Associating with kin selects for disease resistance and against tolerance.

Behavioural and physiological resistance are key to slowing epidemic spread. We explore the evolutionary and epidemic consequences of their different costs for the evolution of tolerance that trades off with resistance. Behavioural resistance affects social cohesion, with associated group-level costs, while the cost of physiological resistance accrues only to the individual. Further, resistance, and the associated reduction in transmission, benefit susceptible hosts directly, whereas infected hosts only benefit indirectly, by reducing transmission to kin. We therefore model the coevolution of transmission-reducing resistance expressed in susceptible hosts with resistance expressed in infected hosts, as a function of kin association, and analyse the effect on population-level outcomes. Using parameter values for guppies, Poecilia reticulata, and their gyrodactylid parasites, we find that: (1) either susceptible or infected hosts should invest heavily in resistance, but not both; (2) kin association drives investment in physiological resistance more strongly than in behavioural resistance; and (3) even weak levels of kin association can favour altruistic infected hosts that invest heavily in resistance (versus selfish tolerance), eliminating parasites. Overall, our finding that weak kin association affects the coevolution of infected and susceptible investment in both behavioural and physiological resistance suggests that kin selection may affect disease dynamics across systems.

Ornaments indicate parasite load only if they are dynamic or parasites are contagious.

Choosing to mate with an infected partner has several potential fitness costs, including disease transmission and infection-induced reductions in fecundity and parental care. By instead choosing a mate with no, or few, parasites, animals avoid these costs and may also obtain resistance genes for offspring. Within a population, then, the quality of sexually selected ornaments on which mate choice is based should correlate negatively with the number of parasites with which a host is infected ("parasite load"). However, the hundreds of tests of this prediction yield positive, negative, or no correlation between parasite load and ornament quality. Here, we use phylogenetically controlled meta-analysis of 424 correlations from 142 studies on a wide range of host and parasite taxa to evaluate explanations for this ambiguity. We found that ornament quality is weakly negatively correlated with parasite load overall, but the relationship is more strongly negative among ornaments that can dynamically change in quality, such as behavioral displays and skin pigmentation, and thus can accurately reflect current parasite load. The relationship was also more strongly negative among parasites that can transmit during sex. Thus, the direct benefit of avoiding parasite transmission may be a key driver of parasite-mediated sexual selection. No other moderators, including methodological details and whether males exhibit parental care, explained the substantial heterogeneity in our data set. We hope to stimulate research that more inclusively considers the many and varied ways in which parasites, sexual selection, and epidemiology intersect.

Skin bacterial microbiome diversity predicts lower activity levels in female, but not male, guppies, Poecilia reticulata.

While the link between the gut microbiome and host behaviour is well established, how the microbiomes of other organs correlate with behaviour remains unclear. Additionally, behaviour-microbiome correlations are likely sex-specific because of sex differences in behaviour and physiology, but this is rarely tested. Here, we tested whether the skin microbiome of the Trinidadian guppy, Poecilia reticulata, predicts fish activity level and shoaling tendency in a sex-specific manner. High-throughput sequencing revealed that the bacterial community richness on the skin (Faith's phylogenetic diversity) was correlated with both behaviours differently between males and females. Females with richer skin-associated bacterial communities spent less time actively swimming. Activity level was significantly correlated with community membership (unweighted UniFrac), with the relative abundances of 16 bacterial taxa significantly negatively correlated with activity level. We found no association between skin microbiome and behaviours among male fish. This sex-specific relationship between the skin microbiome and host behaviour may indicate sex-specific physiological interactions with the skin microbiome. More broadly, sex specificity in host-microbiome interactions could give insight into the forces shaping the microbiome and its role in the evolutionary ecology of the host.

Shoaling guppies evade predation but have deadlier parasites.

Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite. Predators may shift this cost-benefit balance by consuming infected hosts or changing host behaviour, but the strength of these effects remains unclear. Here we use field and lab data on Trinidadian guppies and their Gyrodactylus spp. parasites to show how differential predation pressure influences parasite virulence and transmission. We use an experimentally demonstrated virulence-transmission trade-off to parametrize a mathematical model in which host shoaling (as a means of anti-predator defence), increases contact rates and selects for higher virulence. Then we validate model predictions by collecting parasites from wild, Trinidadian populations; parasites from high-predation populations were more virulent in common gardens than those from low-predation populations. Broadly, our results indicate that reduced social contact selects against parasite virulence.

Transmission dynamics of ectoparasitic gyrodactylids (Platyhelminthes, Monogenea): An integrative review.

Parasite transmission is the ability of pathogens to move between hosts. As a key component of the interaction between hosts and parasites, it has crucial implications for the fitness of both. Here, we review the transmission dynamics of Gyrodactylus species, which are monogenean ectoparasites of teleost fishes and a prominent model for studies of parasite transmission. Particularly, we focus on the most studied host­parasite system within this genus: guppies, Poecilia reticulata, and G. turnbulli/G. bullatarudis. Through an integrative literature examination, we identify the main variables affecting Gyrodactylus spread between hosts, and the potential factors that enhance their transmission. Previous research indicates that Gyrodactylids spread when their current conditions are unsuitable. Transmission depends on abiotic factors like temperature, and biotic variables such as gyrodactylid biology, host heterogeneity, and their interaction. Variation in the degree of social contact between hosts and sexes might also result in distinct dynamics. Our review highlights a lack of mathematical models that could help predict the dynamics of gyrodactylids, and there is also a bias to study only a few species. Future research may usefully focus on how gyrodactylid reproductive traits and host heterogeneity promote transmission and should incorporate the feedbacks between host behaviour and parasite transmission.

Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes.

An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host-parasite coevolution.

The Size, Symmetry, and Color Saturation of a Male Guppy's Ornaments Forecast His Resistance to Parasites.

AbstractSexually selected ornaments range from highly dynamic traits to those that are fixed during development and relatively static throughout sexual maturity. Ornaments along this continuum differ in the information they provide about the qualities of potential mates, such as their parasite resistance. Dynamic ornaments enable real-time assessment of the bearer's condition: they can reflect an individual's current infection status, or they can reflect resistance to recent infections. Static ornaments, however, are not affected by recent infection but may instead indicate an individual's genetically determined resistance, even in the absence of infection. Given the typically aggregated distribution of parasites among hosts, infection is unlikely to affect the ornaments of the vast majority of individuals in a population: static ornaments may therefore be the more reliable indicators of parasite resistance. To test this hypothesis, we quantified the ornaments of male guppies (Poecilia reticulata) before experimentally infecting them with Gyrodactylus turnbulli. Males with more left-right symmetrical black coloration and those with larger areas of orange coloration, both static ornaments, were more resistant. However, males with more saturated orange coloration, a dynamic ornament, were less resistant. Female guppies often prefer symmetrical males with larger orange ornaments, suggesting that parasite-mediated natural and sexual selection act in concert on these traits.

Emerging infectious disease and the challenges of social distancing in human and non-human animals.

The 'social distancing' that occurred in response to the COVID-19 pandemic in humans provides a powerful illustration of the intimate relationship between infectious disease and social behaviour in animals. Indeed, directly transmitted pathogens have long been considered a major cost of group living in humans and other social animals, as well as a driver of the evolution of group size and social behaviour. As the risk and frequency of emerging infectious diseases rise, the ability of social taxa to respond appropriately to changing infectious disease pressures could mean the difference between persistence and extinction. Here, we examine changes in the social behaviour of humans and wildlife in response to infectious diseases and compare these responses to theoretical expectations. We consider constraints on altering social behaviour in the face of emerging diseases, including the lack of behavioural plasticity, environmental limitations and conflicting pressures from the many benefits of group living. We also explore the ways that social animals can minimize the costs of disease-induced changes to sociality and the unique advantages that humans may have in maintaining the benefits of sociality despite social distancing.

Two's company, three's a crowd: Exploring how host-parasite-microbiota interactions may influence disease susceptibility and conservation of wildlife.

A large body of research has demonstrated that host-associated microbiota-the archaeal, bacterial, fungal and viral communities residing on and inside organisms-are critical to host health (Cho & Blaser, 2012). Although the vast majority of these studies focus on humans or model organisms in laboratory settings (Pascoe, Hauffe, Marchesi, & Perkins, 2017), they nevertheless provide important conceptual evidence that the disruption of host-associated microbial communities (termed "dysbiosis") among wild animals may reduce host fitness and survival under natural environmental conditions. Among the myriad of environmental factors capable of inducing dysbiosis among wild animals (Trevelline, Fontaine, Hartup, & Kohl, 2019), parasitic infections represent a potentially potent, yet poorly understood, factor influencing microbial community dynamics and animal health. The study by DeCandia et al. in this issue of Molecular Ecology is a rare example of a host-parasite-microbiota interaction that impacts the health, survival and conservation of a threatened wild animal in its natural habitat. Using culture-independent techniques, DeCandia et al. found that the presence of an ectoparasitic mite (Otodectes cynotis) in the ear canal of the Santa Catalina Island fox (Urocyon littoralis catalinae) was associated with significantly reduced ear canal microbial diversity, with the opportunistic pathogen Staphylococcus pseudintermedius dominating the community. These findings suggest that parasite-induced inflammation may contribute to the formation of ceruminous gland tumours in this subspecies of Channel Island fox. As a rare example of a host-parasite-microbiota interaction that may mediate a lethal disease in a population of threatened animals, their study provides an excellent example of how aspects of disease ecology can be integrated into studies of host-associated microbiota to advance conservation science and practice.

Parasite-induced plasticity in host social behaviour depends on sex and susceptibility.

Understanding the effects of parasites on host behaviour, of host behaviour on parasite infection, and the reciprocal interactions between these processes is vital to improving our understanding of animal behaviour and disease dynamics. However, behaviour and parasite infection are both highly variable within and between individual hosts, and how this variation affects behaviour-parasite feedbacks is poorly understood. For example, it is unclear how an individual's behaviour before infection might change once it becomes infected, or as the infection progresses, and how these changes depend on the host's parasite susceptibility. Here, using the guppy, Poecilia reticulata, and a directly transmitted ectoparasite, Gyrodactylus turnbulli, I show that parasite-induced behavioural plasticity depends on host sex and susceptibility. Among females, time spent shoaling (sociality), a behaviour that increases parasite transmission, did not depend on infection status (infected/not) or susceptibility. By contrast, male sociality in the absence of infection was negatively correlated with susceptibility, suggesting that the most susceptible males use behaviour to avoid infection. However, in late infection, when parasite transmission is most likely, male sociality and susceptibility became positively correlated, suggesting that susceptible males modify their behaviour upon infection potentially to increase transmission and mating opportunities. I discuss the implications of these patterns for disease dynamics.

Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies.

Associating with conspecifics afflicted with infectious diseases increases the risk of becoming infected, but engaging in avoidance behaviour incurs the cost of lost social benefits. Across systems, infected individuals vary in the transmission risk they pose, so natural selection should favour risk-sensitive avoidance behaviour that optimally balances the costs and benefits of sociality. Here, we use the guppy Poecilia reticulata-Gyrodactylus turnbulli host-parasite system to test the prediction that individuals avoid infected conspecifics in proportion to the transmission risk they pose. In dichotomous choice tests, uninfected fish avoided both the chemical and visual cues, presented separately, of infected conspecifics only in the later stages of infection. A transmission experiment indicated that this avoidance behaviour accurately tracked transmission risk (quantified as both the speed at which transmission occurs and the number of parasites transmitting) through the course of infection. Together, these findings reveal that uninfected hosts can use redundant cues across sensory systems to inform dynamic risk-sensitive avoidance behaviour. This correlation between the transmission risk posed by infected individuals and the avoidance response they elicit has implications for the evolutionary ecology of infectious disease, and its explicit inclusion may improve the ability of epidemic models to predict disease spread.

Response to Durif et al.

Our recent study [1] in Current Biology used a magnetic displacement experiment and simulations in an ocean circulation model to provide evidence that young European eels possess a 'magnetic map' that can aid their marine migration. Our results support two major conclusions: first, young eels distinguish among magnetic fields corresponding to locations across their marine range; second, for the fields that elicited significantly non-random orientation, swimming in the experimentally observed direction from the corresponding locations would increase entrainment in the Gulf Stream system. In their critique, Durif et al.[2] seem to conflate the separate and potentially independent 'map step' and 'compass step' of animal navigation. In the map step, an animal derives positional information to select a direction, whereas in the compass step the animal maintains that heading [3,4]. Our experiment was designed such that differences in eel orientation among treatments would indicate an ability to use the magnetic field as a map; the compass cue(s) used by eels was not investigated.

A Magnetic Map Leads Juvenile European Eels to the Gulf Stream.

Migration allows animals to track the environmental conditions that maximize growth, survival, and reproduction [1-3]. Improved understanding of the mechanisms underlying migrations allows for improved management of species and ecosystems [1-4]. For centuries, the catadromous European eel (Anguilla anguilla) has provided one of Europe's most important fisheries and has sparked considerable scientific inquiry, most recently owing to the dramatic collapse of juvenile recruitment [5]. Larval eels are transported by ocean currents associated with the Gulf Stream System from Sargasso Sea breeding grounds to coastal and freshwater habitats from North Africa to Scandinavia [6, 7]. After a decade or more, maturing adults migrate back to the Sargasso Sea, spawn, and die [8]. However, the migratory mechanisms that bring juvenile eels to Europe and return adults to the Sargasso Sea remain equivocal [9, 10]. Here, we used a "magnetic displacement" experiment [11, 12] to show that the orientation of juvenile eels varies in response to subtle differences in magnetic field intensity and inclination angle along their marine migration route. Simulations using an ocean circulation model revealed that even weakly swimming in the experimentally observed directions at the locations corresponding to the magnetic displacements would increase entrainment of juvenile eels into the Gulf Stream System. These findings provide new insight into the migration ecology and recruitment dynamics of eels and suggest that an adaptive magnetic map, tuned to large-scale features of ocean circulation, facilitates the vast oceanic migrations of the Anguilla genus [7, 13, 14].

Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts.

Infectious disease dynamics depend on the speed, number and fitness of parasites transmitting from infected hosts ('donors') to parasite-naive 'recipients'. Donor heterogeneity likely affects these three parameters, and may arise from variation between donors in traits including: (i) infection load, (ii) resistance, (iii) stage of infection, and (iv) previous experience of transmission. We used the Trinidadian guppy, Poecilia reticulata, and a directly transmitted monogenean ectoparasite, Gyrodactylus turnbulli, to experimentally explore how these sources of donor heterogeneity affect the three transmission parameters. We exposed parasite-naive recipients to donors (infected with a single parasite strain) differing in their infection traits, and found that donor infection traits had diverse and sometimes interactive effects on transmission. First, although transmission speed increased with donor infection load, the relationship was nonlinear. Second, while the number of parasites transmitted generally increased with donor infection load, more resistant donors transmitted more parasites, as did those with previous transmission experience. Finally, parasites transmitting from experienced donors exhibited lower population growth rates on recipients than those from inexperienced donors. Stage of infection had little effect on transmission parameters. These results suggest that a more holistic consideration of within-host processes will improve our understanding of between-host transmission and hence disease dynamics.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.

Keeping eyes peeled: guppies exposed to chemical alarm cue are more responsive to ambiguous visual cues.

ABSTRACT: Information received from the visual and chemical senses is qualitatively different. For prey species in aquatic environments, visual cues are spatially and temporally reliable but risky as the prey and predator must often be in close proximity. Chemical cues, by contrast, can be distorted by currents or linger and thus provide less reliable spatial and temporal information, but can be detected from a safe distance. Chemical cues are therefore often the first detected and may provide a context in which prey respond to subsequent ambiguous cues ("context hypothesis"). Depending on this context, early chemical cues may also alert prey to attend to imminent cues in other sensory modalities ("alerting hypothesis"). In the context of predation risk, for example, it is intuitive that individuals become more responsive to subsequent ambiguous cues across sensory modalities. Consistent with the context hypothesis, guppies, Poecilia reticulata, exposed to conspecific alarm cue reduced activity, a classic fright response among fish, in response to a water disturbance more than those exposed to cues of unharmed conspecifics or a water control. Despite this reduction in activity, guppies exposed to alarm cue were more attentive to visual cues than those exposed to the other chemical cues, as predicted by the alerting hypothesis. These responses contrasted with those of guppies exposed to chemical cues of undisturbed, unharmed conspecifics, which were relatively unaffected by the disturbance. This is the first study indicating that unambiguous cues detected by one sensory modality affect animal responses to subsequent ambiguous multimodal cues. SIGNIFICANCE STATEMENT: In moving water, chemical cues can be detected over longer distances than visual cues; they may therefore be detected first and alert animals to imminent visual cues. This effect is likely to be particularly important if these chemical cues are indicative of predation. I investigated how different chemical cues affect (1) guppy response to an ambiguous water disturbance and (2) their responsiveness to subsequent ambiguous visual cues. Guppies based their responses to ambiguous cues on the context implied by chemical cues: those exposed to chemical cues indicative of predation reduced activity, a classic fright response, but increased responsiveness to visual cues, relative to those exposed to control chemical cues. This is the first study to show that unambiguous cues detected by one sense affect animal responses to ambiguous cues detected by other senses.

Imprinting can cause a maladaptive preference for infectious conspecifics.

Recognizing and associating with specific individuals, such as conspecifics or kin, brings many benefits. One mechanism underlying such recognition is imprinting: the long-term memory of cues encountered during development. Typically, juveniles imprint on cues of nearby individuals and may later associate with phenotypes matching their 'recognition template'. However, phenotype matching could lead to maladaptive social decisions if, for instance, individuals imprint on the cues of conspecifics infected with directly transmitted diseases. To investigate the role of imprinting in the sensory ecology of disease transmission, we exposed juvenile guppies,Poecilia reticulata, to the cues of healthy conspecifics, or to those experiencing disease caused by the directly transmitted parasite Gyrodactylus turnbulli In a dichotomous choice test, adult 'disease-imprinted' guppies preferred to associate with the chemical cues of G. turnbulli-infected conspecifics, whereas 'healthy-imprinted' guppies preferred to associate with cues of uninfected conspecifics. These responses were only observed when stimulus fish were in late infection, suggesting imprinted fish responded to cues of disease, but not of infection alone. We discuss how maladaptive imprinting may promote disease transmission in natural populations of a social host.

A further cost for the sicker sex? Evidence for male-biased parasite-induced vulnerability to predation.

Males are typically the sicker sex. Data from multiple taxa indicate that they are more likely to be infected with parasites, and are less "tolerant," or less able to mitigate the fitness costs of a given infection, than females. One cost of infection for many animals is an increased probability of being captured by a predator. A clear, hitherto untested, prediction is therefore that this parasite-induced vulnerability to predation is more pronounced among males than females. We tested this prediction in the sexually size dimorphic guppy, Poecilia reticulata, in which females are typically larger than males. We either sham or experimentally infected guppies with Gyrodactylus turnbulli, elicited their escape response using an established protocol and measured the distance they covered during 60 ms. To discriminate between the effects of body size and those of other inherent sex differences, we size-matched fish across treatment groups. Infection with G. turnbulli reduced the distance covered during the escape response of small adults by 20.1%, whereas that of large fish was unaffected. This result implies that parasite-induced vulnerability to predation is male-biased in the wild: although there was no difference in escape response between our experimentally size-matched groups of males and females, males are significantly smaller across natural guppy populations. These results are consistent with Bateman's principle for immunity: Natural selection for larger body sizes and longevity in females seems to have resulted in the evolution of increased infection tolerance. We discuss the potential implications of sex- and size-biased parasite-induced vulnerability to predation for the evolutionary ecology of this host-parasite interaction in natural communities.

Parasites of Trinidadian guppies: evidence for sex- and age-specific trait-mediated indirect effects of predators.

Predation pressure can alter the morphology, physiology, life history, and behavior of prey; each of these in turn can change how surviving prey interact with parasites. These trait-mediated indirect effects may change in direction or intensity during growth or, in sexually dimorphic species, between the sexes. The Trinidadian guppy, Poecilia reticulata presents a unique opportunity to examine these interactions; its behavioral ecology has been intensively studied in wild populations with well-characterized predator faunas. Predation pressure is known to have driven the evolution of many guppy traits; for example, in high-predation sites, females (but not males) tend to shoal, and this anti-predator behavior facilitates parasite transmission. To test for evidence of predator-driven differences in infection in natural populations, we collected 4715 guppies from 62 sites across Trinidad between 2003 and 2009 and screened them for ectosymbionts, including Gyrodactylus. A novel model-averaging analysis revealed that females were more likely to be infected with Gyrodactylus parasites than males, but only in populations with both high predation pressure and high infection prevalence. We propose that the difference in shoaling tendency between the sexes could explain the observed difference in infection prevalence between males and females in high-predation sites. The infection rate of juveniles did not vary with predation regime, probably because juveniles face constant predation pressure from conspecific adults and therefore tend to shoal in both high- and low-predation sites. This represents the first evidence for age- and sex-specific trait-mediated indirect effects of predators on the probability of infection in their prey.