Chemical mimicry and host specificity in the butterfly Maculinea rebeli,a social parasite of Myrmica ant colonies

Although it has always been assumed that chemical mimicry and camouflage play a major role in the penetration of ant societies by social parasites, this paper provides the first direct evidence for such a mechanism between the larvae of the parasitic butterfly Maculinea rebeli and its ant host Myrmica schencki. In the wild, freshly moulted fourth-instar caterpillars, which have no previous contact with ants, appear to be recognized as ant larvae by foraging Myrmica workers, which return them to their nest brood chambers. Three hypotheses concerning the mechanism controlling this behaviour were tested: (i) the caterpillars produce surface chemicals that allow them to be treated as ant larvae; (ii) mimetic compounds would include hydrocarbons similar to those employed by Myrmica to recognize conspecifics and brood; and (iii) the caterpillars'' secretions would more closely mimic the profile of their main host in the wild, M. schencki, than that of other species of Myrmica. Results of behavioural bioassays and chemical analyses confirmed all three hypotheses, and explained the high degree of host specificity found in this type of highly specialized myrmecophile. Furthermore, although caterpillars biosynthesized many of the recognition pheromones of their host species (chemical mimicry), they later acquired additional hydrocarbons within the ant nest (chemical camouflage), making them near-perfect mimics of their individual host colony''s odour.     

Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature

Social parasites are able to exploit their host's communication code and achieve social integration. For colony foundation, a newly mated slave-making ant queen must usurp a host colony. The parasite's brood is cared for by the hosts and newly eclosed slave-making workers integrate to form a mixed ant colony. To elucidate the social integration strategy of the slave-making workers, Polyergus rufescens, behavioural and chemical analyses were carried out. Cocoons of P. rufescens were introduced into subcolonies of four potential host species: Formica subgenus Serviformica (Formica cunicularia and F. rufibarbis, usual host species; F. gagates, rare host; F. selysi, non-natural host). Slave-making broods were cared for and newly emerged workers showed several social interactions with adult Formica. We recorded the occurrence of abdominal trophallaxis, in which P. rufescens, the parasite, was the donor. Social integration of P. rufescens workers into host colonies appears to rely on the ability of the parasite to modify its cuticular hydrocarbon profile to match that of the rearing species. To study the specific P. rufescens chemical profile, newly emerged callows were reared in isolation from the mother colony (without any contact with adult ants). The isolated P. rufescens workers exhibited a chemical profile closely matching that of the primary host species, indicating the occurrence of local host adaptation in the slave-maker population. However, the high flexibility in the ontogeny of the parasite's chemical signature could allow for host switching.     

Scaling in nests of a social wasp: a property of the social group

The numbers of brood cells in nests built by founding swarms of the Neotropical social wasp Polybia occidentalis closely correlate with the numbers of wasps in the swarms. We analyzed nests of different sizes to determine how they scale with respect to the allocation of brood cells among combs. Three patterns were evident: compared to smaller nests, larger nests have (1) more combs and (2) larger combs; and (3) among nests containing the same number of combs, the last two combs diverge in relative size as nest size increases. Taken together, these results suggest that members of a swarm somehow "know" the size of the swarm they are in. This information feeds back to individual builders, which quantitatively modulate their responses to stigmergic cues in ways that result in the nest-size-scaled allocation of brood cells among combs. The patterns also suggest that swarms fine-tune the final size of their nests by making corrections as they build.     

Evidence for intersexual chemical mimicry in a dioecious plant

The dioecious Mediterranean fig, Ficus carica, displays a unique phenology in which males sometimes bloom synchronously with females (in summer), and sometimes not (in spring). Ficus carica is engaged in an obligatory mutualism with a specific pollinating wasp, which reproduces only within figs, localising them by their specific scents. We show that scents emitted by male figs show seasonal variation within individual trees. Scents of summer male figs resemble those of the co-flowering females, and are different from those of the same male trees in spring, when female figs are absent. These differences hold even if only compounds electrophysiologically active for pollinators are considered. The similar scents of summer males and females may explain why the rewardless females are still pollinated. These results offer a tractable model for future studies of intersexual chemical mimicry in mutualistic pollination interactions.     

Behaviour of female common cuckoos, Cuculus canorus, in the vicinity of host nests before and during egg laying: a radiotelemetry study

We radiotracked 13 common cuckoo females in the southeastern part of the Czech Republic. Seven females laid eggs in the nests of reed warblers, Acrocephalus scirpaceus, sedge warblers, A. schoenobaenus, and marsh warblers, A. palustris. We observed 53 nest visits, of which 26 involved egg laying. Cuckoos spent significantly more time within 50 m of the host nest on the laying day than on the 5 prelaying days. The vantage point used when parasitizing or visiting a nest was on average four times further from the nest than the closest possible vantage point, but there was a positive correlation between these two distances. Cuckoos spent on average 20 min observing host nests from their vantage points before they visited a nest. Comparison of cuckoos' visits to host nests with and without egg laying revealed no significant differences in the duration of visits or in other measures of behaviour. There was significant variation in behaviour between cuckoos, particularly in the time of day when eggs were laid in host nests. This variation can be attributed to the strong, but not absolute, host and habitat specificity of individuals. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Ecology of a bolas spider,Mastophora hutchinsoni: phenology,hunting tactics,and evidence for aggressive chemical mimicry

Summary Bolas spiders are relatively rare members of the large family known as orb weavers. Instead of using a typical web to capture prey, late-stadia and adult female bolas spiders swing a droplet of adhesive on a thread at flying insects. Mastophora hutchinsoni (Araneae: Araneidae) is one of five Mastophora species known from the United States and occurs over much of eastern North America. It is univoltine in Kentucky and overwinters in the egg stage. Spiderling emerged in May, the diminutive males matured in late June and early July, and females matured in early September. Eggs were produced from late September to late October or early November. This report is the first complete documentation of the population phenology of any bolas spider. Newly-emerged M. hutchinsoni spiderlings did not use a bolas, but instead hunted by positioning themselves on the underside of leaf margins where they ambushed small arthropods that crawled along the leaf margins. Subadult and adult female M. hutchinsoni used a bolas to capture moths. Only male moths were captured, specifically three species of Noctuidae (bristly cutworm, bronzed cutworm, and smoky tetanolita) and one species of Pyralidae (bluegrass webworm). Among 492 prey captured by more than twenty spiders at two sites during 1985 and 1986, smoky tetanolita moths and bristly cutworm moths accounted for 93% of the total. The flight behavior of approaching moths, the limited taxa caught from a large available moth fauna, and the fact that only males were caught support the hypothesis that the spider attracts its prey by producing chemicals which mimic the sex pheromones of these moth species. Adult female M. hutchinsoni frequently captured more than one moth species on a given night. The two most common prey species were active at different times of night, the bristly cutworm soon after nightfall and the smoky tetanolita generally between 11:00 p.m. and dawn. This pattern suggests that mating activity of these moth species may be temporally isolated, a common phenomenon when sympatric species have similar pheromones. If so, the spider could capture both species without producing different pheromone-mimicking compounds, simply by hunting during the activity period of each species.The investigation reported in this paper (No. 87-7-76) is in connection with a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Director     

Interspecific differences in carotenoid content and sensitivity to UVB radiation in three acanthocephalan parasites exploiting a common intermediate host

Few endoparasite species are pigmented. Acanthocephalans are an exception however, with several species being characterised by yellow to orange colouration both at the immature (cystacanth) and adult stages. However, the functional and adaptive significance of carotenoid-based colourations in acanthocephalans remains unclear. One possibility is that the carotenoid content of acanthocephalan cystacanths acts as a protective device against ultra-violet radiation (UVR) passing through the translucent cuticle of their crustacean hosts. Indeed, acanthocephalans often bring about behavioural changes in their aquatic intermediate hosts that can increase their exposure to light. Carotenoid composition and damage due to ultra-violet - B (UVB) radiation were investigated in three acanthocephalan parasite species that induce contrasting behavioural alterations in their common intermediate host, the crustacean amphipod Gammarus pulex. The fish acanthocephalans Pomphorhynchus laevis and Pomphorhynchus tereticollis both induce a positive phototaxis in gammarids, such that infected hosts spend more time out of shelters, while remaining benthic. The bird acanthocephalan Polymorphus minutus, on the other hand, induces a negative geotaxis, such that infected hosts typically swim close to the water surface, becoming more exposed to UV radiation. We show that differences in cystacanth colouration between acanthocephalan species directly reflect important differences in carotenoid content. The two fish parasites exhibit a contrasting pattern, with P. tereticollis harbouring a large diversity of carotenoid pigments, whereas P. laevis is characterised by a lower carotenoid content consisting mainly of lutein and astaxanthin. The highest carotenoid content is found in the bright orange P.minutus, with a predominance of esterified forms of astaxanthin. Exposure to UVB radiation revealed a higher susceptibility in P. laevis larvae compared with P. tereticollis and P. minutus, in terms of sublethality (decreased evagination rate) and of damage to DNA (increased cyclobutane pyrimidine dimers production). Although we found important and correlated interspecific differences in carotenoid composition and tolerance to high UVB radiation, our results do not fully support the hypothesis of adaptive carotenoid-based colourations in relation to UV protection. An alternative scenario for the evolution of carotenoid accumulation in acanthocephalan parasites is discussed.     

Chemical defence in avian brood parasites: production and function of repulsive secretions in common cuckoo chicks

The use of active chemical defence against predators is relatively rare in birds. Among others, it has been reported for some members of family Cuculidae whose chicks, when threatened, expel dark foul‐smelling liquid from their cloaca. Apart from the brood parasitic great spotted cuckoo Clamator glandarius, however, this phenomenon has not yet been systematically studied in any other cuckoo species. Here we investigated the repellent behaviour in the evicting brood parasite, the common cuckoo Cuculus canorus, parasitizing the great reed warbler Acrocephalus arundinaceus. We explored whether production of secretions varies with chick age or size, and tested its presumed repellent function against various types of predators. We found that the production of secretions commenced at the age of approximately eight days, then gradually increased and decreased again shortly before fledging. Furthermore, we experimentally confirmed a more intensive repellent effect of the secretions on mammal predators than on avian predators, such as raptors and owls. The secretions have, however, no effect on corvid predators, probably because these scavengers often consume malodorous food. Further experimental studies together with phylogenetic comparative analyses are needed to elucidate the origin and function of this intriguing phenomenon both in parasitic and non‐parasitic cuckoos.     

Interspecific relationships in co‐occurring populations of social parasites and their host ants

Myrmica ant colonies host numerous insect species, including the larvae of Maculinea butterflies and Microdon myrmicae hoverflies. Little is known about the interspecific relationships among these social parasites and their host ants occurring in sympatric populations. We investigated communities of social parasites to assess the strategies allowing them to share the same pool of resources (i.e. Myrmica colonies). The present study was carried out at five sites inhabited by different social parasite communities, each comprising varying proportions of Maculinea teleius, Maculinea nausithous, Maculinea alcon, and Microdon myrmicae. We investigated their spatial distributions, host segregation, the degree of chemical similarity between social parasites and hosts, and temporal overlaps in colony resource exploitation. Spatial segregation among social parasites was found in two populations and it arises from microhabitat preferences and biological interactions. Local conditions can drive selection on one social parasite to use a Myrmica host species that is not exploited by other social parasites. Myrmica scabrinodis and Myrmica rubra nests infested by larvae of two social parasite species were found and the most common co‐occurrence was between Ma. teleius and Mi. myrmicae. The successful coexistence of these two species derives from their exploitation of the host colony resources at different times of the year. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 699–709.     

Public information and conspecific nest parasitism in goldeneyes: targeting safe nests by parasites

Conspecific nest parasitism (CNP) is a widespread alternativereproductive tactic in birds. Several hypotheses have been putforward to explain the evolution and occurrence of CNP, butno generally applicable hypothesis exists. Recent experimentalresults from the common goldeneye (Bucephala clangula), a cavity-nestingduck, have revealed that parasitic females preferentially layeggs in safe nest-sites, implying that nest predation risk isan important ecological determinant of CNP. The present studyfocuses on the mechanisms by which parasites identify safe nest-sites.Predation risk of a given nest-site was predictable betweensuccessive breeding seasons. At the end of the nesting season,females prospected active nest-sites more frequently than nest-sitesthat did not have a nest in the current season. Nest-sites thathad been prospected more frequently by females in year t hada higher probability to be parasitized in year t + 1. The resultssuggest that the use of public information, derived throughnest-site prospecting, enabled parasites to target safe nests.These findings provide a new and potentially generally applicableperspective to understand the evolution and occurrence of CNP.     

Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly

Studies of cophylogenetic associations between hosts and parasites have become increasingly common. Historically, congruence between host and parasite phylogenies has been seen as evidence for cospeciation. Analyses of such coevolutionary relationships, however, are made extremely difficult by the complex interplay of cospeciation, host switching, sorting (extinction), duplication (intrahost speciation) and inertia (lack of parasite speciation) events, all of which may produce incongruence between host and parasite phylogenies. Here we review several methods of analysing cospeciation. We illustrate these methods with an example from a Procellariiformes (seabird) and chewing louse (Halipeurus) association.     

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.     

An unlikely partnership: parasites, concomitant immunity and host defence.

Concomitant immunity (CI) against macroparasites describes a state of effective anti-larval immunity coupled with persistent adult infection. Experimental studies indicate that immunologically concealed adult worms might promote anti-larval immunity via the release of cross-reactive antigens, thus creating a barrier against continual infection and restricting burden size within the host. CI offers an important potential benefit to established worms by preventing overcrowding within the host. Thus, CI may be interpreted as akin to vaccination; relatively long-lived adult worms 'vaccinate' their host with larval surface antigens and so benefit from reduced conspecific competition. The shared responsibility for host vaccination among adult worms leads to a problem of collective action. Here, we build on earlier analytical findings about the evolutionary forces that shape cooperation among parasites in order to produce a stochastic simulation model of macroparasite social evolution. First, we theoretically investigate a parasite adaptation hypothesis of CI and demonstrate its plausibility under defined conditions, despite the possibility of evolutionary 'cheats'. Then we derive a set of predictions for testing the hypothesis that CI is partly a host-manipulative parasite adaptation. Evidence in support of this model would present an unusual case of adaptive population regulation.     

Comparative morphology of Van der Vecht's organ in Polistes social parasites: host ecology and adaptation of the parasite

Camouflage strategies are common in insect social parasites. Being accepted into an alien colony as a dominant nestmate favours behavioural and morphological adaptations to mimic a specific odour. In Polistes social parasites, abdominal tegumental glands are involved in this camouflage strategy. These glands secreting cuticular hydrocarbons are connected with a modified cuticular area of the last gastral sternite of female wasps, named Van der Vecht's organ, whose secretion is involved in rank and dominance recognition. The size of this exocrine area has been demonstrated to be under selective pressure in Polistes, as a response to an efficient dominance recognition. Because chemical and behavioural integration differs between parasitic species, we carried out a comparison of Van der Vecht's organ size between the three Polistes social parasites and their respective hosts. The parasites Polistes sulcifer and Polistes semenowi, capable of a rapid chemical mimicry and specialized to exploit a lowland host, also show an enlarged Van der Vecht's organ. Conversely, the parasite Polistes atrimandibularis, specialized on a mountain species and showing a slow chemical integration, has a smaller organ. The time available for the parasite to tune up its chemical mimicry, before the emergence of workers to be accepted as a dominant nestmate, appears to be the most important selective pressure acting on the size of this abdominal organ. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013 , 109 , 313–319.     

Evolutionary relationships, cospeciation, and host switching in avian malaria parasites

We used phylogenetic analyses of cytochrome b sequences of malaria parasites and their avian hosts to assess the coevolutionary relationships between host and parasite lineages. Many lineages of avian malaria parasites have broad host distributions, which tend to obscure cospeciation events. The hosts of a single parasite or of closely related parasites were nonetheless most frequently recovered from members of the same host taxonomic family, more so than expected by chance. However, global assessments of the relationship between parasite and host phylogenetic trees, using Component and ParaFit, failed to detect significant cospeciation. The event-based approach employed by TreeFitter revealed significant cospeciation and duplication with certain cost assignments for these events, but host switching was consistently more prominent in matching the parasite tree to the host tree. The absence of a global cospeciation signal despite conservative host distribution most likely reflects relatively frequent acquisition of new hosts by individual parasite lineages. Understanding these processes will require a more refined species concept for malaria parasites and more extensive sampling of parasite distributions across hosts. If parasites can disperse between allopatric host populations through alternative hosts, cospeciation may not have a strong influence on the architecture of host-parasite relationships. Rather, parasite speciation may happen more often in conjunction with the acquisition of new hosts followed by divergent selection between host lineages in sympatry. Detailed studies of the phylogeographic distributions of hosts and parasites are needed to characterize these events.     

Playing together,laughing together: rapid facial mimicry and social sensitivity in lowland gorillas

In nonhuman animals, the phenomenon of rapid facial mimicry (RFM)—the automatic, involuntary, and rapid (<1 s) replication of others’ facial expressions—has been mainly investigated in the playful domain. In immature lowland gorillas Gorilla gorilla gorilla both play face (PF) and full PF (FPF) are rapidly mimicked between the players. This makes the species suitable to test hypotheses on the factors influencing RFM during play. The observations on 3 captive groups of lowland gorillas (N = 27) revealed that contrary to expectations, the closeness of social bond negatively influenced the occurrence of RFM but it did not affect either RFM latency or its overlapping index (OVERLAP). RFM was affected by the degree of symmetry of play fighting: the more balanced the session, the higher the occurrence of RFM. Players of the same sex class responded faster than players of different sex. These findings suggest that RFM may help synchronizing behaviors of playmates matching in size (same-sex) and promote symmetric playful interactions. “Laughing together” (measured by the RFM OVERLAP) lasted longer when the responder perfectly mirrored the partner expression (PF→PF; FPF→FPF). If PF and FPF convey information on the different play roughness degree, through “laughing together” the players could coordinate their actions and share positive moods and playful intensity. If the perfect congruency in the motor resonance, also known as social sensitivity, can foster a possible emotional dialogue between gorillas remains to be investigated.     

Evidence for aggressive mimicry in an adult brood parasitic bird,and generalized defences in its host

Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host''s own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host–parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.