morphological adaptations for parasitic parasites often indicates that colonies fail (low life (Cervo et al. 2004), and that the species usurped nest productivity: Klahn 1988, Cervo & shares a common ancestor with obligate para- Lorenzi 1996b, Cervo & Dani 1996) and instances sites, renders P. nimphus the most intriguing spe- where emerging host workers unmask the usurpers cies in which to study chemical adaptations to are reported. Worker rebellion is often observed in facultative parasitic reproductive options. usurped wasp colonies (worker/usurper aggres- In Polistes wasps, conspecific nest usurpa- sions: Klahn 1988, Lorenzi & Cervo 1995, Cervo tion occurs during the pre-worker phase (Reeve et al. 2004; usurper egg destruction by work- 1991), when foundresses are the only adults that ers: Makino 1988; workers with well-developed can contribute to the colony’s chemical signature. ovaries, Cervo & Turillazzi 1989, Dani et al. In Polistes colonies in the post-worker phase, all 1994; nest desertion by workers: Cervo & Lorenzi colony members may contribute to the produc- 1996b). Thus, in nature, workers do not always tion of colony odor (Turillazzi et al. 2000). accept usurpers. In contrast, reports on overt fail- Experimental data show that P. nimphus ures of colonies usurped by Polistes obligate par- usurpers employ different chemical integration asites is rare (but see Dapporto et al. 2004). This methods depending on the host species. P. nim- suggests that adaptations to the parasitic lifestyle phus females mimicked the odor of conspecific are efficient for the obligate parasites, but may be host colonies (as obligate social parasites do), less efficient for facultative parasites. Thus, inves- but were unable to mimic host odors when hosts tigating the mechanisms of infiltration displayed were heterospecifics. In this case, P. nimphus by facultative parasites may provide insight into usurpers marked heterospecific host nest with the first step along the evolutionary pathway to their own odor. These results suggest that P. efficient chemical mimicry. nimphus exhibit some parasite-like traits, such Until recently, no experiment had tested how as absorbing compounds on their cuticles, but facultative usurpers integrate within the host col- these traits are not as efficient as in obligate onies, but two hypotheses have been discussed in social parasites. The chemical signature of each the literature: facultative Polistes parasites were colony is probably unique in P. nimphus (no thought to apply their own odor to host combs or experiment has shown that, but see Turillazzi et to acquire host odors from host combs. al. [1998], Lorenzi & Caprio [2000]), but chemi- cal differences are usually larger between spe- cies than between conspecific colonies (Howard The specialized facultative parasite P. & Blomquist 2005). Results are consistent with nimphus the hypothesis that usurpers overcome colony- level differences in the chemical signature by Recently, Rita Cervo and I investigated the mimicking conspecific host-colony odor, but do chemical strategies used by usurpers entering not overcome species-specific differences when alien nests by employing an experimental pro- usurped nests belong to heterospecifics. cedure that can best be described as cross-foster- ing between colonies (Lorenzi et al. 2006). We examined P. nimphus, the only Polistes wasp The facultative parasite P. biglumis which is known to usurp both conspecific and heterospecific colonies successfully (Cervo et The ability to mimic the chemical signature al. 2004). While conspecific nest usurpation is of conspecifics by facultative Polistes parasites common in free-living Polistes wasps, heter- may not be universal. is a free- ospecific nest usurpation is rare (Cervo et al. living species where foundresses may behave 2004). In the phylogeny of obligate social para- as facultative usurpers by invading conspecific sites, P. nimphus belongs to the sister group of nests, but no evidence indicates that foundresses the obligate social parasites (Choudary et al. are able to usurp heterospecific nests. Results of 560 Lorenzi • ANN. ZOOL. FENNICI Vol. 43

Polistes wasps begins with the primitive chemi- cal strategy of facultative usurpers that taint conspecific host nests with their own odor (as documented in P. biglumis, M. C. Lorenzi et al. [unpubl. data]). Applying odors to host nests may allow the usurper to be accepted by its own brood, but not necessarily by host brood. At high conspecific parasitism pressures, the ability of host workers to unmask usurpers (and reproduce directly) will be favored. At each step in the evolution of chemical strategies of usurpation, the rebellion of host Fig. 1. Schematic diagram showing the hypothetical workers (which can kill usurpers or eliminate evolutionary steps of the chemical strategies employed their eggs; Klahn 1988, Makino 1988, Lorenzi by social parasites for integration into host colonies. In & Cervo 1995, Cervo et al. 2004) may represent this evolutionary pathway, expanded plasticity in the strong selective pressure favoring more efficient chemical signature is a specialized trait, favoring suc- chemical strategies of usurpation. At this point in cessful integration into those host nests that belong to species less phylogenetically related. The terms “mark” the evolution of chemical mimicry, usurpers that or “mimic” refer to the chemical strategy employed by contaminate their own cuticles with conspecific parasites (mark: parasites mark host nests with their host nest odors may have been selected for, as own odor; mimic: parasites mimic host colony odors). such usurpers were able to hide their true iden- tity from host workers. This occurs in P. nimphus usurpers invading conspecific nests (Lorenzi et recognition tests in conspecific usurped colo- al. 2006). nies indicate that in this species usurpers do not Usurpers can be foundresses which leave mimic conspecific host colony odor, but rather their hibernacula late in the spring or which have mark host nest with their own odors (M. C. lost their previous nests (Cervo & Dani 1996). It Lorenzi et al. unpubl. data). If similar tests in is important to note that females isolated from other free-living species give consistent results, nests and nestmates lose exogenous components the evolutionary scenario might be that faculta- of their odor (Gamboa et al. [1986] as cited in tive parasitic species are generally incapable of Gamboa [2004]). It will be interesting to deter- mimicking alien colonies and instead they mark mine if usurpers, which lack nests, are poor in them. The exception might be P. nimphus and exogenous compounds. If scarcity in recognition the other free-living species which successfully cues is a pre-requisite for the acquisition of chem- usurp both con- and hetero-specific colonies in icals from the environment (as suggested by the the wild: P. apachus (Snelling, 1952), P. met- properties of young wasps and mature parasites; ricus (Hunt & Gamboa 1978), P. canadensis see Lorenzi et al. 1999, Panek 2001, Lorenzi et (O’Donnell & Jeanne 1991) P. lanio (Giannotti al. 2004b, Lorenzi & Bagnères 2002, Lorenzi et 1995) and possibly P. dominulus (Cervo & Dani, al. 2004a), usurpers might possess poor cuticular [1996], R. Cervo pers. comm., but see Cervo et blends and absorb the exogenous components of al. [2004] for the success of usurpations). odors when exposed to alien nests. So far I have only discussed conspecific usur- pation; in this case chemical differences between Conclusions usurpers and host nests are small variations in relative proportions within the same qualitative Obligate parasitism evolved from intra-specific hydrocarbon composition. Within a population, parasitism via inter-specific parasitism (Davies conspecific usurpers only acquire colony-spe- et al. 1989, Taylor 1939, Cervo & Dani 1996, cific proportions of compounds that they already Cervo 2006). As shown in Fig. 1, a plausible have. The required degree of plasticity of the evolutionary pathway to chemical mimicry in chemical signature is limited. ANN. ZOOL. FENNICI Vol. 43 • The chemical strategies of Polistes social parasites 561

A further step in the evolution of social para- for a few of these steps. New observations will sitism is thought to be inter-specific parasitism. be necessary to develop a better understand- Here, P. nimphus may represent the next step. In ing of the evolution of the chemical strategies this species, usurpers successfully invade nests in this group. Increasing our understanding of of other species and laboratory simulations indi- the mechanisms of parasite infiltration into host cate that, in contrast to their ability to mimic colonies will contribute to a greater understand- conspecific host odors, P. nimphus usurpers only ing of co-evolutionary processes between social deposit their own odor on heterospecific nests. parasites and their hosts. Again, applying their own odor seems to be the easiest and the most accessible chemical strat- Acknowledgements egy, which is used when chemical differences are larger than between conspecific colonies. One step further in the arms race to trick I wish to thank Rita Cervo for her constructive comments on the manuscript, and F. Prendergast for linguistic revision. hosts, obligate Polistes parasites are consistently Helpful comments on the manuscript were made by Phil poor in recognition cues prior usurpation, and are Starks and two anonymous referees. able to match the host colony chemical signature after usurpation. This is accomplished even when hosts belong to different and distantly related spe- References cies. Here the chemical signature is so dynamic and plastic that parasites can halt the produc- Akino, T. Knapp, J. J. Thomas, J. A. & Elmes, G. W. 1999: tion of parasite-specific compounds and change Chemical mimicry and host specificità in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colo- drastically the composition of their profiles, not- nies. — Proc. R. Soc. Lond. B 266: 1419–1426. withstanding the large differences with the host Bagnères, A. G., Lorenzi, M. C., Dusticier, G., Turillazzi S. species. Obligate parasites probably have not lost & Clément, J. L. 1996: Chemical usurpation of a nest by the ability to apply compounds to host nests, but parasites. — Science 272: 889–892. rather employ both that tactic and their ability to Breed, M. D. 1998: Recognition pheromones of the honey bee. — Bioscience 48: 463–470. resemble hosts chemically to their advantage. Cervo, R. 1990: Il parassitismo sociale nei Polistes. — Ph.D. Although the data available at the moment thesis, University of Florence, Italy. suggests that the three species of obligate social Cervo, R. 1994: Morphological adaptation to the parasitic parasites employ very similar chemical strate- life in Polistes sulcifer and Polistes atrimandibularis gies, this is may not be true. P. atrimandibularis (, ). — Ethol. Ecol. Evol. Special Issue 3: 61–66. is a generalist and invades nests of four different Cervo, R. 2006: Polistes wasps and their social parasites: an host species which partially live in sympatry overview. — Ann. Zool. Fennici 43: 531–549. (Fanelli et al. 2001, Cervo 2006). Recent analy- Cervo, R. & Dani, F. R. 1996: Social parasitism and its evo- ses on microsatellite loci exclude the possibility lution in Polistes. — In: Turillazzi, S. & West-Eberhard, that these parasites form genetically distinct host M. J. (eds.), Natural history and the evolution of paper- wasps races (Fanelli et al. 2005). Thus an extreme plas- : 98–112. Oxford University Press, Oxford. Cervo, R. & Lorenzi, M. C. 1996a: Inhibition of host queen ticity of chemical mimicry mechanisms appears reproductive capacity by the obligate social parasite to be the only adaptation responsible for such Polistes atrimandibularis (Hymenoptera, Vespidae). diversity of hosts. Thus, it will be extremely — Ethology 102: 1042–1047. interesting to examine the chemical strategies Cervo, R. & Lorenzi, M. C. 1996b: Behaviour in usurpers that P. atrimandibularis employs with different and joiners of Polistes biglumis bimaculatus (Hymenop- tera Vespidae). — Insectes Soc. 43: 255–266. hosts, and to try to understand the ecology of Cervo, R. & Turillazzi, S. 1989: Next exchange experi- parasitism of this species. Here, the co-evolu- ments in Polistes gallicus (L.) (Hymenoptera, Vespidae). tionary arms race may be played between a para- — Ethol. Ecol. Evol. 1: 185–193. site and many different antagonist host species at Cervo, R., Dani, F. R. & Turillazzi, S. 1996: Nestmate recog- the same time. nition in three species of stenogastrine wasps (Hymenop- tera, Vespidae). — Behav. Ecol. Sociobiol. 39: 311–319. At the moment, such a scenario for the evo- Cervo, R., Lorenzi, M. C. & Turillazzi, S. 1990a: Nonag- lution of chemical mimicry is reasonable, but gressive usurpation of the nest of Polistes biglumis still needs confirmation, although clues exist bimaculatus by the social parasite Sulcopolistes atri- 562 Lorenzi • ANN. ZOOL. FENNICI Vol. 43

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