The chemical strategies used by Polistes nimphus social wasp usurpers (Hymenoptera Vespidae)

Polistes foundresses can behave as facultative social parasites when, instead of founding their own nest, they usurp colonies of the same or a different species and temporary use the host workforce to raise their own brood. Conspecific usurpation appears to be common among Polistes wasps, but nothing is known about the mechanisms that these facultative social parasites use to have themselves accepted within usurped colonies. Using behavioural tests, we studied the chemical strategies employed by females of Polistes nimphus when they behave as facultative social parasites in colonies of the same or of a different species. We hypothesized that usurpers would mark host nests with their own odours and/or acquire host nest odours in order to camouflage their real identity from host workers. Our results indicated that P. nimphus usurpers used different chemical strategies depending on host nest species: they acquired conspecific host odours but marked heterospecific host combs with their own odours.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 505–512.     

Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not?

Mimicry is one of the most conspicuous and puzzling phenomena in nature. The best-known examples come from insects and brood parasitic birds. Unfortunately, the term 'mimicry' is used indiscriminately and inconsistently in the brood parasitic literature despite the obvious fact that similarities of eggs, nestlings and adults of brood parasites to their hosts could result from many different processes (phylogenetic constraint, predation, intraspecific arms-races, vocal imitation, exploitation of pre-existing preferences, etc.). In this note I wish to plead for a more careful use of the term. I review various processes leading to a similarity between propagules (both eggs and nestlings) of brood parasites and their hosts and stress that: (1) mimetic and non-mimetic similarities should be differentiated, (2) a mere similarity of host and parasite propagules provides no evidence for mimicry, (3) mimicry is more usefully understood as a (coevolutionary) process rather than an appearance, and (4) mimicry terminology should reflect the process which led to mimetic similarity. Accepting the mimicry hypothesis requires both the experimental approach and rejection of alternative hypotheses explaining similarities of host and parasite propagules.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 69–78.     

Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution

Studies of avian brood parasite systems have typically investigated the mimicry of host eggs by specialist parasites. Yet, several examples of similarity between host and parasite chick appearance or begging calls suggest that the escalation of host–parasite arms races may also lead to visual or vocal mimicry at the nestling stage. Despite this, there have been no large-scale comparative studies of begging calls to test whether the similarity of host and parasite is greater than predicted by chance or phylogenetic distance within a geographically distinct species assemblage. Using a survey of the begging calls of all native forest passerines in New Zealand, we show that the begging call of the host-specialist shining cuckoo ( Chrysococcyx lucidus ) is most similar to that of its grey warbler ( Gerygone igata ) host compared to any of the other species, and that this is unlikely to have occurred by chance. Randomization tests revealed that the incorporation of the shining cuckoo's begging calls into our species-set consistently reduced the phylogenetic signal within cluster trees based on begging call similarity. By contrast, the removal of the grey warbler calls did not reduce the phylogenetic signal in the begging call similarity trees. These two results support a scenario in which coevolution of begging calls has not taken place: the begging call of the host retains its phylogenetic signal, whereas that of the parasite has changed to match that of its host.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 208–216.     

Pirate ants (Polyergus breviceps) and sympatric hosts (Formica occulta and Formica sp. cf. argentea): host specificity and coevolutionary dynamics

The pace and trajectory of coevolutionary arms races between parasites and their hosts are strongly influenced by the number of interacting species. In environments where a parasite has access to more than one host species, the parasite population may become divided in preference for a particular host. In the present study, we show that individual colonies of the pirate ant Polyergus breviceps differ in host preference during raiding, with each colony specializing on only one of two available Formica host species. Moreover, through genetic analyses, we show that the two hosts differ in their colony genetic structure. Formica occulta colonies were monogynous, whereas Formica  sp. cf. argentea colonies were polygynous and polydomous (colonies occupy multiple nest sites). This difference has important implications for coevolutionary dynamics in this system because raids against individual nests of polydomous colonies have less impact on overall host colony fitness than do attacks on intact colonies. We also used primers that we designed for four microsatellite loci isolated from P. breviceps to verify that colonies of this species, like other pirate ants, are comprised of simple families headed by one singly mated queen.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 565–572.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.     

Relationship Between Nest Predation Suffered by Hosts and Brown-Headed Cowbird Parasitism: A Comparative Study

There are at least four main hypotheses that may explain how the evolution of host selection by avian brood parasites could be linked to nest predation among their potential hosts. First, selection may have favoured parasite phenotypes discriminating among hosts on the basis of expected nest failure. Second, parasitized nests may be more easily detected by predators and extra costs of parasitism may accelerate the evolution of host defences. Third, selection may have favoured predator phenotypes avoiding parasitized nests because parasitism enhances nest defence. Fourth, female brood parasites may directly or indirectly induce host nesting failures in order to enhance future laying opportunities. We collected data on brood parasitism and nest failure due to predation to test these hypotheses in a comparative approach using North American passerines and their brood parasite, the brown-headed cowbird Molothrus ater. Under the hypotheses 1 or 3 we predicted brood parasitism to be negatively associated with nest predation across species, whereas this relation is expected to be positive if hypotheses 2 or 4 are true. We demonstrate that independent of host suitability, nest location, habitat type, length of the nestling period, body mass and similarity among species due to common ancestry, species experiencing relatively high levels of nest predation suffered lower levels of cowbird parasitism. Our results suggest a previously ignored role for nest predation suffered by hosts on the dynamics of the coevolutionary relationships between hosts and avian brood parasites. Co-ordinating editor: Dr. F. Stuefer     

Intra‐specific body size variation in Polistes paper wasps as a response to social parasite pressure

1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter‐adaptations to resist parasite attacks. 2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony. 3. We searched for host morphological traits related to fighting ability that could be considered counter‐adaptations. As a host–parasite co‐evolutionary arms race can only occur where the two lineages co‐exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure. 4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.     

The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution

Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.     

A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite

Avian brood parasites reduce the reproductive output of their hosts and thereby select for defence mechanisms such as ejection of parasitic eggs. Such defence mechanisms simultaneously select for counter-defences in brood parasites, causing a coevolutionary arms race. Although coevolutionary models assume that defences and counter-defences are genetically influenced, this has never been demonstrated for brood parasites. Here, we give strong evidence for genetic differences between ejector and nonejectors, which could allow the study of such host defence at the genetic level, as well as studies of maintenance of genetic variation in defences. Briefly, we found that magpies, that are the main host of the great spotted cuckoo in Europe, have alleles of one microsatellite locus (Ase64) that segregate between accepters and rejecters of experimental parasitic eggs. Furthermore, differences in ejection rate among host populations exploited by the brood parasite covaried significantly with the genetic distance for this locus.     

Behaviour in usurpers and late joiners ofPolistes biglumis bimaculatus (Hymenoptera,Vespidae)

Summary During the late pre-emergence phase, a foundress of the paper waspPolistes biglumis bimaculatus may be expelled by a conspecific female from her own nest (usurpation) or, less frequently, joined by another female of the same species (late association). The behaviour of femalePolistes biglumis bimaculatus, when usurping a conspecific colony or joining another foundress, is compared with that of foundresses on non-usurped colonies. The most conspicous difference is the intense abdomen stroking behaviour the usurper performs over the comb surface on the first days after usurpation. As observed in otherPolistes species, once usurpers and joiners arrive on a strange nest they will destroy most of the immature brood of the previous nest owner. Although host workers are not aggressive towards the intruder females, reproductive success of usurpers and joiners is low compared with that of legitimate foundresses. The same behaviours observed on usurped colonies are found in the obligate social parasites ofPolistes. These behaviours are therefore discussed in the context of the evolution of intra- and inter-specific parasitism.     

Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host–parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes ( Bucephala islandica ), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host–parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host–parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.     

Venom volatiles of the paper wasp social parasite <Emphasis Type="Italic">Polistes sulcifer</Emphasis> elicit intra-colonial aggression on the nest of the host species <Emphasis Type="Italic">Polistes dominulus</Emphasis>

Insect social parasites rely on host workers to rear and protect their own brood. To conquer a host colony, a parasite must overcome the defensive mechanisms of the host, often by exploiting its chemical communication system. A widespread strategy involves the production of specific allomones (the so-called “propaganda pheromones”) to facilitate the usurpation process by manipulating the defensive behavior of the host. Polistes sulcifer is the obligate and permanent social parasite of the congeneric paper wasp Polistes dominulus. In this study, we investigated if the venom volatiles, well known to be alarm pheromones in the host species, could be used by the parasite to manipulate the host defense. We thus performed laboratory bioassays, to evaluate the possible effect of the venom volatile compounds of the parasite on the host. Our results show that host colony members reacted to the venom volatiles extract of the parasite with an increase in intra-colonial aggression compared to the reaction induced by the venom volatiles extract of the host foundress. Besides, a re-analysis of previously published chemical data showed that the parasite venom volatiles profile differs from that of the host: the spiroacetals are absent, whilst the amides are very abundant in the parasite venom when compared with that of the host. Similar to other insect social parasites, Polistes wasp parasites might be able to increase their invasion success by using venom volatile pheromones to distract the host defenders.     

Differences in intestinal microbiota between avian brood parasites and their hosts

The intestinal microbiota determines the effectiveness of digestion in vertebrates, and is influenced by the external environment (mainly the diet), gut characteristics, and phylogeny. Avian brood-parasitic nestlings of the sub-family Cuculinae develop in nests of phylogenetically distant passerines and can be fed with the host diet. If the shaping of bacterial communities is dominated by phylogenetic constraints, and therefore the microbiota of parasitic nestlings differs from that of host nestlings, the energy and micronutrients that parasites and hosts obtain from a similar amount of food would be different. In this case, the bacterial communities of parasitic and host nestlings would have important consequences with respect to brood parasite development. By experimentally creating mixed broods of magpies ( Pica pica ) and great spotted cuckoos ( Clamator glandarius ), we investigated their cloacal microbiota using ribosomal intergenic spacer analysis. We found significant differences in bacterial assemblages of the parasitic and host nestlings, although none of the phylotypes were specific in either great spotted cuckoos or magpies. Cuckoos presented more complex communities, which could help the brood parasitic life style and allow the digestion of food provided by different potential hosts. Moreover, the intestinal morphology is different between the two species due to phylogenetic differences in the two taxa, which would influence the dissimilar bacterial assemblages. The detected differences in microbiota of great spotted cuckoo and magpie nestlings, which might occur in other brood parasite–host systems, may imply a lower digestion efficiency in parasites. Thus, the higher level requirements of cuckoo nestlings may be explained, at least in part, by cuckoos having a suboptimal bacterial community for processing the host diet.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 406–414.     

The social parasite wasp Polistes atrimandibularis does not form host races

Parasites that exploit the parental behaviour of several host species may be selected to form distinct host-specific genetic lineages. This process is well documented in bird brood parasites, but not in insect social parasites. Polistes atrimandibularis is the only paper-wasp social parasite known to exploit four host species. It does not form genetically distinct host races according to analyses based on microsatellite loci. Also, there were no size-matching between parasites and host species. Instead, P. atrimandibularis queens seemed to be successful as parasites in this population only when they originated from nests of P. dominulus, the largest species. The other host species are a sink for P. atrimandibularis since adult females emerging from those nests appear too small to usurp colonies themselves. Traits that may help P. atrimandibularis infiltrate multiple species may include its nonaggressive usurpation tactics and its ability to acquire host cuticular hydrocarbon recognition labels.     

Ectoparasite load is linked to ontogeny and cell-mediated immunity in an avian host system with pronounced hatching asynchrony

Several contrasting hypotheses have been proposed to account for host age-biased parasite distribution, with some of them suggesting a key role of ectoparasites in the evolution and maintenance of weight hierarchies within broods. We examined parasite distribution among individual hosts across the whole period of host exposure to the parasite in a host system that shows distinct within-brood differences in age and age-related mortality. By contrast to previous hypotheses, we found that the abundance of a haematophagous, mobile ectoparasite Carnus haemapterus on nestling European rollers ( Coracias garrulus ) was highest approximately during the mid-nestling stage of their host, coinciding with the inflection point of the host growth phase. Parasite load increased neither with absolute resource availability (i.e. body size), nor body condition index. By contrast to previous evidence, higher parasite load under natural conditions was associated with a stronger cell-mediated immune response. However, this association was moderated by low parasite densities, as well as a better brood body condition index. Overall, although we revealed remarkable host ontogenetic effects on parasite distribution, the present study suggests that a highly mobile ectoparasite generally prefers healthier hosts. We propose that, in host systems with a marked asynchrony of hatching and background mortality within the brood, parasites favour persistence rather than nutritional attractiveness of the host.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 463–473.     

Spring Usurpation Restlessness: A Wasp Social Parasite Adapts its Seasonal Activity to the Host Cycle

In animals, restlessness is a strategy to fulfil a goal within a narrow seasonal window when ecological and physiological constraints require the performance of certain fundamental events. Although restlessness can be expected in parasitic species that have their biological cycle similar to that of the host, no 'urge to parasitize' has thus far been demonstrated in any host-parasite pair. The paper wasp, Polistes sulcifer , is a social parasite that has lost the nest-building ability and marked by the absence of the worker caste; it depends on a congeneric host species to reproduce. Host colony usurpation is successful when it occurs in a well-defined seasonal window. The short time available for host-nest usurpation might lead to parasite restlessness that overlaps this period. Under controlled laboratory conditions, we demonstrated that the parasite females exhibit 'usurpation restlessness' during the period in which field usurpations occur. Additional experiments showed that both this period and laboratory temperature influence the parasite's 'urge to usurp'.     

Long‐term coevolution between avian brood parasites and their hosts

Coevolutionary theory predicts that the most common long‐term outcome of the relationships between brood parasites and their hosts should be coevolutionary cycles based on a dynamic change selecting the currently least‐defended host species, given that when well‐defended hosts are abandoned, hosts will be selected to decrease their defences as these are usually assumed to be costly. This is assumed to be the case also in brood parasite‐host systems. Here I examine the frequency of the three potential long‐term outcomes of brood parasite–host coevolution (coevolutionary cycles, lack of rejection, and successful resistance) in 182 host species. The results of simple exploratory comparisons show that coevolutionary cycles are very scarce while the lack of rejection and successful resistance, which are considered evolutionary enigmas, are much more frequent. I discuss these results considering (i) the importance of different host defences at all stages of the breeding cycle, (ii) the role of phenotypic plasticity in long‐term coevolution, and (iii) the evolutionary history of host selection. I suggest that in purely antagonistic coevolutionary interactions, such as those involving brood parasites and their hosts, that although cycles will exist during an intermediate phase of the interactions, the arms race will end with the extinction of the host or with the host acquiring successful resistance. As evolutionary time passes, this resistance will force brood parasites to use previously less suitable host species. Furthermore, I present a model that represents the long‐term trajectories and outcomes of coevolutionary interactions between brood parasites and their hosts with respect to the evolution of egg‐rejection defence. This model suggests that as an increasing number of species acquire successful resistance, other unparasitized host species become more profitable and their parasitism rate and the costs imposed by brood parasitism at the population level will increase, selecting for the evolution of host defences. This means that although acceptance is adaptive when the parasitism rate and the costs of parasitism are very low, this cannot be considered to represent an evolutionary equilibrium, as conventional theory has done to date, because it is not stable.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

Sulcopolistes atrimandibularis,Social Parasite and Predator of an Alpine Polistes (Hymenoptera,Vespidae)1

Sulcopolistes atrimandibularis Zimmermann is the obligate social parasite of Polistes biglumis bimaculatus Geoffry in Furcroy, a mountain species of paper wasp. Unlike all the other hymenopteran social parasites, the Sulcopolistes female obtains part of the food for her immature brood by plundering other nests of the host species. Parasite females can control more than one host nest: one of them (the nursery nest) she uses solely for reproduction purposes (from which the Sulcopolistes reproductives emerge) and others (supply nests) are used for exploiting the Polistes brood content. It is possible that this behaviour is an adaptation to the extremely short colonial cycle of the host.     

Usurpations and late associations in the solitary founding social wasp,Polistes biglumis bimaculatus (Hymenoptera: Vespidae)

One hundred twenty-five colonies of a population of the montane, haplometrotic, paper waspPolistes biglumis bimaculatus were marked for identification and then periodically surveyed during an entire summer period. This made it possible to record intraspecific nest usurpations (both single and multiple) and to observe associations between two females, defined here as late associations. Both usurpation and late association occurred primarily in the latter half of the preemergence period. Some evidence suggests that a foundress usurps a conspecific nest as a consequence of her own nest failure. After nest failure, usurpation and late association are the only available options for achieving reproductive success because, in the mountain habitat, the short summer does not allow for successful renesting. Late associations generally occurred earlier than usurpation. However, our evidence suggests that nest usurpation and late association may be the same phenomenon.