Repeated origins of social parasitism in allodapine bees indicate that the weak form of Emery's rule is widespread,yet sympatric speciation remains highly problematic

The evolutionary origins of social parasitism are very unevenly distributed among ants, bees and wasps, but social parasite lineages are frequently close relatives of their host lineages. Two explanations for these relationships have been proposed: (1) initially, social species are more likely to become parasitic on relatively closely related social species, because they share life history, physiological and behavioural traits that allow successful integration within the host colony; and (2) social parasites have evolved directly from their host lineage via sympatric speciation. Comparative approaches, covering multiple origins and intermediate evolutionary stages, are needed to determine which of these possibilities is more likely. We use molecular phylogenetics to examine multiple origins of parasitism in the bee tribe Allodapini. We identify seven origins resulting in obligate social parasitism (inquilinism), one origin of facultative social parasitism, which was followed by subsequent speciation and where both daughter species remained facultatively parasitic, and one case of frequent facultative heterospecific co‐nesting that probably represents incipient social parasitism. All host–parasite lineage pairs show strong phylogenetic affinities, but only the case of facultative heterospecific nesting involves true sister species relationships. Our results are consistent with the range of parasitic relationships that are expected under an allopatric model for the origin of social parasitism, but are highly problematic for a sympatric speciation model. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 320–331.     

Antigenic variation during the developmental cycle of Trypanosoma brucei

During the complex life cycle of Trypanosoma brucei, changes in the exposed surface antigens occur in both the mammalian host and the insect vector (Glossina spp.). These antigenic changes are associated with alterations of the variant surface glycoprotein (VSG) composition or with the loss of the VSG. In the bloodstream of the mammalian host, trypanosomes successfully evade destruction by the host's immune response by continuously expressing alternative VSGs, at low frequency, which are not destroyed by host antibodies. When ingested by the tsetse fly, the bloodstream trypanosomes rapidly lose their surface coat and surface membrane antigens are exposed which are normally covered in the bloodstream. In the salivary glands of the tsetse fly, the trypanosomes differentiate to the metacyclic stage, which reacquires a surface coat. The antigenic composition of the metacyclics is heterogeneous. The same metacyclic types are expressed regardless of the bloodstream antigenic type ingested by the tsetse fly. In the mammal the metacyclics differentiate to long-slender bloodstream forms but continue to express the metacyclic VSG for at least three days. The next VSGs expressed in the mammalian host appear to be influenced by the antigenic type ingested by the tsetse. The ingested antigenic type is often expressed in the first parasitemia following expression of the metacyclic antigenic types.     

Insecticides in host-parasitoid interactions

The equilibrium and local stability properties are described of insect host-parasitoid models that include the effects of insecticide application. The models are framed in discrete time making it important to distinguish between different sequences of parasitism and insecticide kill in the host's life cycle. Four possibilities are considered: (1) Insecticides act prior to parasitism and only kill hosts. (2) Insecticides act after parasitism and only kill hosts. (3) Insecticides act after parasitism and also kill parasitized hosts at the same rate. (4) Insecticides act prior to parasitism and also kill adult parasitoids. There is a clear ranking of the different application strategies in terms of their effect on the depression of the host equilibrium and their contribution to stability.     

Polydnaviruses: potent mediators of host insect immune dysfunction

Endoparasitic insects are used as biological control agents to kill many species of insect pest. One key to the success of parasitoids that develop in the hemocoel of their host is their ability to knock out the host's immune system, inducing a decline in the responsiveness of a variety of cellular and humoral components so that parasitoid eggs are not encapsulated. In many species parasitized by braconid and ichneumonid wasps, host immunosuppression appears to be mediated by polydnaviruses (PDVs) injected by the female parasitoid into the host hemocoel. The viruses exhibit a complex and intimate genetic relationship with the wasp, since viral sequences are integrated within the wasp's chromosomal DNA. Here Mark Lavine and Nancy Beckage summarize the current evidence for mechanisms of virally induced host immunosuppression in parasitized insects, as well as the roles of other factors including wasp ovarian proteins and venom components, in suppressing hemocyte-mediated and humoral immune responses. Interestingly, in some species, the PDV-induced host immunosuppression appears transitory, with older parasitoid larvae probably exploiting other mechanisms to protect themselves from the host's immune system during the final stages of parasitism. During the final stages of parasitism, the parasitoids likely exploit other mechanisms of immunoevasion via antigen masking, antigen mimicry, or production of active inhibitors of the hemocyte-mediated encapsulation response as well as inhibiting melanization.     

Brood-parasitism by the Shining Cuckoo Chrysococcyx lucidus at Kaikoura, New Zealand

For three seasons starting in 1976 I studied the breeding of Shining Cuckoos Chrysococcyx lucidus in forest near Kaikoura, New Zealand. There is no evidence that the cuckoo parasitizes any host on mainland New Zealand other than the Grey Warbler Gerygone igata. A nestling cuckoo returned to within 1 km of its natal site in a subsequent breeding season, presumably after migrating beyond New Zealand. Empirical and theoretical estimates of the area occupied by Shining Cuckoos while breeding are given. Cuckoos near Kaikoura laid during ten weeks, the modal week of laying following seven weeks after the presumed peak of arrival of birds in New Zealand. First clutches of the host escaped parasitism because they were laid before most cuckoos arrived. Parasitized clutches received one cuckoo egg which replaced a host's egg. It was laid before, just after or long after the host began incubating, and mimicry was lacking. Cuckoo eggs, which were about 8% of the adult cuckoo's weight, hatched in 14–17 days. The frequency of parasitism near Kaikoura was 55% of late clutches (n = 40).
At 3–7 days old, nestling Shining Cuckoos evicted from the nest all other contents. The nestling period was at least 19 days. Growth in weight followed a logistic curve and the equation is given. Just over half the cuckoo eggs produced fledglings. The effect of brood-parasitism on the Grey Warbler's productivity was small. Only 17% of late warbler eggs, and late eggs only, were prevented by parasitism from yielding fledglings. Late laying by some Shining Cuckoos (relative to the host's incubational cycle), and late eviction, often led to brief inter-specific competition among nestlings for food. The brief coexistence of young Warblers and Cuckoos in the nest may explain the apparent mimicry by newly-hatched Shining Cuckoos of the host's young.     

The Biology of Vampyrophrya pelagica (Chatton & Lwoff, 1930), a Histophagous Apostome Ciliate Associated with Marine Calanoid Copepods

ABSTRACT. The histophagous apostome. l'ampyrophrya pelagica , occurs on calanoid copepods in North Carolina. Its life cycle has two pathways: one when the copepod host is injured; the other when the host is ingested by an invertebrate predator. The ciliate, immediately after encysting on a copepod. metamorphoses to a feeding stage. When its host is injured or ingested by a predator, it excysts enters the wound and ingests the host's cytoplasm. In the single-host life cycle, after feeding, the ciliate encysts within the cadaver; in the two-host life cycle, after feeding it encysts upon a substrate. Encysted cells divide into 2–32 migratory tomites. Freed tomites are motionless in the water column until the water is disturbed, at which time they spring in the direction of any vibration, which many times results from a feeding copepod. Tomites select specific hosts, since not all species of copepods are infested. We hypothesize that the single-host life cycle yields many tomites that heavily infest hosts at random, and passage through the predator (two-host life cycle) results in fewer, but more widely dispersed tomites that are released continuously. The two-host life cycle is facultative for the individual, but may be obligate for the continuation of the species.     

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.     

Phylogenetic inference from platyhelminth life-cycle stages

Studies of the life cycle stages of digeneans and oncophoreans (= monogeneans and cestodes) indicate that these two groups had separate origins from free-living rhabdocoel-like ancestors and that the original single-host life cycles became 2-host cycles through accidental ingestion, in digeneans by free-swimming adults being ingested by vertebrates, and in cestodes by eggs being ingested by invertebrates. In both lines a third host was incorporated as a means of increasing the efficiency of transfer between hosts, in digeneans between the primary mollusc and the secondary vertebrate, and in cestodes between the secondary (“first intermediate”) host and the primary vertebrate host.     

When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model

It has been suggested that discrimination and rejection of thenestlings of avian brood parasites are most likely to evolvewhen the parasite nestling is raised alongside the host nestlings,for example, many cowbird-host systems. Under these circumstances,the benefits of discrimination are high because the host parentsmay save most of their brood. However, there is a general absenceof nestling rejection behavior among hosts of nonevicting parasites.In a cost-benefit equilibrium model, based on the premise thathost species learn to recognize their offspring through imprintingon first breeding, we show that nestling recognition can beadaptive for hosts of cowbirds, but only under strict conditions.Namely, when host nestling survival alongside the parasite islow, rates of parasitism are high and the average clutch sizeis large. All of these conditions are seldom simultaneouslyachieved in real systems. Most importantly, the parasite nestling,on average, does not sufficiently depress host nestling survivalto outweigh the costs of nestling recognition and rejectionerrors. Thus, we argue that nestling acceptance behaviors byhosts of nonevicting brood parasites may be explained as anevolutionary equilibrium in which recognition costs act as astabilizing selection pressure against rejection when most ofthe host's offspring survive parasitism.     

Interactions between parasitized and unparasitized conspecifics: parasitoids modulate competitive dynamics

Parasitism influences many aspects of a host's behavior and physiology. Therefore, parasitism is also likely to influence the competitive ability of the host. Field populations of phytophagous insects are often a mix of parasitized and unparasitized conspecifics and the inclusion of parasitism in their competitive dynamics may alter expected outcomes. We investigated the influence of parasitism by the hymenopteran parasitoid Phanerotoma franklini Gahan on the competitive interactions among larvae of its host Acrobasis vaccinii Riley. We found that parasitized larvae were poorer competitors and required less food to complete development compared to unparasitized larvae. To examine the influence of parasitism on the competitive dynamics of this system, we constructed an individual-based model parameterized with our laboratory data. The model examined the role of resource availability and parasitism rate on larval survival. The model suggests that parasitized larvae (and, hence parasitoids) experience higher levels of mortality from competition than unparasitized larvae. Further, the model also suggests that the decreased consumption of resources by parasitized larvae results in a decline in the occurrence of competition as the parasitism rate increases. We suggest that these observations may be general to many parasitoid-host systems.     

Intracellular parasitism: cell biological adaptations of parasitic protozoa to a life inside cells

Several protozoan parasites evade the host's immune defence because most of their development takes place inside specific host cells. Only a few of these protozoa live within the host cell cytosol. Most parasites are sequestered within membrane-bound compartments, collectively called ‘vacuoles’. Recent advances in the cell biology of intracellular parasites have revealed fundamental differences in the strategies whereby such organisms gain entry into their respective host cells. These differences have important implications for host-parasite interaction and for nutrient acquisition by the parasite. Leishmania spp. take advantage of the phagocytic properties of their host cells and presumably contribute little to the uptake process. In contrast, apicomplexan parasites have developed highly specialised organelles, called micronemes and rhoptries, to actively invade a variety of nucleated cells and, in the case of Plasmodium falciparum, human erythrocytes. Following invasion, parasites use a multitude of strategies to protect themselves from the defence mechanisms of the parasitized cells. In addition, they induce novel pathways within the infected cell that allow a most efficient nutrient acquisition both from the host cell cytoplasm and from the extracellular environment. Parasite-induced changes of host cells are most apparent in erythrocytes infected with Plasmodium spp. Mammalian erythrocytes are deficient in de novo protein and lipid biosynthesis and, consequently, pathways which allow the transport of macromolecules and small solutes are established by metabolic activities of the parasite. Research into the cell biology of intracellular parasitism has identified fascinating phenomena some of which we are beginning to understand at a molecular level. They are fascinating because they allow insights into a very intimate interaction between two eukaryotic cells of entirely different phylogenetic origins.     

The population dynamical implications of male-biased parasitism in different mating systems

Although there is growing evidence that males tend to suffer higher levels of parasitism than females, the implications of this for the population dynamics of the host population are not yet understood. Here we build on an established 'two-sex' model and investigate how increased susceptibility to infection in males affects the dynamics, under different mating systems. We investigate the effect of pathogenic disease at different case mortalities, under both monogamous and polygynous mating systems. If the case mortality is low, then male-biased parasitism appears similar to unbiased parasitism in terms of its effect on the population dynamics. At higher case mortalities, we identified significant differences between male-biased and unbiased parasitism. A host population may therefore be differentially affected by male-biased and unbiased parasitism. The dynamical outcome is likely to depend on a complex interaction between the host's mating system and demography, and the parasite virulence.     

以鸟类视觉模型揭示中杜鹃对冠纹柳莺的卵色模拟(英文)

于2009年4—7月,采用光谱仪量化卵色和建立鸟类视觉模型的方法,在贵州宽阔水自然保护区对中杜鹃(Cuculus saturatus)寄生冠纹柳莺(Phylloscopus reguloides)的卵色模拟进行了研究。中杜鹃产白色卵带极少数而微小的棕色斑,明显大于宿主卵,重2.06g,体积1.91cm3。从人眼看,中杜鹃卵对宿主卵在很大程度上是模拟的,但视觉模型表明,两者的卵色在色调和色度上都完全分离,揭示了人眼探测不到的卵色模拟情况。该文首次对中杜鹃的雏鸟特征进行描述,在4日龄以后雏鸟嘴裂中出现三角形黑斑,并随着日龄的增长而更加明显,这种特征在霍氏中杜鹃(C.optatus)的雏鸟中也存在,但未见于其他种类的杜鹃雏鸟。     

The symbiotic water mite Unionicola formosa (Acari: Unionicolidae) ingests mucus and tissue of its molluscan host

Unionicola formosa is a symbiotic water mite that passes most of its life cycle in the mantle cavity of freshwater mussels. Although mites of this genus are often referred to as parasitic, little is known about their nutritional biology. A few species reportedly pierce the gill of a host mussel and ingest tissue or hemolymph. The present study was undertaken to identify possible sources of nutrition for U. formosa. To determine if mites ingested particulate matter in the mucous strand produced by a mussel during feeding, mussels with resident mites were exposed to a suspension of fluorescent microspheres. There was no evidence that U. formosa ingested the beads. Histochemical staining did, however, indicate a mucous material present in the midgut of the mites. Sodium dodecyl sulfate-polyacrylamide gel electrophoretic assays revealed a high molecular weight component, consistent with a mucopolysaccharide, present both in the mussel gill and the mites. Results from western blots and an immunoaffinity binding assay with antibodies against mussel gill tissue and hemolymph also indicated that mites ingested host tissue. Whereas U. formosa probably does not ingest particulate material acquired by its host's suspension feeding, it is apparent that this mite utilizes host mucus, gill tissue, or hemolymph for at least part of its nutrition.     

Parasites of the superorganism: are they indicators of ecosystem health?

The concept of ecosystem health is derived from analogies with human health, which subsequently leads to the implication that the ecosystem has organismal properties, a 'superorganism' in the Clementsian sense. Its application and usefulness has been the subject of a contentious debate; yet, the term 'ecosystem health' has captured the public's imagination and woven its way into the current lexicon, even incorporated into public policy. However, the application of parasites as bioindicators of ecosystem health poses a curious conundrum. Perceptions of parasites range from mild distaste to sheer disgust among the general public, the media, environmental managers and non-parasitologists in the scientific community. Nevertheless, the biological nature of parasitism incorporates natural characteristics that are informative and useful for environmental management. The helminths in particular have evolved elegant means to ensure their transmission, often relying on complex life cycle interactions that include a variety of invertebrate and vertebrate hosts. The assemblage of these diverse parasites within a host organism potentially reflect that host's trophic position within the food web as well as the presence in the ecosystem of any other organisms that participate in the various parasite life cycles. Perturbations in ecosystem structure and function that affect food web topology will also impact upon parasite transmission, thus affecting parasite species abundance and composition. As such, parasite populations and communities are useful indicators of environmental stress, food web structure and biodiversity. In addition, there may be useful other means to utilise parasitic organisms based on their biology and life histories such as suites or guilds that may be effective bioindicators of particular forms of environmental degradation. The challenge for parasitology is to convince resource managers and fellow scientists that parasites are a natural part of all ecosystems, each species being a potentially useful information unit, and that healthy ecosystems have healthy parasites.     

External structure of cuticle injuries and larval mouth parts of the chiggers Euschoengastia rotundata and Neotrombicula vulgaris (Trombiculidae)

When E. rotundata larvae parasitize the abdominal part of the body of their host (Clethrionomys glareolus), capsules with round terminal opening are formed from which hind part of the mite's body projects forwards. Organization of the capsules shows that their walls are formed by a substance (probably by larval saliva) which differs from host's tissues. At the bottom of the capsules there are larval adhesive sites with openings in the proximal parts of stylostomes which resemble in their structure these of N. vulgaris larvae. The latter do not form capsules when feeding on their natural hosts, Microtus arvalis. Proximal part of stylostome is formed in both cases by amorphous glutinous substance bearing imprints of mite's mobile digits of chelicerae and hypostome. Mouth parts of hungry mites and satiated larvae of both species differ only in relative sizes of constituent parts. Soft apical part of hypostome turns backwards during the feeding and forms a sucker. The feeding of larvae of trombiculids in capsules, which is formally regarded as ectoparasitism, can apparently be considered as a special type of parasitism.     

Condition and fecundity of the damselfly,Enallagma ebrium (Hagen): the importance of ectoparasites

Summary The extent, magnitude, and cause of natural covariation between degree of parasitism and other variables known or suspected of influencing host fitness (such as host age or body size) has been understudied. We demonstrate that degree of parasitism by larval water mites (Arrenurus spp.) was associated with reduced condition of males and with lowered fecundity of young females of the damselfly, Enallagma ebrium (Hagen) (Odonata: Coenagrionidae). We also demonstrate that degree of parasitism can covary with both age and size of host damselflies. We explain the putative causes of such natural covariation, and we suggest that degree of parasitism, host age, and host size can all interact to determine damselfly fitness. We expect that natural covariation between the host's phenotype and degree of parasitism will be frequently observed. Studies of such natural covariation will help researchers to assess better the importance of several variables on host reproductive success and to understand better the dynamics of host-parasite interactions.     

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.     

Integrative neuroimmunomodulation of gastrointestinal function during enteric parasitism.

Enteric helminths have a significant impact on the structure, function, and neural control of the gastrointestinal (GI) tract of the host. Interactions between the host's nervous and immune systems redirect activity in neuronal circuits intrinsic to the gut into an alternative repertoire of defensive and adaptive motor programs. Gut inflammation and activation of the enteric neuroimmune axis play integral roles in the dynamic interaction between host and parasite that occurs at the mucosal surface. Three inter-related themes are stressed in this review to underscore the pivotal role that neural control mechanisms play in the host's GI tract functional responses to enteric parasitism. First, we address the discovery that signaling molecules of both parasite and host origin can reorient the dynamic ecology of enteric host-parasite interactions. Second, we explore what has been learned from investigations of altered gut propulsive and secretomotor reflex activities that occur during enteric parasitic infections and the emerging picture derived from these studies that elucidates how nerves help facilitate and orchestrate functional reorganization of the parasitized gut. Third, we provide an overview of the direct impact that enteric parasitism has on nerve cell function and neurotransmission pathways in both the enteric and central nervous systems of the host. In summary, this review highlights and clarifies the complex mechanisms underlying integrative neuroimmunophysiological responses to the presence of both invasive and noninvasive enteric helminths and identifies directions for future research investigations in this highly important but understudied area.     

The adaptive significance of inquiline parasite workers

Social parasites exploit the socially managed resources of their host's society. Inquiline social parasites are dependent on their host throughout their life cycle, and so many of the traits inherited from their free-living ancestor are removed by natural selection. One trait that is commonly lost is the worker caste, the functions of which are adequately fulfilled by host workers. The few inquiline parasites that have retained a worker caste are thought to be at a transitional stage in the evolution of social parasitism, and their worker castes are considered vestigial and non-adaptive. However, this idea has not been tested. Furthermore, whether inquiline workers have an adaptive role outside the usual worker repertoire of foraging, brood care and colony maintenance has not been examined. In this paper, we present data that suggest that workers of the inquiline ant Acromyrmex insinuator play a vital role in ensuring the parasite's fitness. We show that the presence of these parasite workers has a positive effect on the production of parasite sexuals and a negative effect on the production of host sexuals. This suggests that inquiline workers play a vital role in suppressing host queen reproduction, thus promoting the rearing of parasite sexuals. To our knowledge, these are the first experiments on inquiline workers and the first to provide evidence that inquiline workers have an adaptive role.