Do avian brood parasites eavesdrop on heterospecific sexual signals revealing host quality? A review of the evidence

Eavesdropping can be defined as the extraction of information from the interactions between other individuals. It provides a relatively cheap way of gathering relevant information for fitness enhancement. Here, we propose that obligate avian brood parasites, which always lay their eggs in foreign nests of individuals of other species, may eavesdrop on their host sexual signals to locate nests of high quality individuals in which to lay their parasitic eggs. Sexual signal variation can honestly signal parental quality. Thus, by eavesdropping on sexual signals, parasites may select high quality foster parents for their own offspring. Such a use of sexual signals within host populations by brood parasites differs from signal exploitation theory that proposes that parasite only use signals to locate potential host independently from signaller quality. Here, we review the avian literature concerning host choice within a host species by obligate avian brood parasites and find evidence for host selection within individuals of a host species on the basis of cues potentially functioning as sexually selected traits, or at least revealing parental abilities. We have also found support for the existence of benefits linked to host selection by avian brood parasites. Finally, one study reported on the attenuation of a sexual ornament in host populations under strong pressure by brood parasites. Most of these findings have been interpreted as evidence for host selection by avian brood parasites based on the conspicuousness of sexual signals. We suggest, however, that these findings may in fact reveal eavesdropping on host signalling performance by brood parasites which would use the information extracted to choose the better individuals among conspecifics of a given host. This provides a new perspective for the study of host selection in obligate brood parasites, and raises interesting questions for the study of animal cognition that would deserve experimental studies.     

Lower begging responsiveness of host versus parasitic brown-headed cowbird (Molothrus ater) nestlings is related to species identity but not to early social experience

The survival of young brood parasites depends critically on their many adaptations to exploit hosts. Parasitic survival is particularly related to competitive superiorty for foster parental care whenever host young are not destroyed in parasitized nests.Brown-headed cowbirds (Molothrus ater) are generalist obligate parasites whose early social environments are unpredictable regarding host species and numbers of nestmates. Young avian brood parasites typically beg more intensively and loudly than foster siblings, but an untested prediction is that young parasites are also more likely to respond by begging to a wider variety of stimulus types. Avian vocalizations were used in a playback experiment to stimulate begging behavior in cowbird hosts. Compared with age-matched cowbird nestlings, hosts begged less frequently to acoustic stimuli, and lower begging responsiveness was irrespective of whether hosts had been reared in parasitized nests.     

Innate versus learned recognition of conspecifics in great spotted cuckoos Clamator glandarius

When birds raised by another species become adults, they (if they are non-brood-parasitic species) usually attempt to mate with birds of their foster species rather than with birds of their own species, a phenomenon called sexual imprinting. Avian brood parasites lay their eggs in nests of other species (the hosts) that rear the young, but the problem of sexual imprinting among brood parasites has generally been neglected, and brood parasites have been considered as an exception among birds. Here, we show, with data from field observations and field experiments, firstly, that adult great spotted cuckoos Clamator glandarius sometimes maintain contact with both older nestling and fledgling cuckoos. Adult cuckoos visited parasitized nests during the last days of the nestling period (5 observations) and, when parasitic chicks left the nest, adult cuckoos maintained contact with the young (14 observations). Adults and fledgling cuckoos communicated vocally (5 observations), and an adult great spotted cuckoo even fed a parasite fledgling in two cases. Secondly, when experimentally cross-fostered in nests of magpie Pica pica hosts outside the parasite breeding range (thus avoiding visual and acoustic communication with adult cuckoos), young cuckoos did not learn to recognize their own species when only one cuckoo chick was introduced per nest, but they learnt to recognize conspecifics when two cuckoos were reared together. This means that young great spotted cuckoos apparently must learn to recognize conspecifics, that is, recognition is not innate. Social interactions between adult brood parasites and young have also been reported in other brood parasites; thus, brood parasites are probably not an exception to the general phenomenon of imprinting, and young brood parasites may need to be imprinted on conspecifics, although more studies on other brood parasite species are needed to confirm this. Received: 7 January 1999 / Accepted after revision: 27 February 1999     

Condition-dependent adaptive phenotypic plasticity and interspecific gene-culture coevolution

Evolutionary socioecological theory and research proposing linking parasites with human social organization is uncommon and therefore welcome. However, more generally, condition-dependent adaptive phenotypic plasticity requires environmental uncertainty on a small scale, accompanied by reliable cues. In addition, genes in parasites may select among biologically adaptive cultural alternatives directly without necessarily going through human genetic predispositions, resulting in inter-specific gene-culture coevolution.     

血吸虫逃避补体杀伤的机制研究

寄生虫免疫逃避的机理非常复杂,且随着虫种,生活史阶段的不同而不同。传统的对寄生虫免疫逃避的解释的有抗原变异,抗原伪装等等,现在的研究认为,一些补体调节因子,如ＣＤ５５ＣＤ５９等可能在血吸虫童虫逃避补体杀伤中起重要作用。     

Parasites of the mind. Why cultural theorists need the meme’s eye view

Are there any such things as mind parasites? By analogy with biological parasites, such cultural items are supposed to subvert or harm the interests of their host. The hypothesis of cultural parasitism has appeared in different guises in the burgeoning field of cultural evolution. To unpack the notion of mind parasites, we first clear some conceptual ground around the concept of cultural adaptation and its relation to human agency. We then formulate Millikan’s challenge: how can cultural items develop novel purposes of their own, cross-cutting or subverting our own personal purposes? If this central challenge is not met, talk of cultural ‘parasites’ or ‘selfish memes’ remains vacuous. First, we discuss why other attempts to answer Millikan’s challenge have failed. In particular, we put to rest the claims of panmemetics, a somewhat sinister worldview according to which human culture is nothing more than a swarm of selfish agents, plotting and scheming behind the scenes. Next, we reject a more reasonable, but still overly permissive approach to mind parasites, which equates them with biologically maladaptive culture. Finally, we present our own answer to Millikan’s challenge: certain systems of misbelief can be fruitfully treated as cultural parasites, designed by cultural evolution to subvert the interests of their human hosts. As a proof of concept, we discuss witchcraft beliefs in early modern Europe, and show how the meme’s eye view promises to shed new light on a mystery that historians and social scientists have been wrestling with for decades.     

The evolution and development of human social systems requires more than parasite-stress avoidance explanation

Fincher & Thornhill (F&T) present a model of in-group assortative sociality resulting from differing levels of parasite-stress in differing geographical locations in the United States and the world. Their model, while compelling, overlooks some important issues, such as mutualistic associations with parasites that are beneficial to humans and how some religious practices increase parasite risk.     

Immigration, parasitic infection, and United States religiosity

Fincher & Thornhill (F&T) present a powerful case for the relationship between parasite-stress and religiosity. We argue, however, that the United States may be more religious than can be accounted for by parasite-stress. This greater religiosity might be attributable to greater sensitivity to immigration, which may hyperactivate evolved mechanisms that motivate avoidance of potential carriers of novel parasites.     

Self-referent phenotype matching in a brood parasite: the armpit effect in brown-headed cowbirds (Molothrus ater)

Most birds and mammals learn characteristics of conspecifics from their parents and siblings. In interspecific brood parasites, however, early social learning could lead to species recognition errors because young are reared among heterospecifics. Conceivably, juvenile parasites might inspect and memorize aspects of their own phenotype, and later match features of encountered individuals to that template. We tested for such self-referent phenotype matching by manipulating feather colors of hand-reared fledglings (n = 21) of the parasitic brown-headed cowbird (Molothrus ater). In simultaneous choice trials (n = 6 trials/subject) between dyed and normal-colored adult females, juvenile cowbirds (< 2 months old) approached more quickly and associated preferentially with individuals that were colored similar to themselves. These preferences remained even when differences between the associative behaviors of juvenile males and females were controlled statistically. Our data imply that cowbirds incorporate their own plumage color into their recognition template. This provides the first evidence of self-referent phenotype matching through experimental manipulation of a recognition cue. Received: 11 April 2000 / Accepted after revision: 2 September 2000     

囊虫病诊断技术的发展与临床应用

囊虫病是一种由猪囊尾蚴寄生于人体组织内主要引起脑、眼等重要器官或组织损害的常见寄生虫病。目前对其诊断的实验技术研究已发展到高层水平,但被临床应用的并不多。本文从多个方面较全面地分析和回答了出现此现象的原因,并提出了拟解决临床问题的见解与探索思路。     

Using trained pouched rats to detect land mines: another victory for operant conditioning

We used giant African pouched rats (Cricetomys gambianus) as land mine-detection animals in Mozambique because they have an excellent sense of smell, weigh too little to activate mines, and are native to sub-Saharan Africa, and therefore are resistant to local parasites and diseases. In 2009 the rats searched 93,400 m(2) of land, finding 41 mines and 54 other explosive devices. Humans with metal detectors found no additional mines. On average, the rats emitted 0.33 false alarm for every 100 m(2) searched, which is below the threshold given by International Mine Action Standards for accrediting mine-detection animals. These findings indicate that Cricetomys are accurate mine-detection animals and merit continued use in this capacity.     

Zoonotic and non-zoonotic diseases in relation to human personality and societal values: Support for the parasite-stress model

The parasite-stress model of human sociality proposes that humans' ontogenetic experiences with infectious diseases as well as their evolutionary historical interactions with these diseases exert causal influences on human psychology and social behavior. This model has been supported by cross-national relationships between parasite prevalence and human personality traits, and between parasite prevalence and societal values. Importantly, the parasite-stress model emphasizes the causal role of non-zoonotic parasites (which have the capacity for human-to-human transmission), rather than zoonotic parasites (which do not), but previous studies failed to distinguish between these conceptually distinct cate- gories. The present investigation directly tested the differential predictive effects of zoonotic and non-zoonotic (both human-specific and multihost) parasite prevalence on personality traits and societal values. Supporting the parasite-stress model, cross-national differences in personality traits (unrestricted sexuality, extraversion, openness to experi- ences) and in societal values (individualism, collectivism, gender equality, democratiza- tion) are predicted specifically by non-zoonotic parasite prevalence.     

On the adaptive origins and maladaptive consequences of human inbreeding: Parasite prevalence, immune functioning, and consanguineous marriage

We propose that consanguineous marriages arise adaptively in response to high parasite prevalence and function to maintain coadapted gene complexes and associated local adaptation that defend against local pathogens. Therefore, a greater prevalence of inbreeding by consanguineous marriage is expected in geographical regions that historically have had high levels of disease-causing parasites. Eventually such marriages may, under the contemporary high movement of people with modern transportation, jeopardize the immunity of those who practice inbreeding as this leads to an increased susceptibility to novel pathogens. Therefore, a greater frequency of inbreeding is expected to predict higher levels of contemporary mortality and morbidity from infectious diseases. This parasite model of human inbreeding was supported by an analysis involving 72 countries worldwide. We found that historically high levels of pathogen prevalence were related positively to the proportion of consanguineous marriages, and that a higher prevalence of such marriages was associated with higher contemporary mortality and morbidity due to pathogens. Our study addresses plausible alternative explanations. The results suggest that consanguineous marriage is an adaptive consequence of historical pathogen ecologies, but is maladaptive in contemporary disease ecologies.     

Health Is Associated With Antiparasite Behavior and Fear of Disease-Relevant Animals in Humans

Evolutionary arms races between humans and parasites resulted in a set of behavioral adaptations that serve as parasite-avoidance mechanisms. We investigated associations among reported health of the respondent, antiparasite behavior, and sensitivity to disgust and fear of disease-relevant and irrelevant animals. Ninety-seven participants (15–19 years old) rated their fear and disgust at 25 colorful pictures of disease-relevant and disease-irrelevant invertebrates. Consistent with previous work, we found that participants reported greater fear and disgust of disease-relevant invertebrates relative to disease-irrelevant invertebrates. Better perceived health correlated with lower fear of disease-relevant invertebrates. Sensitivity to disgust correlated with reported antiparasite behaviors. Contrary to expectations, we found a positive correlation between antiparasite behavior and reported health, which suggests that antiparasite behavior influences perceived health (but not vice versa), and we found that males perform more antiparasite behaviors than females. These results support the idea that disgust and fear of disease-relevant objects are adaptive emotions that prevent contact with contagious objects, especially in individuals with low perceived health.     

Parasite-stress promotes in-group assortative sociality: the cases of strong family ties and heightened religiosity

Throughout the world people differ in the magnitude with which they value strong family ties or heightened religiosity. We propose that this cross-cultural variation is a result of a contingent psychological adaptation that facilitates in-group assortative sociality in the face of high levels of parasite-stress while devaluing in-group assortative sociality in areas with low levels of parasite-stress. This is because in-group assortative sociality is more important for the avoidance of infection from novel parasites and for the management of infection in regions with high levels of parasite-stress compared with regions of low infectious disease stress. We examined this hypothesis by testing the predictions that there would be a positive association between parasite-stress and strength of family ties or religiosity. We conducted this study by comparing among nations and among states in the United States of America. We found for both the international and the interstate analyses that in-group assortative sociality was positively associated with parasite-stress. This was true when controlling for potentially confounding factors such as human freedom and economic development. The findings support the parasite-stress theory of sociality, that is, the proposal that parasite-stress is central to the evolution of social life in humans and other animals.     

Effects of repetitive stress during the acute phase of Trypanosoma cruzi infection on chronic Chagas' disease in rats

The effect of repetitive stress during acute infection with Trypanosoma cruzi (T. cruzi) on the chronic phase of ensuing Chagas' disease was the focus of this investigation. The aim of this study was to evaluate in Wistar rats the influence of repetitive stress during the acute phase of infection (7 days) with the Y strain of T. cruzi on the chronic phase of the infection (at 180 days). Exposure to ether vapor for 1 min twice a day was used as a stressor. Repetitive stress enhanced the number of circulating parasites and cardiac tissue disorganization, from a moderate to a severe diffuse mononuclear inflammatory process and the presence of amastigote burden in the cardiac fibers. Immunological parameters revealed that repetitive stress triggered a reduced concanavalin A induced splenocyte proliferation in vitro with major effects on the late chronic phase. Serum interleukin-12 concentration decreased in both stressed and infected rats in the early phase of infection although it was higher on 180 days post-infection. These results suggest that repetitive stress can markedly impair the host's immune system and enhance the pathological process during the chronic phase of Chagas' disease.     

Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite

Brood parasitism imposes several fitness costs on the host species. To reduce these costs, hosts of avian brood parasites have evolved various defenses, of which egg rejection is the most prevalent. In the face of variable host-parasite mimicry and the costs of egg discrimination itself, many hosts reject only some foreign eggs. Here, we experimentally varied the recognition cues to study the underlying cognitive mechanisms used by the Chalk-browed Mockingbird (Mimus saturninus) to reject the white immaculate eggs laid by the parasitic Shiny Cowbird (Molothrus bonariensis). Immaculate eggs are the only parasite eggs rejected by this host, as it accepts all polymorphic, spotted eggs laid by cowbirds. Using a within-breeding pair experimental design, we tested for the salience of spotting, UV reflectance, and brightness in eliciting rejection. We found that the presence of spotting significantly decreased the probability of rejection while increments in brightness significantly increased rejection frequencies. The cognitive rules underlying mockingbird rejection behavior can be explained by a decision-making model which predicts changes in the levels of rejection in direct relation to the number of relevant attributes shared between host and parasite eggs.     

Disgusting clusters: trypophobia as an overgeneralised disease avoidance response

Individuals with trypophobia have an aversion towards clusters of roughly circular shapes, such as those on a sponge or the bubbles on a cup of coffee. It is unclear why the condition exists, given the harmless nature of typical eliciting stimuli. We suggest that aversion to clusters is an evolutionarily prepared response towards a class of stimuli that resemble cues to the presence of parasites and infectious disease. Trypophobia may be an exaggerated and overgeneralised version of this normally adaptive response. Consistent with this explanation, individuals with trypophobia, as well as comparison individuals, reported aversion towards disease-relevant cluster stimuli, but only the trypophobic group reported aversion towards objectively harmless cluster stimuli that had no relevance to disease. For both groups the level of aversion reported was predicted uniquely by a measure of disgust sensitivity. Scaled emotion ratings and open-ended responses revealed that the aversive response was predominantly based on the disease avoidance emotion, disgust. Many open-ended responses also described skin sensations (e.g. skin itching or skin crawling). These findings support the proposal that individuals with trypophobia primarily perceive cluster stimuli as cues to ectoparasites and skin-transmitted pathogens.     

Scary and nasty beasts: Self-reported fear and disgust of common phobic animals

Animal phobias are one of the most prevalent mental disorders. We analysed how fear and disgust, two emotions involved in their onset and maintenance, are elicited by common phobic animals. In an online survey, the subjects rated 25 animal images according to elicited fear and disgust. Additionally, they completed four psychometrics, the Fear Survey Schedule II (FSS), Disgust Scale – Revised (DS-R), Snake Questionnaire (SNAQ), and Spider Questionnaire (SPQ). Based on a redundancy analysis, fear and disgust image ratings could be described by two axes, one reflecting a general negative perception of animals associated with higher FSS and DS-R scores and the second one describing a specific aversion to snakes and spiders associated with higher SNAQ and SPQ scores. The animals can be separated into five distinct clusters: (1) non-slimy invertebrates; (2) snakes; (3) mice, rats, and bats; (4) human endo- and exoparasites (intestinal helminths and louse); and (5) farm/pet animals. However, only snakes, spiders, and parasites evoke intense fear and disgust in the non-clinical population. In conclusion, rating animal images according to fear and disgust can be an alternative and reliable method to standard scales. Moreover, tendencies to overgeneralize irrational fears onto other harmless species from the same category can be used for quick animal phobia detection.     

Statistical inference and spatial patterns in correlates of IQ

Cross-national comparisons of IQ have become common since the release of a large dataset of international IQ scores. However, these studies have consistently failed to consider the potential lack of independence of these scores based on spatial proximity. To demonstrate the importance of this omission, we present a re-evaluation of several hypotheses put forward to explain variation in mean IQ among nations namely: (i) distance from central Africa, (ii) temperature, (iii) parasites, (iv) nutrition, (v) education, and (vi) GDP. We quantify the strength of spatial autocorrelation (SAC) in the predictors, response variables and the residuals of multiple regression models explaining national mean IQ. We outline a procedure for the control of SAC in such analyses and highlight the differences in the results before and after control for SAC. We find that incorporating additional terms to control for spatial interdependence increases the fit of models with no loss of parsimony. Support is provided for the finding that a national index of parasite burden and national IQ are strongly linked and temperature also features strongly in the models. However, we tentatively recommend a physiological - via impacts on host-parasite interactions - rather than evolutionary explanation for the effect of temperature. We present this study primarily to highlight the danger of ignoring autocorrelation in spatially extended data, and outline an appropriate approach should a spatially explicit analysis be considered necessary.