Schistosoma mansoni: human skin ceramides are a chemical cue for host recognition of cercariae

Schistosoma mansoni cercariae recognize the human host with a sequence of behavioral responses particularly to chemical host cues. After attaching to the skin surface, cercariae are stimulated by so far unknown skin components to hold enduring contact with the skin and to start creeping towards entry sites. We studied the chemical stimulus of human skin for the cercarial enduring contact response by fractionation of human and pig skin surface extracts and offering the fractions to the cercariae via membrane filters. Enduring contact was stimulated exclusively by ceramides, specific lipids of the uppermost skin layers. This chemical cue differs from the 6 chemical host signals used by S. mansoni cercariae in other behavioral steps of host invasion, and thus underlines the specialization of S. mansoni cercariae particularly in chemical host signals. All together, the enduring contact response of the cercariae is, like the other phases of host invasion, well adapted to the chemical properties of human skin.     

EVOLUTIONARY PATTERNS OF ALTERED BEHAVIOR AND SUSCEPTIBILITY IN PARASITIZED HOSTS

Adaptation is the usual context for interpreting parasite-host interactions. For example, altered host behavior is often interpreted as a parasite adaptation, because in some cases it enhances parasite transmission. Resistance to parasites also has obvious adaptive value for hosts. However, it is difficult to evaluate the adaptive significance of host-parasite interactions without considering the historical context in which these traits have evolved and if they can be predicted by host (or parasite) phylogeny. We examined the influence of host phylogeny on patterns of altered behavior and resistance to parasitism in a cockroach-acanthocephalan system. A consensus cladogram for cockroach subfamilies was produced from the morphological data of McKittrick. We used this cladogram to predict patterns of altered host behavior in seven cockroach host species. Each species was experimentally infected with a single species of acanthocephalan, Moniliformis moniliformis, a parasite that is transmitted when cockroaches are eaten by rodent final hosts. Activity patterns, substrate choices, and responses to light were measured for control and infected animals. These data were recoded into a behavioral matrix of discrete characters. We determined the most parsimonious distribution of the behavioral characters on the tree obtained from McKittrick's data. We then measured the concordance between the behavioral data and the cockroach cladogram with the consistency index (CI). We compared the observed CI to the expected value based on a randomization of observed character states. For three different models of evolutionary character change, there was no evidence of strong concordance (significantly large CI) between altered host behavior and host relationships. Parsimony analysis of the interior nodes of the phylogenetic reconstruction suggested that unaltered behavior was the ancestral state for most host behaviors. We also compared host phylogeny to a data set on the susceptibility of 29 cockroach species to infection with M. moniliformis. At the species level, there was a significant concordance between susceptibility and host phylogeny. This pattern was consistent with the finding that susceptibility of species varied significantly among different subfamilies. However, at the subfamily level, susceptibility was not strongly concordant with phylogeny. We predict that, given enough time, resistance should be lost in subfamilies that are currently resistant to parasitism. In spite of the potential importance of phylogeny in the evolution of behavior and susceptibility, we found little evidence for phylogenetic effects in this system. We conclude that changes in the behavioral responses of hosts to parasites and, to a lesser extent, changes in susceptibility are more frequent than cockroach speciation events in different cockroach lineages. This finding strengthens the assertion that at least some of the altered behaviors are adaptive for host and/or parasite.     

Host identification by Schistosoma japonicum cercariae

Attachment, the first phase of host identification by Schistosoma japonicum cercariae, can occur in 2 different ways. Cercariae clinging to the water surface simply swing around and transfer to the host skin. Free-swimming cercariae behave like S. mansoni: upon touching a substrate, they switch from tailward to forward movement, swim in an arc, and attach to it with the penetration organ. Neither type of attachment is influenced by chemical, thermal, or specific mechanical stimuli from the host. The second phase, remaining on the host, requires a solid hydrophobic surface and seems to depend only on the cercaria's ability to cling to it. This phase is not influenced by chemical or thermal stimuli. The third phase, creeping across the host surface, is independent of chemical and mechanical stimuli. Cercariae migrate in thermal gradients to a preferred temperature of 37 +/- 3 C and then attempt to penetrate. Penetration, the fourth phase, was evoked by human skin surface lipids. The free fatty acid (FA) fraction was identified as exclusively stimulating components. Saturated FA's were effective at chain lengths between 10 and 14 carbon atoms (pH 7.0), and unsaturated FA's were effective at longer chains and their activity increased with increasing number of double bonds. Dog skin surface components did not stimulate cercarial penetration, which can be attributed to the lack of free FA's. A temperature of 32-40 C also stimulated penetration responses, which might be the main stimulus in animal hosts, whose skin surfaces contain no or only a few free FA's. FA's and heat evoked a transformation of cercarial tegument simultaneous with penetration behavior, making the organisms osmotically sensitive. The host identification of S. japonicum cercariae is very nonspecific compared with the differentiated host recognition of S. mansoni.     

Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages

The transmission stages of parasites are key determinants of parasite fitness, but they also incur huge mortality. Yet the selective forces shaping the sizes of transmission stages remain poorly understood. We ran a comparative analysis of interspecific variation in the size of transmission stages among 404 species of parasitic trematodes. There are two transmission steps requiring infective stages in the life cycle of trematodes: transmission from the definitive to the first intermediate (snail) host is achieved by eggs and/or the miracidia hatched from those eggs, and transmission from the first to the second intermediate host is achieved by free-swimming cercariae. The sizes of these stages are under strong phylogenetic constraints. Our results show that taxonomy explains >50% of the unaccounted variance in linear mixed models, with most of the variance occurring at the superfamily level. The models also demonstrated that mollusc size is positively associated with egg volume, miracidial volume and cercarial body volume, but not with the relative size of the cercarial tail. In species where they encyst on substrates, cercariae have significantly larger bodies than in species penetrating chordates, although the relative size of the cercarial tail of species using chordates as second intermediate hosts was larger than in other trematode species. Habitat also matters, with larger cercarial tails seen in freshwater trematodes than in marine ones, and larger miracidial volumes in freshwater species than in marine ones. Finally, the latitude (proxy for local temperature) at which the trematode species were collected had no effect on the sizes of transmission stages. We propose that resource availability within the snail host, the probability of contacting a host, and the density and viscosity of the water medium combine to select for different transmission stage sizes.     

Essay on Contemporary Issues in Ethology: Variation among Mammalian Alarm Call Systems and the Problem of Meaning in Animal Signals

Understanding the information conveyed by animal signals requires studies of both production and perception. It is important to determine the relationship between signal morphology and the circumstances of production, the way signaller behavior varies with motivational state and the role of context in mediating responses to signals. Alarm calls are well-suited to research of this type because they are widespread in birds and mammals and typically evoke unambiguous responses. We review studies of alarm calling in primates and ground-dwelling sciurid rodents, concentrating especially on whether these signal systems may be viewed as ‘functionally referential’, that is, as conveying sufficient information about an event for receivers to select appropriate responses. Comparisons of the physical, behavioral and habitat characteristics of these species suggest that incompatibility of the escape responses required to avoid different classes of predators may have been an important factor in the evolution of functionally referential alarm calls.     

Cercarial kissing marks-no superficial make-up

In the presence of fluorochrome-conjugated lectins, the products of schistosome cercarial penetration glands can be visualized as distinct deposits, or 'kissing marks', at sites of attachment and attempted penetration of the host's skin. Ewert Linder has observed that 'kissing marks' are also recognized by antibodies present in the schistosome-infected host. This has raised the question of whether cercarial secretions or antigenically related products play a role within the infected host, and has motivated studies on the distribution of such antigens in the parasite at different developmental stages.     

An ethogram of body patterning behavior in the biomedically and commercially valuable squid Loligo pealei off Cape Cod, Massachusetts.

Squids have a wide repertoire of body patterns; these patterns contain visual signals assembled from a highly diverse inventory of chromatic, postural, and locomotor components. The chromatic components reflect the activity of dermal chromatophore organs that, like the postural and locomotor muscles, are controlled directly from the central nervous system. Because a thorough knowledge of body patterns is fundamental to an understanding of squid behavior, we have compiled and described an ethogram (a catalog of body patterns and associated behaviors) for Loligo pealei. Observations of this species were made over a period of three years (> or = 440 h) and under a variety of behavioral circumstances. The natural behavior of the squid was filmed on spawning grounds off Cape Cod (northwestern Atlantic), and behavioral trials in the laboratory were run in large tanks. The body pattern components--34 chromatic (including 4 polarization components), 5 postural, and 12 locomotor--are each described in detail. Eleven of the most common body patterns are also described. Four of them are chronic, or long-lasting, patterns for crypsis; an example is Banded Bottom Sitting, which produces disruptive coloration against the substrate. The remaining seven patterns are acute; they are mostly used in intraspecific communication among spawning squids. Two of these acute patterns--Lateral Display and Mate Guarding Pattern--are used during agonistic bouts and mate guarding; they are visually bright and conspicuous, which may subject the squids to predation; but we hypothesize that schooling and diurnal activity may offset the disadvantage presented by increased visibility to predators. The rapid changeability and the diversity of body patterns used for crypsis and communication are discussed in the context of the behavioral ecology of this species.     

PATHWAYS TO SOCIAL EVOLUTION: RECIPROCITY,RELATEDNESS, AND SYNERGY

Many organisms live in populations structured by space and by class, exhibit plastic responses to their social partners, and are subject to nonadditive ecological and fitness effects. Social evolution theory has long recognized that all of these factors can lead to different selection pressures but has only recently attempted to synthesize how these factors interact. Using models for both discrete and continuous phenotypes, we show that analyzing these factors in a consistent framework reveals that they interact with one another in ways previously overlooked. Specifically, behavioral responses (reciprocity), genetic relatedness, and synergy interact in nontrivial ways that cannot be easily captured by simple summary indices of assortment. We demonstrate the importance of these interactions by showing how they have been neglected in previous synthetic models of social behavior both within and between species. These interactions also affect the level of behavioral responses that can evolve in the long run; proximate biological mechanisms are evolutionarily stable when they generate enough responsiveness relative to the level of responsiveness that exactly balances the ecological costs and benefits. Given the richness of social behavior across taxa, these interactions should be a boon for empirical research as they are likely crucial for describing the complex relationship linking ecology, demography, and social behavior.     

Possible involvement of microcystins in the unexplained mass mortalities of Lesser Flamingo (<Emphasis Type="Italic">Phoeniconaias minor</Emphasis> Geoffroy) at Lake Manyara in Tanzania

We examined the effects of food and light on the swimming behavior of nauplii of the cyclopoid Apocyclops royi (Lindberg, 1940) (Copepoda: Cyclopoida) and the calanoid Pseudodiaptomus annandalei Sewell, 1919 (Copepoda: Calanoida). Several behavioral parameters such as swimming patterns, speed, and trajectories exhibited distinct ontogenetic differences between the two species. When algae Isochrysis galbana (Haptophyta: Isochrysidales) were offered as food to the nauplii of A. royi, they showed fast circle swimming behavior, while nauplii of P. annandalei never exhibited such behavior, neither with, nor without algae. The different behavioral patterns between the nauplii of both species suggest they both have different foraging strategies in detecting and capturing food.     

The physiology of itch

The perception of itch is associated with many parasites and their vectors, especially following penetration of the skin by the parasites themselves, as in cercarial dermatitis of schistosome infections, or penetration of arthropod mouthparts during blood feeding. Many ectoparasites such as scabies, lice and fleas, provoke sensations of itch - even when the insects are no longer (or have never been) present, giving rise to the phenomenon of delusory parasitosis. Itch, and the host 'grooming' responses with which it is associated, is increasingly recognized as an important factor in modulating vector feeding behaviour, which can have profound effects on the transmission dynamics of vector borne parasites. As a background to future reviews of this developing subject, we asked John Alexander, author of the classic Arthropods and Human Skin (Springer-Verlag, 1984), to explain what is itch, and to discuss what is known about its underlying Physiology.     

Mirror-induced behavior in the magpie (Pica pica): evidence of self-recognition

Comparative studies suggest that at least some bird species have evolved mental skills similar to those found in humans and apes. This is indicated by feats such as tool use, episodic-like memory, and the ability to use one's own experience in predicting the behavior of conspecifics. It is, however, not yet clear whether these skills are accompanied by an understanding of the self. In apes, self-directed behavior in response to a mirror has been taken as evidence of self-recognition. We investigated mirror-induced behavior in the magpie, a songbird species from the crow family. As in apes, some individuals behaved in front of the mirror as if they were testing behavioral contingencies. When provided with a mark, magpies showed spontaneous mark-directed behavior. Our findings provide the first evidence of mirror self-recognition in a non-mammalian species. They suggest that essential components of human self-recognition have evolved independently in different vertebrate classes with a separate evolutionary history.     

非人灵长类冲突后行为的研究进展

冲突后行为（post-conflict behavior）在非人灵长类中普遍存在。通过对旧大陆灵长类和类人猿的冲突后行为的观察,人们早期主要关注其和解行为,随着研究的不断深入,近些年来则对转向攻击行为、安慰行为和替代和解行为等其他冲突后行为也多有涉猎。目前主要应用匹配控制观察法来研究灵长类的冲突后行为,发现不同的物种往往有不同的冲突后行为模式,她们的统治风格、亲豫关系、等级地位远近及冲突起因等因素会对冲突后行为产生影响,进而发现不同的冲突后行为模式具有不同的功能,并且提出了社会认知、社会约束和关系价值假说。     

The behavioral context of visual displays in common marmosets (Callithrix jacchus)

Communication is important in social species, and may occur with the use of visual, olfactory or auditory signals. However, visual communication may be hampered in species that are arboreal have elaborate facial coloring and live in small groups. The common marmoset fits these criteria and may have limited visual communication. Nonetheless, some (contradictive) propositions concerning visual displays in the common marmoset have been made, yet quantitative data are lacking. The aim of this study was to assign a behavioral context to different visual displays using pre–post‐event‐analyses. Focal observations were conducted on 16 captive adult and sub‐adult marmosets in three different family groups. Based on behavioral elements with an unambiguous meaning, four different behavioral contexts were distinguished: aggression, fear, affiliation, and play behavior. Visual displays concerned behavior that included facial expressions, body postures, and pilo‐erection of the fur. Visual displays related to aggression, fear, and play/affiliation were consistent with the literature. We propose that the visual display “pilo‐erection tip of tail” is related to fear. Individuals receiving these fear signals showed a higher rate of affiliative behavior. This study indicates that several visual displays may provide cues or signals of particular social contexts. Since the three displays of fear elicited an affiliative response, they may communicate a request of anxiety reduction or signal an external referent. Concluding, common marmosets, despite being arboreal and living in small groups, use several visual displays to communicate with conspecifics and their facial coloration may not hamper, but actually promote the visibility of visual displays. Am. J. Primatol. 75:1084–1095, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.     

Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae)

Sexual communication can contribute to population divergence and speciation because of its effect on assortative mating. We examined the role of communication in assortative mating in the Enchenopa binotata species complex of treehoppers. These plant-feeding insects are a well studied case of sympatric speciation resulting from shifts to novel host-plant species. Shifting to hosts with different phenologies causes changes in life-history timing. In concert with high host fidelity, these changes reduce gene flow between populations on ancestral and novel hosts and facilitate a rapid response to divergent natural selection. However, some interbreeding can still occur because of partial overlap of mating periods. Additional behavioral mechanisms resulting in reproductive isolation may thus be important for divergence. In E. binotata, mating pairs form after an exchange of plant-borne vibrational signals. We used playback experiments to examine the relevance of inter- and intraspecific variation in male advertisement signals for female mate choice in a member of the E. binotata species complex. Female signals given in response to male signals provided a simple and reliable assay. Male species and male individual identity were important determinants of female responses. Females failed to respond to the signals of the two most closely related species in the complex, but they responded strongly to the signals of conspecific males, as well as to those of the most basal species in the complex. Communication systems in the E. binotata species complex can therefore play a role in reproductive isolation. Female responses were influenced by among-individual variation in male signals and females, suggesting the involvement of sexual selection in the evolution of these communication systems.     

Evolution and Function of Drumming as Communication in Mammals

An amazing variety of mammals produce seismic vibrations bydrumming a part of their body on a substrate. The drumming cancommunicate multiple messages to conspecifics about territorialownership, competitive superiority, submission, readiness tomate, or presence of predators. Drumming also functions in interspecificcommunication when prey animals drum to communicate to predatorsthat they are too alert for a successful ambush. The diversityof mammals that drum in varied contexts suggest independentevolution in different lineages. Footdrumming, as with othersignals, probably originated by ritualization of older formsof behavior not associated with communication such as runningand digging. Footdrumming patterns are species specific andrange from single thumps to individual footdrum signatures.Although mammals communicate above ground with airborne drummingsignals, they can also transmit sound seismically into the burrowwhere the signals become airborne and are received with earsespecially adapted to hear low-frequency sound. Footdrumminghas been studied the most extensively in kangaroo rats, Dipodomys.A comparison of species of different body mass shows that smallersized, non-territorial species have no ritualized footdrumming;medium-sized species drum a simple pattern in limited contexts;while larger-sized species communicate territorial ownershipwith complex patterns. Future studies should examine the mechanicsand energy requirements of drumming to test hypotheses aboutbody size limitations on the evolution of footdrumming. Ourunderstanding of drumming as communication is limited untilinvestigators conduct field tests of responses to drumming signalsin the contexts in which the signals are generated.     

Changes in survival characteristics of Diplostomum spathaceum cercariae emerged from cadmium-exposed Lymnaea stagnalis

The effect of exposing Lymnaea stagnalis (Gastropoda: Pulmonata), infected with Diplostomum spathaceum (Trematoda: Diplostomatidae), to 100 microg l(-1) cadmium for 7 days on survival characteristics (survival, tail loss, decaudized cercarial life-span) of emerged cercariae was investigated. Exposure of L. stagnalis to cadmium resulted in significantly increased D. spathaceum cercarial survival and an inhibited tail loss compared to controls. The normal parallel relationship which exists over time between decreasing cercarial survival and increasing tail loss in controls was changed in cercariae from cadmium-exposed hosts with an increased proportion of cercarial deaths occurring without tail loss. The decaudized cercarial life-span over the survival period of the cercarial population did not significantly change. However comparisons between individuals decaudized during the initial 24 h time period with those which were decaudized during the final period of cercarial survival showed a significantly altered life span which did not occur in the control population. As a potential indicator of penetration 'fitness' comparisons were also undertaken between control and exposed cercariae decaudized during the initial 24 h time period, which revealed that the decaudized cercarial life-span from the exposed hosts was significantly different from controls. This may have important implications for the ability of cercariae to migrate through the tissues of their target host. The importance and relevance of these results to parasite transmission are discussed.     

Stress responses and the mesolimbic dopamine system: social contexts and sex differences

Organisms react to threats with a variety of behavioral, hormonal, and neurobiological responses. The study of biological responses to stress has historically focused on the hypothalamic-pituitary-adrenal axis, but other systems such as the mesolimbic dopamine system are involved. Behavioral neuroendocrinologists have long recognized the importance of the mesolimbic dopamine system in mediating the effects of hormones on species specific behavior, especially aspects of reproductive behavior. There has been less focus on the role of this system in the context of stress, perhaps due to extensive data outlining its importance in reward or approach-based contexts. However, there is steadily growing evidence that the mesolimbic dopamine neurons have critical effects on behavioral responses to stress. Most of these data have been collected from experiments using a small number of animal model species under a limited set of contexts. This approach has led to important discoveries, but evidence is accumulating that mesolimbic dopamine responses are context dependent. Thus, focusing on a limited number of species under a narrow set of controlled conditions constrains our understanding of how the mesolimbic dopamine system regulates behavior in response to stress. Both affiliative and antagonistic social interactions have important effects on mesolimbic dopamine function, and there is preliminary evidence for sex differences as well. This review will highlight the benefits of expanding this approach, and focus on how social contexts and sex differences can impact mesolimbic dopamine stress responses.     

Purification and properties of a proteolytic enzyme from the cercariae of the human trematode parasite Schistosoma mansoni.

Skin penetration by the cercarial stage of the human trematode parasite Schistosoma mansoni is mediated by the secretion of proteolytic enzymes able to digest components of mammalian connective tissues. In the present study the purification of these proteinases from cercarial homogenates is reported. The major proteinase species has a mol. wt. of approx. 25 000 and exists in monomeric form as determined by sodium dodecyl sulphate/polyacrylamide-gel electrophoresis. This proteinase has an isoelectric point of 6.0. Studies presented here, with a variety of substrates and inhibitors, confirm previous claims that these proteinases belong to the serine class, and, in addition, suggest that they resemble the vertebrate chymotrypsins rather than trypsins or elastases. However, the amino acid composition of the cercarial proteinase differs significantly from bovine chymotrypsin and from the human leucocyte chymotrypsin-like cathepsin G. The amino-acid-composition differences between these proteinases are consistent with their differences in isoelectric point. In order to obtain an insight into the role of the proteinase in skin penetration, its activity on cartilage proteoglycan monomers and on the isolated peptide backbone of proteoglycan was studied. The results of the present study indicate that the cercarial enzyme catalyses a limited specific digestion of the peptide core.     

Schistosoma mansoni: correlations between mouse strain, skin eicosanoid production, and cercarial skin penetration

We have previously reported that cercarial penetration is highly correlated with cercarial production of leukotrienes (LT's) and hydroxyeicosatetraenoic acids (HETE's). Because skin also produces various eicosanoids, we undertook an investigation of skin eicosanoids in various strains of mice and 1 strain of rat in order to ascertain if skin eicosanoids could be correlated to cercarial penetration. SENCAR, ICR, NMRI, A/J, C3H/HeJ, C57Bl/6, ASEBIC, and BALB/c mouse strains were used in this study as well as the SD-Rat strain. The ability of cercariae to penetrate skin was strain specific. A/J and SENCAR mice had the highest penetration rates (approximately 98%), whereas the SD-Rat strain had the lowest (43%). These penetration rates we linearly correlated with tail skin HETE production at 10 min (R = 0.826), whereas HETE production at 60 min had a parabola-shaped relationship (R = 0.793). The primary infection of mice with Schistosoma mansoni cercariae may therefore be directly correlated with both the skin's innate ability to synthesize HETE, as well as with cercarial eicosanoid production, especially HETE levels. However, we believe that skin eicosanoid production is just one of many factors affecting cercarial skin penetration. Other factors discussed are: skin surface fatty acid levels, cercarial eicosanoid production, epidermal vs. dermal eicosanoid production, and the immunocompetence of the host.     

Divergence in Olfactory Host Plant Preference in D. mojavensis in Response to Cactus Host Use

Divergence in host adaptive traits has been well studied from an ecological and evolutionary perspective, but identification of the proximate mechanisms underlying such divergence is less well understood. Behavioral preferences for host plants are often mediated by olfaction and shifts in preference may be accompanied by changes in the olfactory system. In this study, we examine the evolution of host plant preferences in cactophilic Drosophila mojavensis that feeds and breeds on different cacti throughout its range. We show divergence in electrophysiological responses and olfactory behavior among populations with host plant shifts. Specifically, significant divergence was observed in the Mojave Desert population that specializes on barrel cactus. Differences were observed in electrophysiological responses of the olfactory organs and in behavioral responses to barrel cactus volatiles. Together our results suggest that the peripheral nervous system has changed in response to different ecological environments and that these changes likely contribute to divergence among D. mojavensis populations.