Pathogen Avoidance Behaviours Research Articles

Social neuroscience of disgust.

Disgust can be thought of as an affective system that has evolved to detect signs of pathogens, parasite and toxins as well as to stimulate behaviors that reduce the risk of their acquisition. Disgust incorporates social cognitive mechanisms to regulate exposure to and, or anticipate and avoid exposure to pathogens and toxins. Social cognition entails the acquisition of social information about others (ie, social recognition) and from others (ie, social learning). This involves recognizing and assessing other individuals and the pathogen/parasite/contamination/toxin threat they pose and deciding about when and how to interact with and, or avoid them. Social cognition provides a frame-work for examining the expression of disgust and the associated neurobiological mechanisms. Here, we briefly consider the relations between social cognition and pathogen/parasite/toxin avoidance behaviors. We briefly discuss aspects of: (1) the odor mediated social recognition of actual and potentially infected individuals and the impact of parasite/pathogen threat on disgust mate and social partner choice; (2) the roles of "out-groups" (strangers, unfamiliar individuals) and "in-groups" (familiar individuals) in the expression of disgust and pathogen avoidance behaviors; (3) individual and social learning of disgust and empathy for disgust; (4) toxin elicited disgust and anticipatory disgust; (5) the neurobiological mechanisms, and in particular the roles of the nonapeptide, oxytocin and estrogenic mechanism associated with social cognition and the expression of disgust. These findings on the social neuroscience of disgust have a direct bearing on our understanding of the roles of disgust in shaping human and nonhuman social behavior.

The role of social cognition in parasite and pathogen avoidance.

The acquisition and use of social information are integral to social behaviour and parasite/pathogen avoidance. This involves social cognition which encompasses mechanisms for acquiring, processing, retaining and acting on social information. Social cognition entails the acquisition of social information about others (i.e. social recognition) and from others (i.e. social learning). Social cognition involves assessing other individuals and their infection status and the pathogen and parasite threat they pose and deciding about when and how to interact with them. Social cognition provides a framework for examining pathogen and parasite avoidance behaviours and their associated neurobiological mechanisms. Here, we briefly consider the relationships between social cognition and olfactory-mediated pathogen and parasite avoidance behaviours. We briefly discuss aspects of (i) social recognition of actual and potentially infected individuals and the impact of parasite/pathogen threat on mate and social partner choice; (ii) the roles of 'out-groups' (strangers, unfamiliar individuals) and 'in-groups' (familiar individuals) in the expression of parasite/pathogen avoidance behaviours; (iii) individual and social learning, i.e. the utilization of the pathogen recognition and avoidance responses of others; and (iv) the neurobiological mechanisms, in particular the roles of the nonapeptide, oxytocin and steroid hormones (oestrogens) associated with social cognition and parasite/pathogen avoidance.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Evolution of pathogen and parasite avoidance behaviours.

All free-living animals are subject to intense selection pressure from parasites and pathogens resulting in behavioural adaptations that can help potential hosts to avoid falling prey to parasites. This special issue on the evolution of parasite avoidance behaviour was compiled following a Royal Society meeting in 2017. Here we have assembled contributions from a wide range of disciplines including genetics, ecology, parasitology, behavioural science, ecology, psychology and epidemiology on the disease avoidance behaviour of a wide range of species. Taking an interdisciplinary and cross-species perspective allows us to sketch out the strategies, mechanisms and consequences of parasite avoidance and to identify gaps and further questions. Parasite avoidance strategies must include avoiding parasites themselves and cues to their presence in conspecifics, heterospecifics, foods and habitat. Further, parasite avoidance behaviour can be directed at constructing parasite-retardant niches. Mechanisms of parasite avoidance behaviour are generally less well characterized, though nematodes, rodents and human studies are beginning to elucidate the genetic, hormonal and neural architecture that allows animals to recognize and respond to cues of parasite threat. While the consequences of infection are well characterized in humans, we still have much to learn about the epidemiology of parasites of other species, as well as the trade-offs that hosts make in parasite defence versus other beneficial investments like mating and foraging. Finally, in this overview we conclude that it is legitimate to use the word 'disgust' to describe parasite avoidance systems, in the same way that 'fear' is used to describe animal predator avoidance systems. Understanding disgust across species offers an excellent system for investigating the strategies, mechanisms and consequences of behaviour and could be a vital contribution towards the understanding and conservation of our planet's ecosystems.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Consumption, contact and copulation: how pathogens have shaped human psychological adaptations.

Disgust is an emotion intimately linked to pathogen avoidance. Building on prior work, we suggest disgust is an output of programmes that evolved to address three separate adaptive problems: what to eat, what to touch and with whom to have sex. We briefly discuss the architecture of these programmes, specifying their perceptual inputs and the contextual factors that enable them to generate adaptive and flexible behaviour. We propose that our sense of disgust is the result of these programmes and occurs when information-processing circuitries assess low expected values of consumption, low expected values of contact or low expected sexual values. This conception of disgust differs from prior models in that it dissects pathogen-related selection pressures into adaptive problems related to consumption and contact rather than assuming just one pathogen disgust system, and it excludes moral disgust from the domain of disgust proper. Instead, we illustrate how low expected values of consumption and contact as well as low expected sexual values can be used by our moral psychology to provide multiple causal links between disgust and morality.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Neuronal and non-neuronal signals regulate Caernorhabditis elegans avoidance of contaminated food.

One way in which animals minimize the risk of infection is to reduce their contact with contaminated food. Here, we establish a model of pathogen-contaminated food avoidance using the nematode worm Caernorhabditis elegans. We find that avoidance of pathogen-contaminated food protects C. elegans from the deleterious effects of infection and, using genetic approaches, demonstrate that multiple sensory neurons are required for this avoidance behaviour. In addition, our results reveal that the avoidance of contaminated food requires bacterial adherence to non-neuronal cells in the tail of C. elegans that are also required for the cellular immune response. Previous studies in C. elegans have contributed significantly to our understanding of molecular and cellular basis of host–pathogen interactions and our model provides a unique opportunity to gain basic insights into how animals avoid contaminated food.This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.

Why do people vary in disgust?

People vary in the degree to which they experience disgust toward—and, consequently, avoid—cues to pathogens. Prodigious work has measured this variation and observed that it relates to, among other things, personality, psychopathological tendencies, and moral and political sentiments. Less work has sought to generate hypotheses aimed at explaining why this variation exists in the first place, and even less work has evaluated how well data support these hypotheses. In this paper, we present and review the evidence supporting three such proposals. First, researchers have suggested that variability reflects a general tendency to experience anxiety or emotional distress. Second, researchers have suggested that variability arises from parental modelling, with offspring calibrating their pathogen avoidance based on their parents' reactions to pathogen cues. Third, researchers have suggested that individuals calibrate their disgust sensitivity to the parasite stress of the ecology in which they develop. We conclude that none of these hypotheses is supported by existing data, and we propose directions for future research aimed at better understanding this variation.This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.

The structure and function of pathogen disgust.

Researchers have long noted that many of the multiple elicitors of disgust have some relation to infectious disease. There is an emerging consensus that disgust evolved in Animalia to direct the behaviours that reduce risk of infection, so-called 'parasite avoidance theory'. If this is correct, then the disgust motive should be structured in a manner that reflects the ways in which infectious disease can be avoided. In this study, we generated a set of items based on the epidemiology of disease transmission. These were then rated for their capacity to elicit disgust by a large, predominantly North American/UK sample and subjected to factor analysis to identify latent variables. While a number of plausible factor solutions emerged, Velicer's MAP (minimum average partial) test suggested six domains: atypical appearance, lesions, sex, hygiene, food and animals. This structure did not exactly mirror the transmission routes of infections, as we initially predicted, but it may rather reflect distinct kinds of behavioural tasks involved in avoiding disease. This finding makes sense from the perspective of a cognitive system that evolved under selection for a behavioural response to threats from the social and biological environment. We suggest that regularly occurring types of infectious disease problems have produced regularities in the domain structure of pathogen disgust and discuss the implications of these results for understanding the structure, function and measurement of motives such as disgust in humans and other animals.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens.

Mammals live and thrive in environments presenting ongoing threats from parasites in the form of biting flies, ticks and intestinal worms and from pathogens as wound contaminants and agents of infectious disease. Several strategies have evolved that enable animals to deal with parasites and pathogens, including eliminating away from the sleeping–resting areas, use of an array of grooming techniques, use of saliva in licking, and consuming medicinal plant-based compounds. These strategies all are species-specific and reflect the particular environment that the animal inhabits.This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.

Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores.

Mammalian herbivores are typically infected by parasitic nematodes, which are acquired through direct, faecal-oral transmission. These parasites can cause significant production losses in domestic livestock, but much less is known about impacts on wild mammalian hosts. We review three elements of parasitism from the host's perspective: fitness costs of infection, risks of infection during foraging and benefits of nutritious pasture. The majority of wildlife studies have been observational, but experimental manipulation is increasing. Treatment with anthelmintics to manipulate parasite load has revealed varied impacts of parasites on fitness variables across host species, but has not produced consistent evidence for parasite-induced anorexia or impaired body condition. Some experimental studies of infection risk have manipulated faecal contamination and detected faecal avoidance by hosts. Only two field studies have explored the trade-off between infection risk and nutritional benefit generated by avoidance of contaminated patches. Overall, field studies of costs, risks and benefits of the host-parasite relationship are limited and few have examined more than one of these elements. Parasitism has much in common with predation, and future insights into anti-parasite responses by wild hosts could be gained from the conceptual and technical developments in research on anti-predator behaviour.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Ectoparasite defence in humans: relationships to pathogen avoidance and clinical implications.

Currently, disgust is regarded as the main adaptation for defence against pathogens and parasites in humans. Disgust's motivational and behavioural features, including withdrawal, nausea, appetite suppression and the urge to vomit, defend effectively against ingesting or touching sources of pathogens. However, ectoparasites do not attack their hosts via ingestion, but rather actively attach themselves to the body surface. Accordingly, by itself, disgust offers limited defence against ectoparasites. We propose that, like non-human animals, humans have a distinct ectoparasite defence system that includes cutaneous sensory mechanisms, itch-generation mechanisms and grooming behaviours. The existence of adaptations for ectoparasite defence is supported by abundant evidence from non-human animals, as well as more recent evidence concerning human responses to ectoparasite cues. Several clinical disorders may be dysfunctions of the ectoparasite defence system, including some that are pathologies of grooming, such as skin picking and trichotillomania, and others, such as delusory parasitosis and trypophobia, which are pathologies of ectoparasite detection. We conclude that future research should explore both distinctions between, and overlap across, ectoparasite defence systems and pathogen avoidance systems, as doing so will not only illuminate proximate motivational systems, including disgust, but may also reveal important clinical and social consequences.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Both hygienic and non-hygienic honeybee, Apis mellifera, colonies remove dead and diseased larvae from open brood cells.

Hygienic behaviour is a group defence in which dead or diseased individuals are excluded. In the honeybee, Apis mellifera, hygienic behaviour refers to uncapping and removing dead and diseased larvae and pupae from sealed brood cells. We quantified removal of freeze-killed and chalkbrood-infected larvae from open cells in 20 colonies. We also measured removal of freeze-killed brood from sealed cells. Study colonies ranged from non-hygienic to fully hygienic (52-100% removal within 2 days). All larvae killed in open cells were removed. This shows that all colonies, including those with low hygienic behaviour against dead brood in sealed cells, are highly hygienic against dead brood in open cells and suggests that low hygienic behaviour against dead brood in sealed cells is a trait in its own right. This may also contribute to understanding why hygienic behaviour is uncommon in A. mellifera, which is puzzling as it reduces several diseases without detrimental effects. In particular, the result provides indirect support for the hypothesis that there are two adaptive peaks conferring disease resistance: (i) high hygienic behaviour: diseased brood are removed quickly, in some cases before becoming infective; (ii) low hygienic behaviour: diseased brood remain isolated within sealed cells.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Feeding decisions under contamination risk in bonobos.

Threats from parasites and pathogens are ubiquitous, and many use pathways that exploit host trophic interactions for their transmission. As such, host organisms have evolved a behavioural immune system to facilitate contamination-risk assessment and avoidance of potential contaminants in various contexts, including feeding. Detecting pathogen threats can rely on different sensory modalities allowing animals to screen for a wide array of contaminants. Here, we present a series of experiments in which bonobos showed clear avoidance of contaminated food items, and were sensitive to risk along a contamination probability gradient. Across experiments, bonobos appeared to use multisensorial cues to inform their feeding decisions. In addition, bonobos showed reduced tactile, gustatory and tool use activities when in the presence of contaminant versus control odours in a challenging foraging context. Our experiments build on previous work conducted in Japanese macaques and chimpanzees aiming at a better understanding of the ways in which the behavioural immune system operates in primates.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Insect societies fight back: the evolution of defensive traits against social parasites.

Insect societies face many social parasites that exploit their altruistic behaviours or their resources. Due to the fitness costs these social parasites incur, hosts have evolved various behavioural, chemical, architectural and morphological defence traits. Similar to bacteria infecting multicellular hosts, social parasites have to successfully go through several steps to exploit their hosts. Here, we review how social insects try to interrupt this sequence of events. They can avoid parasite contact by choosing to nest in parasite-free locales or evade attacks by adapting their colony structure. Once social parasites attack, hosts attempt to detect them, which can be facilitated by adjustments in colony odour. If social parasites enter the nest, hosts can either aggressively defend their colony or take their young and flee. Nest structures are often shaped to prevent social parasite invasion or to safeguard host resources. Finally, if social parasites successfully establish themselves in host nests, hosts can rebel by killing the parasite brood or by reproducing in the parasites' presence. Hosts of social parasites can therefore develop multiple traits, leading to the evolution of complex defence portfolios of co-dependent traits. Social parasites can respond to these multi-level defences with counter-adaptations, potentially leading to geographical mosaics of coevolution.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Parasite avoidance behaviours in aquatic environments.

Parasites, including macroparasites, protists, fungi, bacteria and viruses, can impose a heavy burden upon host animals. However, hosts are not without defences. One aspect of host defence, behavioural avoidance, has been studied in the terrestrial realm for over 50 years, but was first reported from the aquatic environment approximately 20 years ago. Evidence has mounted on the importance of parasite avoidance behaviours and it is increasingly apparent that there are core similarities in the function and benefit of this defence mechanism between terrestrial and aquatic systems. However, there are also stark differences driven by the unique biotic and abiotic characteristics of terrestrial and aquatic (marine and freshwater) environments. Here, we review avoidance behaviours in a comparative framework and highlight the characteristics of each environment that drive differences in the suite of mechanisms and cues that animals use to avoid parasites. We then explore trade-offs, potential negative effects of avoidance behaviour and the influence of human activities on avoidance behaviours. We conclude that avoidance behaviours are understudied in aquatic environments but can have significant implications for disease ecology and epidemiology, especially considering the accelerating emergence and re-emergence of parasites.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Anti-parasite behaviour of birds

Birds have many kinds of internal and external parasites, including viruses, bacteria and fungi, as well as protozoa, helminths and arthropods. Because parasites have negative effects on host fitness, selection favours the evolution of anti-parasite defences, many of which involve behaviour. We provide a brief review of anti-parasite behaviours in birds, divided into five major categories: (i) body maintenance, (ii) nest maintenance, (iii) avoidance of parasitized prey, (iv) migration and (v) tolerance. We evaluate the adaptive significance of the different behaviours and note cases in which additional research is particularly needed. We briefly consider the interaction of different behaviours, such as sunning and preening, and how behavioural defences may interact with other forms of defence, such as immune responses. We conclude by suggesting some general questions that need to be addressed concerning the nature of anti-parasite behaviour in birds.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Distinct Roles of Sensory Neurons in Mediating Pathogen Avoidance and Neuropeptide-Dependent Immune Regulation

Increasing evidence implies an extensive and universal interaction between the immune system and thenervous system. Previous studies showed that OCTR-1, a neuronal G-protein-coupled receptor (GPCR) analogous to human norepinephrine receptors, functions in sensory neurons to control the gene expression of both microbial killing pathways and the unfolded protein response (UPR) in Caenorhabditis elegans. Here, we found that OCTR-1-expressing neurons, ASH, are involved in controlling innate immune pathways. In contrast, another group of OCTR-1-expressing neurons, ASI, was shown to promote pathogen avoidance behavior. We also identified neuropeptide NLP-20 and AIA interneurons, which are responsible for the integration of conflicting cues and behaviors, as downstream components of the ASH/ASI neural circuit. These findings provide insights into a neuronal network involved inregulating pathogen defense mechanisms in C.elegans and might have broad implications for the strategies utilized by metazoans to balance theenergy-costly immune activation and behavioral response.

Small RNA-mediated Cry toxin silencing allows Bacillus thuringiensis to evade Caenorhabditis elegans avoidance behavioral defenses.

Pathogen avoidance behavior protects animal hosts against microbial pathogens. Pathogens have evolved specific strategies during coevolution in response to such host defenses. However, these strategies for combatting host avoidance behavioral defenses remain poorly understood. Here, we used Caenorhabditis elegans and its bacterial pathogen Bacillus thuringiensis as a model and determined that small RNA (sRNA)-mediated Cry toxin silencing allowed pathogens to evade host avoidance behavioral defenses. The B. thuringiensis strain YBT-1518, which encodes three nematicidal cry genes, is highly toxic to C. elegans. However, the expression of the most potent toxin, Cry5Ba, was silenced in this strain when YBT-1518 was outside the host. Cry5Ba silencing was due to the sRNA BtsR1, which bound to the RBS site of the cry5Ba transcript via direct base pairing and inhibited Cry5Ba expression. Upon ingestion by C. elegans, Cry5Ba was expressed in vivo by strain YBT-1518. Cry5Ba silencing may allow B. thuringiensis to avoid nematode behavioral defenses and then express toxins once ingested to kill the host and gain a survival advantage. Our work describes a novel model of sRNA-mediated regulation to aid pathogens in combating host avoidance behavioral defenses.

Mir-67 regulates P. aeruginosa avoidance behavior in C. elegans

Pathogen avoidance behaviors are found throughout the animal kingdom and are important for animal's survival in nature. As a free-living nematode, C. elegans is exposed to a variety of microorganisms, including toxic or pathogenic bacteria, in soil. C. elegans can develop efficient avoidance responses to pathogenic bacteria to minimize the infection risk. However, the role of microRNAs (miRNAs) in pathogen avoidance in C. elegans remains unclear. In this report, we showed that the miRNA mir-67 was involved in a behavioral avoidance response to P. aeruginosa PA14. Exposure to P. aeruginosa PA14 induced the expression of mir-67 in worms. mir-67(n4899) mutants exhibited a reduced ability to avoid P. aeruginosa PA14. By combining quantitative proteomic analysis with miRNA target prediction algorithms, we identified SAX-7/L1CAM, which is transmembrane cell adhesion receptor molecule, as the target of mir-67. Silencing of sax-7 by RNAi on mir-67 mutants rescued avoidance behavioral. Our data demonstrate that the mir-67-SAX-7 pathway modulate the behavioral avoidance response to pathogens, thus providing a new perspective in the role of miRNAs in host–microbe interactions.

Enhanced behavioral immune defenses in a C. elegans C-type lectin-like domain gene mutant

C-type lectin-like domain (CTLD) proteins occupy crucial functions in the immune system of vertebrates, but their role in invertebrate immunity is much less understood. The nematode Caenorhabditis elegans possesses a highly diverse CTLD protein encoding (clec) gene repertoire. A role of C. elegans clec genes in pathogen defense is always assumed, yet experimental evidence for clec immune function is rare. To systematically test the potential function of clec genes in the C. elegans defense against pathogens, we screened 39 clec mutants for survival on the Gram-positive pathogen Bacillus thuringiensis (BT18247) and 37 clec mutants on the Gram-negative pathogen Pseudomonas aeruginosa (PA14). We found that clec mutants can exhibit either decreased or, unexpectedly, increased resistance to infection. Since we observed high escape behavior for some of the clec mutants on BT18247 during the initial screen, we then asked if increased pathogen avoidance behavior underlies the increased resistance of some clec mutants. We thus tested lawn leaving behavior of the resistant clec-29(ok3181), clec-34(ok2120), clec-151(ok2264), and C54G4.4(ok2110) mutant on BT18247. We found that C54G4.4(ok2110) mutant animals exhibit a particularly strong lawn leaving behavior, in addition to prolonged feeding cessation when exposed to BT18247. Together, our results indicate that clec genes mediate both resistance and susceptibility to infection. Further, behavioral analyses of the C54G4.4(ok2110) mutant implicate C54G4.4 in the regulation of pathogen avoidance behavior towards BT18247. We conclude that C. elegans clec genes may act both as positive and negative regulators of physiological as well as behavioral immune defense responses.

Investigating the Heritability of a Learned Pathogen Avoidance Behavior in Caenorhabditis elegans

In defiance of the laws of traditional Mendelian inheritance, multigeneration epigenetic inheritance of changes in gene expression in response to the experience of parental generations has been widely observed in both plants and animals. The roundworm Caenorhabditis elegans (C. elegans) has emerged as a premier model system for the study of transgenerational epigenetic inheritance, and heritable, epigenetic effects on gene expression have been seen in response to a variety of environmental conditions. It has been hypothesized that worms might be particularly adept at epigenetic inheritance of acquired traits due to their abundant use of small RNA silencing pathways, which have been shown to mediate gene silencing phenomena that can be epigenetically inherited for tens of generations. Here we investigate whether a well‐studied learned behavior in the worm can be inherited, and whether small RNA‐mediated gene silencing plays a role in mediating learningC. elegans that have been infected by the pathogenic soil bacterium Pseudomonas aeruginosa (P. aeruginosa, strain PA14) learn to avoid this food source through a mechanism involving alterations in serotonin expression in specific chemosensory neurons. In this associative learning regimen, worms are trained on plates that contain both pathogenic PA14 and nonpathogenic Escherichia coli (E. coli). At adulthood, worms are assayed for their preference between PA14 and E. coli using a standard behavioral choice assay. Similar to what has been seen previously, we find that only 29% of trained worms choose PA14 over E. coli, whereas naïve worms (which have never been exposed to PA14) choose PA14 37% of the time (p<.01, one‐tailed t test). To determine whether this learned avoidance behavior can be inherited by subsequent generations, the F1 progeny of trained worms were raised on plates that contained only E. coli and tested in the choice assay at adulthood. 41% of these worms were found in the PA14 spot, which was not significantly different from naïve worms (p=0.21), suggesting that learned pathogen avoidance cannot be epigenetically inherited. Some previously reported cases of siRNA‐mediated epigenetic inheritance in worms required that animals be exposed to the initial silencing trigger for several generations before epigenetic inheritance was established. To ask whether multi‐generation infection to pathogen could result in inheritance of avoidance behavior, synchronized populations of worms were continuously grown in the presence of pathogen for 3, 5, and 7 generations. When we performed learning assays on F1 progeny of the third, fifth, and seventh generation trained worms, we again saw a lack of inheritance of pathogen avoidance. To test the hypothesis that siRNAs play a role in the pathogen avoidance behavior, we are performing learning assays on strains of C. elegans containing mutations that disrupt siRNA pathways. In addition, we are using immunofluorescence for serotonin and mRNA‐seq for genome‐wide analysis to ask whether sub‐phenotypic changes in gene expression can be inherited even in the absence of inheritance of the avoidance behavior. Although other studies have examined epigenetic inheritance of learned behaviors or changes in gene expression, few studies have examined both. Taken together, our experiments will address this important gap between gene expression and phenotype.