Hammering homoplasy: multiple gains and losses of vibrational sounding in cryptine wasps (Insecta: Hymenoptera: Ichneumonidae)

Many hosts of parasitic wasps are, when attacked, either at an immobile stage, living in a concealed environment, or both, thus making their detection especially difficult. Cryptine ichneumonid wasps often parasitize beetle or moth larvae, prepupae or even pupae in tunnels in wood, and many others attack cocooned hosts in various states of concealment. The structure of the antennal tips shows a range of adaptations at least the most extreme of which appear to be involved in locating deeply concealed hosts through vibrational sounding (= echolocation through solid media). We show that, within the Cryptinae, the tips of the antenna are modified into a hammer-like structure that is suitable for knocking a substrate; this form of echo-location is typical to the tribe Cryptini, although it is also found in a few phygadeuontines and in the hemigastrine genus Echthrus . Electron micrographs are presented to illustrate the different degrees of antennal modifications found in the subfamily. Comparative analysis using independent contrasts was then used to demonstrate a statistically significant association between degree of antennal hammer development and attacking, typically wood-boring, beetle hosts of the families Cerambycidae and Buprestidae.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 82–102.     

Biology of Rhoophilus loewi (Hymenoptera: Cynipoidea: Cynipidae), with implications for the evolution of inquilinism in gall wasps

The sole described indigenous afrotropical cynipid, the South African endemic Rhoophilus loewi , was originally described as a gall inducer. As predicted by phylogenetic relationships, we confirm that R. loewi is instead an inquiline wasp. Although all other cynipid inquilines develop in galls induced by cynipid wasps, or very rarely cecidomyiid midges, R. loewi is the only cynipid inquiline of a lepidopteran gall, inducing secondary inquiline cells in galls induced by a cecidosid moth genus Scyrotis on Rhus species (Anacardiaceae). Rhoophilus is a lethal inquiline; its larval cells expand into the hollow interior of the host gall resulting in death of the gall inducer. Rhoophilus loewi is redescribed and the final-instar larva described for the first time. We describe host-plant associations, the morphology and phenology of gall formation, and the suite of parasitoid Hymenoptera associated with these galls. The community centred on Scyrotis galls is compared with those observed in other hosts of inquiline cynipids. Elucidation of the life history of R. loewi has fundamental implications for understanding the evolution of cynipid wasps.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 153–172.     

Natural enemies of Paropsis atomaria Olivier (Coleoptera: Chrysomelidae) in south-eastern Queensland eucalypt plantations

Abstract  A field survey for natural enemies of Paropsis atomaria was conducted at two south-eastern Queensland Eucalyptus cloeziana plantation sites during 2004–2005. Primary egg and larval parasitoids and associated hyperparasitoids were identified to genus or species, and parasitism rates were determined throughout the season. Predators were identified to family level but their impact was not quantified. P. atomaria adults were also examined as potential hosts for parasitic mites and nematodes. An undescribed species of Neopolycystus (Pteromalidae) was the major primary egg parasitoid species reared from egg batches, parasitising half of all egg batches collected. Three hyperparasitoid species ( Baeoanusia albifunicle (Encyrtidae), Neblatticida sp. (Encyrtidae) and Aphaneromella sp. (Platygasteridae) were present, representing around one-quarter to one-third of all emergent wasps; this is the first host association record for Neopolycystus–B. albifunicle. In contrast to populations of P. atomaria from the Australian Capital Territory, primary larval parasitism was very low, around 1%, and attributable only to the tachinid flies Anagonia sp. and Paropsivora sp. However, the presence of the sit-and-wait larval hyperparasitoid, Perilampus sp. (Perilampidae) was high, emerging from around 17% of tachinid pupae, with planidia infesting a further 40% of unparasitised hosts. Three species of podapolipid mites parasitised sexually mature P. atomaria adults, while no nematodes were found in this study. Spiders were the most common predators and their abundance was positively correlated with P. atomaria adult and egg numbers. Although natural enemy species composition was identical between our two study sites, significant differences in abundance and frequency were found between sites.     

Host plant toxicity affects developmental rates in a polyphagous fruit fly: experimental evidence

Various, non-exclusive mechanisms have been invoked to explain the observed association between host plant use and speciation in insect species. In the Afrotropical genus Ceratitis (Diptera: Tephritidae), morphological, molecular, and biochemical data suggest that evolutionary radiation of stenophagous clades originates from their ability to exploit toxic hosts. To test whether, and to what extent, the development and fitness of Ceratitis fasciventris , a polyphagous congener known to infest over 43 host species, is adversely affected by host plant toxicity, we compared the rates of development, survival, and reproduction of captive bred individuals in four media that differ in alkaloid concentration. Despite reduced pupal and adult sizes, C. fasciventris larvae developing under low alkaloid concentrations successfully developed to the adult stage, probably as a result of accelerated pupation and ensuing restricted exposure to the toxic environment. High alkaloid concentrations, however, impaired their developmental process and prevented subsequent reproduction. The adverse effects of host plant toxicity on larval development in polyphagous fruit flies indicate that high alkaloid concentrations pose a significant constraint on host use by polyphagous Ceratitis species.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 728–737.     

How is host egg mimicry maintained in the cuckoo (Cuculus canorus)?

To investigate the evolutionary mechanism (host specificity vs. random searching) maintaining mimicry between cuckoo egg appearance and that of different European cuckoo Cuculus canorus hosts, we studied the level of mimicry between the appearance of C. canorus eggs and that of their hosts' eggs in different habitats in southern Finland by using ultraviolet-visible reflectance spectrophotometry. In the main habitat used by C. canorus for reproduction, eggs laid in nests of different host species differed in appearance. Host use by C. canorus was not related to the abundance of hosts, and the level of mimicry was not related to host abundance in the habitat. Furthermore, a close match between C. canorus egg appearance and that of host eggs within habitats was detected after removing the potentially confounding effect of host abundance. In the only two suitable host species nesting in trees (namely chaffinch Fringilla coelebs and brambling Fringilla montifringilla ) we detected changes in C. canorus egg appearance that paralleled those of the two host species. Thus our findings suggest the existence of a correlation between the appearance of C. canorus eggs and that of their hosts' eggs within different habitat types, and suggest that mimicry is maintained by strict host preferences by each C. canorus female when laying.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 57–68.     

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.     

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.     

Meadow pipit (Anthus pratensis) egg appearance in cuckoo (Cuculus canorus) sympatric and allopatric populations

Host populations tend to show less ability to discriminate against parasites when living in their absence. However, comparison of rejection rates among sympatric and allopatric host populations does not allow determination of whether the greater tolerance in allopatric populations reflects a genetic change or phenotypic plasticity. Here we test the existence of changes in a host's adaptation to brood parasitism in the absence of parasitism by studying intraclutch variation in egg appearance, which is a genetically determined component of host defence favouring discrimination of parasitic eggs. We investigated egg phenotypes of a common host of the European cuckoo, Cuculus canorus , in the presence and in the absence of cuckoos. By using objective spectroradiometry techniques of colour assessment we compared intraclutch variation between populations of meadow pipit, Anthus pratensis , sympatric (England) and allopatric (Iceland and Faeroe Islands) with C. canorus . Allopatric populations of A. pratensis showed greater intraclutch variation in egg appearance in the ultraviolet part of the spectrum than did a population sympatric with C. canorus . Two possible alternative mechanisms explaining these findings are discussed.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 543–549.     

Differences in environmental predictability underlie divergent competitive abilities in three congeneric hydroids

Species in which individuals experience predictable and uniform environments should be most finely adapted to their environment. Many hydrozoan species in the genus Hydractinia simultaneously occupy similar microhabitats (gastropod shells inhabited by hermit crabs) but experience considerable differences in their immediate environment (size and species of shells and hosts). In the present study, hydroid species experience differences in environmental predictability and traits that mediate competitive ability (growth form and growth rate). The inferred competitive ability was directly proportional to the extent to which the gastropod environment promotes interactions between small, juvenile colonies, which always end in competitive elimination. Extensive intraspecific variation in competitive ability was explained primarily by crab host species or site. Dense host populations impose more severe disturbance regimes that favour competitively inferior, but disturbance-resistant, phenotypes. Interplay between different types of variation (gastropods and hermit crabs) provides a possible mechanism for the maintenance of intraspecific growth form variation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 322–338.     

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.     

Volatile chemical release by bethylid wasps: identity, phylogeny, anatomy and behaviour

The structures of volatile chemicals released by parasitic wasps in the family Bethylidae are shown to correspond to the subfamily to which the species belong. Species in the Epyrinae release skatole (3-methylindole) and species in the Bethylinae release a spiroacetal (2-methyl-1,7-dioxaspiro [5.5]undecane): these compounds are chemically very different. The enantiomeric composition of the spiroacetal differs between congeneric species. Chemical release is a discrete event under the active control of both male and female wasps. Structural differences between the mandibular glands and intramandibular glands suggest the mandibular glands to be the source of released volatiles. Real-time mass spectrometry shows that the spiroacetal is released by Goniozus nephantidis females during dyadic resource contests, with release more common during more aggressive interactions. Chemical tagging with deuterium further shows that the volatile is released by the loser of an agonistic interaction and not the winner. The function of spiroacetal and skatole release by bethylids is discussed.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 837–852.     

An inquiline fig wasp using seeds as a resource for small male production: a potential first step for the evolution of new feeding habits?

The processes allowing evolutionary transitions in resources used by parasitic wasps are largely unknown. Microhymenopteran communities associated with figs could provide a model system to investigate such transitions. We investigate here a species of genus Idarnes . The larvae generally develop as inquilines of the pollinating wasp larvae. However, in figs where the parasitic pressure is high, eggs are laid in developing seeds. These eggs turn into small males. This is the first report of seed consumption by a fig wasp. Using an alternative resource to produce small males could provide a pathway to select for increased ability to use this resource and hence provide an intermediate step for evolving the capacity to use new resources.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 9–17.     

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.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

Adaptations in the common cuckoo (Cuculus canorus) to host eggs in a multiple-hosts system of brood parasitism

The common cuckoo Cuculus canorus parasitism greatly reduces the reproductive success of its hosts and imposes strong selection pressure for hosts to evolve defences against parasitism, such as the ability to recognize and reject dissimilar parasitic eggs, which, in turn, selects for better egg mimicry by the cuckoo. In the co-evolutionary interaction, however, it remains unknown how the cuckoo successfully expanded its range of host usage and how they developed egg mimicry. Most previous studies were conducted in areas where a very few number of host species (i.e. one or two at most) are sympatric with the cuckoo. Several host species, however, breed sympatric with the cuckoo and have been parasitized in the study site in Nagano, central Japan. Such a multiple-hosts system will provide valuable insights for understanding the cuckoo–hosts interactions in the past. In the present study, we report quantitative profiles of eggs based on spectrometer reflectance for four major host species and the corresponding cuckoo gentes. The hosts include the oriental reed warbler ( Acrocephalus orientalis ), bull-headed shrike ( Lanius bucephalus ), azure-winged magpie ( Cyanopica cyana ), and black-faced bunting ( Emberiza spodocephala ). We show that (1) egg morphs of each host and corresponding cuckoo gens can be categorized by two chromatic components of reflectance spectra and (2) there is a significant difference in a particular chroma component between hosts and the cuckoo. We suggest that the cuckoo parasitism in central Japan originated from parasitism on the black-faced bunting.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 291–300.     

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.     

An extraordinary shift in life habit within a genus of cyclopid copepods in Lake Tanganyika

We here describe a new species of cyclopid copepod, Eucyclops bathanalicola sp. nov. , parasitic on a gastropod endemic to Lake Tanganyika, Bathanalia straeleni (Cerithioidea, Paludomidae). E. bathanalicola is distinguished by the possession of praecoxal claws on the maxillules, by the modified maxillae which lack any trace of an endopod on the powerful distal claw, and by the reduction of the maxillipeds to minute unarmed lobes. In the character states exhibited by the female body, antennules and swimming legs 1–5, the new species closely resembles a typical free living Eucyclops . The impact of the adoption of parasitism as a life habit is expressed primarily in the modification of the postmandibular mouthparts. As a member of the Cyclopidae, this species represents a unique foray into a parasitic lifestyle from an otherwise free-living group of copepods inhabiting Lake Tanganyika. This is the first record of a parasitic copepod on a mollusc host within this ancient lake and only the second family of freshwater gastropods reported to host copepods.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 146 , 275–285. No claim to original US government works.     

A mass recruitment event in the land crab Gecarcinus ruricola (Linnaeus, 1758) (Brachyura: Grapsoidea: Gecarcinidae), and a description of the megalop

A mass return to land of the megalop of the land crab Gecarcinus ruricola is reported. The return occurred in June 2004 on the island of Providencia in the western Caribbean: this is the first detailed report of larval return in this species, and the most detailed report for any gecarcinid. Crabs emerged from the sea as megalops over 2 to 3 days, and moved rapidly landwards. Vast numbers migrated > 50 m across land before moulting to the first crab – the megalop is clearly the invasive stage. The megalop is described for the first time, and criteria are identified to discriminate it from other Caribbean gecarcinids.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 146 , 149–164.     

Convergence and parallelism among cicadas of Argentina and the southwestern United States (Hemiptera: Cicadoidea)

Cicadas of the genera Derotettix in Argentina and Okanagodes in the south-western United States resemble each other in colour, live on salt-tolerant plants ( Atriplex spp. etc.), nearly match the colour of their respective host plants and produce songs above the range of avian hearing. The Argentine cicadas are smaller, but have nearly identical thermal limits for activity measured by the minimum temperature for flight (20–24 °C) and a body temperature at heat torpor (48–49 °C). The species shift activity from basking sites to shade at temperatures above 37 °C, although O .  gracilis rises to a significantly higher temperature (40.7 °C) than its congener (38.2 °C) or Derotettix (37.2 °C). The thermal tolerances are the highest reported for cicada species. A third group using halophytes in Argentina ( Babras sonorivox ) has similar temperature tolerances and is cryptically coloured. The genera are convergent with respect to morphology, coloration, body size, behaviour, habitat choice and host plant selection. The similarities of thermal tolerances and their influence on behaviour can be viewed as parallelism because the underlying mechanisms are the same in all species studied.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 281–288.