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.     

Coevolutionary interactions in a host–parasite system

Interactions between parasitic cuckoos and their hosts represent a classic example of coevolution, where adaptations in the parasite to exploit the host select for defences, which in turn select for new parasite adaptations. Current interactions between the two parties may be at an evolutionary equilibrium or, alternatively, a coevolutionary arms race may be taking place. By taking into account the effect of gene flow in 15 European magpie ( Pica pica ) populations, we studied the coevolutionary interactions with its brood parasite, the great spotted cuckoo ( Clamator glandarius ). Our results suggest that, in Europe, magpies and cuckoos are engaged in an ongoing coevolutionary process because, despite controlling for the large amounts of gene flow among different magpie populations, we still found a positive relationship between host defence (i.e. foreign egg recognition and rejection) and parasite selection pressure.     

Optimality of cell arrangement and rules of thumb of cell initiation in Polistes dominulus: a modeling approach

Possible adaptivity and mechanisms of nest construction of apaper wasp, Polistes dominulus, were studied by analyses ofnest structures and modeling. Results suggest that nests arenot built in agreement with the currently accepted "economymaterial usage" hypothesis because (1) the number of naturalforms is much less than expected under this criterion, and(2) there are non-optimal structures. Maximization of nest compactnessis a new hypothesis that better predicts natural structures.By examining the predictions of different building rules andcomparing model-generated structures to natural nests, we foundthat the nest structure provides sufficient (quantitative)information for governing the building process on (or verynear) the optimal path. We assume that non-optimal natural formsare the consequence of rules of thumb being used by wasps duringconstruction. A family of rules based on information on theage of cells was able to account for all natural forms, includingthe assumed optimal and non-optimal forms.     

Modelling the arms race in avian brood parasitism

In brood parasitism, interactions between a parasite and its host lead to a co-evolutionary process called an arms race, in which evolutionary progress on one side provokes a further response on the other side. The host evolves defensive means to reduce the impact of parasitism, while the parasite evolves means to counter the host's defence. To gain insights into the co-evolutionary process of the arms race, a model is developed and analysed, in which the host's defence and the parasite's counterdefence are assumed to be genetically determined. First, the effect of parasite counterdefence on host defence is analysed. I show that parasite counterdefence can critically affect the establishment of host defence, giving rise to three situations in the equilibrium state: The host shows (1) no defence, (2) an intermediate level of defence or (3) perfect defence. Based on these results, the evolution of parasite counterdefence is considered in connection with host defence. It is suggested that the parasite can evolve counterdefence to a certain degree, but once it has established counterdefence beyond this, the host gives up its defence against parasitism provided the defence entails some cost to perform. Dynamic aspects of selection pressure are crucial for these results. Based on these results, I propose a hypothetical evolutionary sequence in the arms race, along which interactions between the host and parasite proceed.     

Social parasitism of <Emphasis Type="Italic">Polistes dominulus</Emphasis> by <Emphasis Type="Italic">Polistes nimphus</Emphasis> (Hymenoptera,Vespidae)

Summary Interspecific facultative social parasitism is well known in ants and in bumble-bees, but it is rarer in wasps. This form of parasitism is traditionally considered to be an intermediate stage in the evolution of obligate interspecific parasitism, where the parasites are no longer able to nest alone. We report field and experimental observations of a newly discovered facultative parasitic relationship between two closely related free-living Polistes species: P. nimphus and P. dominulus. P. nimphus foundresses sometimes usurp the nests of the larger P. dominulus before worker emergence. The invading queen takes over the nest with abundant abdomen stroking on the nest surface and is accepted by workers if they emerge 6 or more days after usurpation. Morphometric comparisons show that the usurper species, though smaller than its victims, has morphological adaptations consisting of larger heads, mandibles and front femora relative to their body size that may give it an advantage during nest invasion. This strategy is likely to be taken only after the foundress loses her original nest because invading P. nimphus queens have lower reproductive success than they would have had on their own nest. Overall, we found that P. nimphus usurpers use strategies of invasion similar to those of two obligate parasites, suggesting that this may be an example of one of the pathways by which social parasitism evolved.Received 4 April 2003; revised 8 August 2003; accepted 14 September 2003.     

A quantitative threshold for nest-mate recognition in a paper social wasp

Nest-mate recognition is fundamental for protecting social insect colonies from intrusion threats such as predators or social parasites. The aggression of resident females towards intruders is mediated by their cuticular semiochemicals. A positive relation between the amount of cues and responses has been widely assumed and often taken for granted, even though direct tests have not been carried out. This hypothesis has important consequences, since it is the basis for the chemical insignificance strategy, the most common explanation for the reduction in the amount of semiochemicals occurring in many social parasites. Here we used the social wasp Polistes dominulus, a model species in animal communication studies and host of three social parasites, to test this hypothesis. We discovered that different amounts of cuticular hydrocarbons (CHC) of a foreign female evoke quantitatively different behavioural reactions in the resident foundress. The relation between CHC quantity and the elicited response supports the idea that a threshold exists in the chemical recognition system of this species. The chemical insignificance hypothesis thus holds in a host–parasite system of Polistes wasps, even though other explanations should not be discarded.     

Coevolution of a marine gastropod predator and its dangerous bivalve prey

The fossil record of the interaction between the predatory whelk Sinistrofulgur and its dangerous hard‐shelled bivalve prey Mercenaria in the Plio‐Pleistocene of Florida was examined to evaluate the hypothesis that coevolution was a major driving force shaping the species interaction. Whelks use their shell lip to chip open the shell of their prey, often resulting in breakage to their own shells, as well as to their prey. Mercenaria evolved a larger shell in response to an intensifying level of whelk predation. Reciprocally, an increase in attack success (ratio of successful to unsuccessful attacks) and degree of stereotypy of attack position by the predator suggest reciprocal adaptation by Sinistrofulgur to increase efficiency in exploiting hard‐shelled prey. A decrease in prey effectiveness (ratio of unsuccessful to total whelk predation attempts) and an increase in the minimum boundary of a size refuge from whelk predation for Mercenaria may indicate that predator adaptation has outpaced prey antipredatory adaptation. Evolutionary size increase in Sinistrofulgur most likely occurred in response to prey adaptation to decrease the likelihood of feeding‐induced shell breakage and unsuccessful predation when encounters with damage‐inducing prey occur, coupled with (or reinforced by) an evolutionary response to the whelk's own predators. Predator adaptation to Mercenaria best explains temporal changes in whelk behaviour to decrease performance loss (shell breakage) associated with feeding on hard‐shelled prey; this behavioural change limits attacks on prey to when the whelk's shell lip is thickest and most resistant to breakage. Despite evidence of reciprocal adaptation between predator and prey, the contribution of Mercenaria to Sinistrofulgur evolution is likely only a component of the predator's response to dangerous bivalve prey. This study highlights the importance of understanding the interactions among several species in order to provide the appropriate context to test evolutionary hypotheses about any specific pair of species. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80 , 409–436.     

Brood parasitism selects for no defence in a cuckoo host

In coevolutionary arms races, like between cuckoos and their hosts, it is easy to understand why the host is under selection favouring anti-parasitism behaviour, such as egg rejection, which can lead to parasites evolving remarkable adaptations to ‘trick’ their host, such as mimetic eggs. But what about cases where the cuckoo egg is not mimetic and where the host does not act against it? Classically, such apparently non-adaptive behaviour is put down to evolutionary lag: given enough time, egg mimicry and parasite avoidance strategies will evolve. An alternative is that absence of egg mimicry and of anti-parasite behaviour is stable. Such stability is at first sight highly paradoxical. I show, using both field and experimental data to parametrize a simulation model, that the absence of defence behaviour by Cape bulbuls (Pycnonotus capensis) against parasitic eggs of the Jacobin cuckoo (Clamator jacobinus) is optimal behaviour. The cuckoo has evolved massive eggs (double the size of bulbul eggs) with thick shells, making it very hard or impossible for the host to eject the cuckoo egg. The host could still avoid brood parasitism by nest desertion. However, higher predation and parasitism risks later in the season makes desertion more costly than accepting the cuckoo egg, a strategy aided by the fact that many cuckoo eggs are incorrectly timed, so do not hatch in time and hence do not reduce host fitness to zero. Selection will therefore prevent the continuation of any coevolutionary arms race. Non-mimetic eggs and absence of defence strategies against cuckoo eggs will be the stable, if at first sight paradoxical, result.     

Plant-Herbivore Interactions and Theory of Coevolution1

Abstract We consider a mathematical model for the coevolution of a plant's defense against herbivores and the herbivore's ability to exploit the plant. The result of coevolution is predicted using the phase portrait of trait value dynamics and contour plots of fitnesses. The following results are derived: (1) The fitnesses of both plant and herbivore are higher at an “armless” state in which both plant and herbivore invest a minimum amount of energy and/or resources in defense and feeding respectively, than at the coevolutionarily stable state (CSS); (2) Perpetual increase in the trait values of both species may occur when the marginal costs of defense and feeding abilities decrease as these abilities increase; (3) If the marginal costs of defense and feeding abilities increase as the abilities increase, there is a coevolutionary equilibrium with finite trait values; (4) There may be more than one coevolutionarily stable state (CSS).     

Geographical variation in host–ant specificity of the parasitic butterfly Maculinea alcon in Denmark

Abstract  1. Maculinea alcon uses three different species of Myrmica host ants along a north–south gradient in Europe. Based on this geographical variation in host ant use, Elmes et al . (1994) suggested that M. alcon might consist of three or more cryptic species or host races, each using a single and different host-ant species.
2. Population-specific differences in allozyme genotypes of M. alcon in Denmark ( Gadeberg & Boomsma, 1997 ) have suggested that genetically differentiated forms may occur in a gradient across Denmark, possibly in relation to the use of different host ants.
3. It was found that two host-ant species are indeed used as hosts in Denmark, but not in a clear-cut north–south gradient. Furthermore, specificity was not complete for many M. alcon populations. Of five populations investigated in detail, one used primarily M. rubra as a host, another exclusively used M. ruginodis , while the other three populations used both ant species. No population in Denmark used M. scabrinodis as a host, although this species was present in the habitat and is known to be a host in central and southern Europe.
4. In terms of number of parasites per nest and number of nests parasitised, M. rubra seems to be a more suitable host in populations where two host species are used simultaneously. Host-ant species has an influence on caterpillar size but this varies geographically. Analyses of pupae did not, however, show size differences between M. alcon raised in M. rubra and M. ruginodis nests.
5. The geographical mosaic of host specificity and demography of M. alcon in Denmark probably reflects the co-evolution of M. alcon with two alternative host species. This system therefore provides an interesting opportunity for studying details of the evolution of parasite specificity and the dynamics of host-race formation.     

Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism

In a coevolutionary arms race between an interspecific broodparasite and its host species, both are expected to evolveadaptations and counteradaptations. We studied egg discriminationin the Australian warbler (Acrocephalus australis). This speciesis currently not significantly parasitized by the seven speciesof cuckoo for which it is a suitable host. However, experimentalbrood parasitism in the warbler revealed a fine tuned egg discriminationresponse towards non-mimetic and conspecific eggs, the firstsuch evidence in an Australian passerine: (1) non-mimetic eggswere significantly more often rejected than conspecific eggs;(2) only non-mimetic dummy eggs were rejected selectively,whereas rejection of conspecific eggs entailed a rejectioncost; (3) replacement of a host's egg with a conspecific eggduring egg laying resulted in a significantly higher rejectionrate than after the day of clutch completion; (4) by contrast,rejection rate after addition of a conspecific egg was independentof nest stage; (5) conspecific eggs introduced into a clutchduring the egg laying period led to a significantly highernest desertion rate and a lower egg ejection rate than afterthe day of clutch completion; and (6) addition of a conspecificegg led to egg ejection while egg replacement with a conspecificegg led to nest desertion. The fact that this species respondsdifferentially toward different modes of artificial parasitismsuggests that its egg discrimination has evolved to minimizethe costs of rejection and parasitism. The ability to rejecthighly mimetic conspecific eggs may explain the current paucityof brood parasitism in this species. The significance of thisfor brood parasite-host coevolution is discussed.     

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

Distribution of social wasps (Hymenoptera: Vespidae) in New Zealand in 1987

Abstract

More than 50 000 social wasps (Hymenoptera: Vespidae) were collected between March and August 1987 from throughout New Zealand. The most widespread species is the German wasp (Vespula germanica). The common wasp (V. vulgaris) has colonised about half the country and appears to be still spreading. It tends to appear in urban areas first, presumably because it is transported there with people and/or their belongings. The Asian paper wasp (Polistes chinensis) and Australian paper wasp (P. humilis), are confined to the northern half of the North Island, but the former species is spreading south.     

Nest recognition in neighboring colonies: a comparison of two European species of Polistes wasps (P. dominulus and P. nimphus, Hymenoptera: Vespidae)

The ability of two species of Polistes wasps to distinguish their own from nearby nests was tested, following the procedure used by Espelie et al. Our experiments demonstrated that, in the laboratory, females of Polistes dominulus and Polistes nimphus preferentially selected their own nests rather than nearby nests. We also evaluated the role of odor cues in nest recognition by washing nests in hexane to remove the apolar solvent-soluble components of nest odor. Although P. nimphus females continued to discriminate nests even after washing, P. dominulus individuals failed to discriminate between their own and a foreign neighboring nest. In both species, wasps were able to recognize their own nests when nest extracts were subsequently reapplied to the nest surface. These results indicate that P. dominulus wasps recognize their nests through perception of nest odor. The ability of P. nimphus wasps to distinguish their own nests even after presumed removal of the nest odor is discussed. Received: January 27, 2000 / Accepted: May 22, 2000     

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.     

Not everything is everywhere: the distance decay of similarity in a marine host–parasite system

Aim We test the similarity–distance decay hypothesis on a marine host–parasite system, inferring the relationships from abundance data gathered at the lowest scale of parasite community organization (i.e. that of the individual host). Location Twenty‐two seasonal samples of the bogue Boops boops (Teleostei: Sparidae) were collected at seven localities along a coastal positional gradient from the northern North‐East Atlantic to the northern Mediterranean coast of Spain. Methods We used our own, taxonomically consistent, data on parasite communities. The variations in parasite composition and structure with geographical and regional distance were examined at two spatial scales, namely local parasite faunas and component communities, using both presence–absence (neighbour joining distance) and abundance (Mahalanobis distance) data. The influence of geographical and regional distance on faunal/community divergence was assessed through the permutation of distance matrices. Results Our results revealed that: (1) geographical and regional distances do not affect the species composition in the system under study at the higher scales; (2) geographical distance between localities contributes significantly to the decay of similarity estimated from parasite abundance at the lowest scale (i.e. the individual host); (3) the structured spatial patterns are consistent in time but not across seasons; and (4) a restricted clade of species (the ‘core’ species of the bogue parasite fauna) contributes substantially to the observed patterns of both community homogenization and differentiation owing to the strong relationship between local abundance and regional distribution of species. Main conclusions The main factors that tend to homogenize the composition of parasite communities of bogue at higher regional scales are related to the dispersal of parasite colonizers across host populations, which we denote as horizontal neighbourhood colonization. In contrast, the spatial structure detectable in quantitative comparisons only, is related to a vertical neighbourhood colonization associated with larval dispersal on a local level. The stronger decline with distance in the spatial synchrony of the assemblages of the ‘core’ species indicates a close‐echoing environmental synchrony that declines with distance. Our results emphasize the importance of the parasite supracommunity (i.e. parasites that exploit all hosts in the ecosystem) to the decay of similarity with distance.     

Unique physiology of host–parasite interactions in microsporidia infections

Microsporidia are intracellular parasites of all major animal lineages and have a described diversity of over 1200 species and an actual diversity that is estimated to be much higher. They are important pathogens of mammals, and are now one of the most common infections among immunocompromised humans. Although related to fungi, microsporidia are atypical in genomic biology, cell structure and infection mechanism. Host cell infection involves the rapid expulsion of a polar tube from a dormant spore to pierce the host cell membrane and allow the direct transfer of the spore contents into the host cell cytoplasm. This intimate relationship between parasite and host is unique. It allows the microsporidia to be highly exploitative of the host cell environment and cause such diverse effects as the induction of hypertrophied cells to harbour prolific spore development, host sex ratio distortion and host cell organelle and microtubule reorganization. Genome sequencing has revealed that microsporidia have achieved this high level of parasite sophistication with radically reduced proteomes and with many typical eukaryotic pathways pared-down to what appear to be minimal functional units. These traits make microsporidia intriguing model systems for understanding the extremes of reductive parasite evolution and host cell manipulation.