Evolution and Ecology of Parasite Avoidance.

Parasite avoidance is a host defense that reduces the contact rate with parasites. We investigate avoidance as a primary driver of variation among individuals in the risk of parasitism and the evolution of host-parasite interactions. To bridge mechanistic and taxonomic divides, we define and categorize avoidance by its function and position in the sequence of host defenses. We also examine the role of avoidance in limiting epidemics and evaluate evidence for the processes that drive its evolution. Throughout, we highlight important directions to advance our conceptual and theoretical understanding of the role of avoidance in host-parasite interactions. We emphasize the need to test assumptions and quantify the effect of avoidance independent of other defenses. Importantly, many open questions may be most tractable in host systems that have not been the focus of traditional behavioral avoidance research, such as plants and invertebrates.

Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding.

BACKGROUND: The ability of animals and their microbiomes to adapt to starvation and then restore homeostasis after refeeding is fundamental to their continued survival and symbiosis. The intestine is the primary site of nutrient absorption and microbiome interaction, however our understanding of intestinal adaptations to starvation and refeeding remains limited. Here we used RNA sequencing and 16S rRNA gene sequencing to uncover changes in the intestinal transcriptome and microbiome of zebrafish subjected to long-term starvation and refeeding compared to continuously fed controls. RESULTS: Starvation over 21 days led to increased diversity and altered composition in the intestinal microbiome compared to fed controls, including relative increases in Vibrio and reductions in Plesiomonas bacteria. Starvation also led to significant alterations in host gene expression in the intestine, with distinct pathways affected at early and late stages of starvation. This included increases in the expression of ribosome biogenesis genes early in starvation, followed by decreased expression of genes involved in antiviral immunity and lipid transport at later stages. These effects of starvation on the host transcriptome and microbiome were almost completely restored within 3 days after refeeding. Comparison with published datasets identified host genes responsive to starvation as well as high-fat feeding or microbiome colonization, and predicted host transcription factors that may be involved in starvation response. CONCLUSIONS: Long-term starvation induces progressive changes in microbiome composition and host gene expression in the zebrafish intestine, and these changes are rapidly reversed after refeeding. Our identification of bacterial taxa, host genes and host pathways involved in this response provides a framework for future investigation of the physiological and ecological mechanisms underlying intestinal adaptations to food restriction.

Evolution of behavioural resistance in host-pathogen systems.

Behavioural resistance to parasites is widespread in animals, yet little is known about the evolutionary dynamics that have shaped these strategies. We show that theory developed for the evolution of physiological parasite resistance can only be applied to behavioural resistance under limited circumstances. We find that accounting explicitly for the behavioural processes, including the detectability of infected individuals, leads to novel dynamics that are strongly dependent on the nature of the costs and benefits of social interactions. As with physiological resistance, evolutionary dynamics of behavioural resistance can also lead to mixed strategies that balance these costs and benefits.

Social Influences on Food Avoidance in Lemur catta.

Previous primate research has demonstrated social learning related to accepting novel foods, but little evidence suggests social learning of food avoidance. Ring-tailed lemurs (Lemur catta)have been observed to shake their heads rapidly in response to sour and bitter stimuli. This study investigated whether this head-shaking behavior may have a social function. The experiment presented a performing lemur with two items of the same type of fruit, one of which had been manipulated to take on a sour flavor, and the other which was not manipulated and served as a control. The performer could taste each of the stimuli while an observing lemur had the opportunity to watch the performer's behavior from an adjacent enclosure. The observer was then presented with two stimuli with the same qualities. This study evaluated whether a preceding head-shaking reaction by the performer improved the success rate of the observer avoiding bitter stimuli to greater than chance. Our results reveal that following a head shake by the performer in response to the sour stimuli, observer avoidance of sour stimuli was statistically greater than chance, indicating that there may be social influences on food avoidance in this species. Further research should focus on confirming this effect and characterizing the full set of socially influential food reaction behaviors.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Genetic variation in parasite avoidance, yet no evidence for constitutive fitness costs.

Behavioral avoidance of parasites is a widespread strategy among animal hosts and in human public health. Avoidance has repercussions for both individual and population-level infection risk. Although most cases of parasite avoidance are viewed as adaptive, there is little evidence that the basic assumptions of evolution by natural selection are met. This study addresses this gap by testing whether there is a heritable variation in parasite avoidance behavior. We quantified behavioral avoidance of the bacterial parasite Serratia marcescens for 12 strains of the nematode host Caenorhabditis elegans. We found that these strains varied in their magnitude of avoidance, and we estimated the broad-sense heritability of this behavior to be in the range of 11%-26%. We then asked whether avoidance carries a constitutive fitness cost. We did not find evidence of one. Rather, strains with higher avoidance had higher fitness, measured as population growth rate. Together, these results direct future theoretical and empirical work to identify the forces maintaining genetic variation in parasite avoidance.

Host density shapes the relative contribution of vector-based and aerial transmission of a pathogenic fungus.

Pathogen transmission mode is a key determinant of epidemiological outcomes. Theory shows that host density can influence the spread of pathogens differentially depending on their mode of transmission. Host density could therefore play an important role in determining the pathogen transmission mode. We tested theoretical expectations using floral arrays of the alpine carnation Dianthus pavonius in field experiments of spore dispersal of the anther-smut fungus, Microbotryum, by vector (pollinator)-based floral transmission and passive aerial transmission at a range of host densities. Pollinators deposited fewer spores per plant at high host density than at lower density (ranging from a 0.2-2 m spacing between plants), and vector-based spore deposition at higher densities declined more steeply with distance from diseased plant sources. In contrast, while aerial spore deposition declined with distance from the diseased source, the steepness of this decline was independent of host density. Our study indicates that the amount and distance of vector-based transmission are likely to be a nonmonotonic function of host density as a result of vector behavior, which is not readily encapsulated by fixed dispersal functions. We conclude that the spatial spread of pathogens by vectors is likely to be greater at lower and intermediate densities, whereas the spatial spread of aerially transmitted pathogens would be greater at high densities. These contrasting patterns could lead to differential importance of each transmission mode in terms of its contribution to subsequent infections across host densities.

Integrating concepts of physiological and behavioral resistance to parasites.

Conceptual parallels between physiological and behavioral forms of resistance to parasites have led to the development of terminology like "the behavioral immune system" to refer to behaviors that combat parasites. I extend this metaphor by applying findings from research on physiological resistance to generate predictions for the ecology and evolution of behavioral resistance (here, synonymous with avoidance). In certain cases, behavioral resistance may follow similar evolutionary dynamics to physiological resistance. However, more research on the nature of the costs of behavioral resistance is needed, including how parasite transmission mode may be a key determinant of these costs. In addition, "acquiring" behavioral resistance may require specific mechanisms separate from classical forms of conditioning, due to constraints on timing of host learning processes and parasite incubation periods. Given existing literature, behavioral resistance to infectious disease seems more likely to be innate than acquired within the lifetime of an individual, raising new questions about how individual experience could shape anti-parasite behaviors. This review provides a framework for using existing literature on physiological resistance to generate predictions for behavioral resistance, and highlights several important directions for future research based on this comparison.

Epidemiological transitions in human evolution and the richness of viruses, helminths, and protozoa.

BACKGROUND AND OBJECTIVES: In absolute terms, humans are extremely highly parasitized compared to other primates. This may reflect that humans are outliers in traits correlated with parasite richness: population density, geographic range area, and study effort. The high degree of parasitism could also reflect amplified disease risk associated with agriculture and urbanization. Alternatively, controlling for other variables, cultural and psychological adaptations could have reduced parasitism in humans over evolutionary time. METHODOLOGY: We predicted the number of parasites that would infect a nonhuman primate with human phenotypic characteristics and phylogenetic position, and then compared observed parasitism of humans in eight geopolitical countries to the predicted distributions. The analyses incorporated study effort, phylogeny, and drivers of parasitism in 33 primate species. RESULTS: Analyses of individual countries were not supportive of either hypothesis. When analyzed collectively, however, human populations showed consistently lower than expected richness of protozoa and helminths, but higher richness of viruses. Thus, human evolutionary innovations and new parasite exposures may have impacted groups of parasites in different ways, with support for both hypotheses in the overall analysis. CONCLUSIONS AND IMPLICATIONS: The high level of parasitism observed in humans only applies to viruses, and was not extreme in any of our tests of individual countries. In contrast, we find consistent reductions in protozoa and helminths across countries, suggesting reduced parasitism by these groups during human evolution. We propose that hygienic and technological advances might have extinguished fecal-orally or indirectly transmitted parasites like helminths, whereas higher human densities and host-shifting potential of viruses have supported increased virus richness. LAY SUMMARY: Vastly more parasite species infect humans than any other primate host. Controlling for factors that influence parasite richness, such as the intensity of study effort and body mass, we find that humans may have more viruses, but fewer helminths and protozoa, than expected based on evolutionary analyses of parasitism in other primates.