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

Jessica F. Stephenson

doi:10.1098/rsbl.2019.0557

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

Biology Letters ◽

10.1098/rsbl.2019.0557 ◽

2019 ◽

Vol 15 (11) ◽

pp. 20190557 ◽

Cited By ~ 5

Author(s):

Jessica F. Stephenson

Keyword(s):

Poecilia Reticulata ◽

Parasite Infection ◽

Behavioural Plasticity ◽

Parasite Transmission ◽

Disease Dynamics ◽

Late Infection ◽

Reciprocal Interactions ◽

Host Sex ◽

Mating Opportunities ◽

Host Behaviour

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.

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

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0093 ◽

2017 ◽

Vol 372 (1719) ◽

pp. 20160093 ◽

Cited By ~ 9

Author(s):

Jessica F. Stephenson ◽

Kyle A. Young ◽

Jordan Fox ◽

Jukka Jokela ◽

Joanne Cable ◽

...

Keyword(s):

Poecilia Reticulata ◽

Interactive Effects ◽

Parasite Transmission ◽

Disease Dynamics ◽

Population Growth Rates ◽

Transmission Parameters ◽

The Relationship ◽

Infectious Disease Dynamics ◽

Lower Population ◽

Transmission Speed

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’.

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Host behaviour, age and sex correlate with ectoparasite prevalence and intensity in a colonial mammal, the little brown bat

Behaviour ◽

10.1163/1568539x-00003233 ◽

2014 ◽

Vol 152 (1) ◽

pp. 83-105 ◽

Cited By ~ 17

Author(s):

Quinn M.R. Webber ◽

Liam P. McGuire ◽

Steven B. Smith ◽

Craig K.R. Willis

Keyword(s):

Pathogen Transmission ◽

Myotis Lucifugus ◽

Physical Contact ◽

Wildlife Diseases ◽

Colonial Species ◽

Host Seeking ◽

Host Sex ◽

Little Brown Bat ◽

Host Behaviour ◽

Age And Sex

The influence of behaviour on host-parasite dynamics has theoretical support but few empirical studies have examined this influence for wild-captured hosts, especially in colonial species, which are thought to face generally high risk of exposure. Behavioural tendencies of hosts in novel environments could mediate host exposure. We tested the hypothesis that behavioural tendencies of hosts, and host sex and age, correlate with prevalence and intensity of ectoparasites in a gregarious mammal, the little brown bat (Myotis lucifugus). We also tested whether relationships between host behaviour and parasite prevalence and intensity would vary between taxa of ectoparasites which differ in host-seeking behaviour. We predicted that individual hosts displaying active and explorative behaviours would have higher prevalence and intensity of parasites that depend on physical contact among hosts for transmission (mites) but that host behaviour would not influence prevalence and intensity of mobile ectoparasites with active host-seeking behaviour (fleas). We recorded behavioural responses of wild-captured bats in a novel-environment test and then sampled each individual for ectoparasites. After accounting for age and sex we found mixed support for our hypotheses in some but not all demographics. More active adult and young of the year (YOY) males were more likely to host mites while more active adult and YOY females were less likely to host fleas. Our results highlight possible differences in the influence of host and parasite behaviour on parasite transmission dynamics for colonial compared to non-colonial species and have conservation implications for understanding pathogen transmission in bat white-nose syndrome and other wildlife diseases.

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Context-dependent behavioral plasticity compromises disruptive selection on sperm traits in squid

10.1101/2020.08.20.258988 ◽

2020 ◽

Author(s):

Noritaka Hirohashi ◽

Noriyosi Sato ◽

Yoko Iwata ◽

Satoshi Tomano ◽

Md Nur E Alam ◽

...

Keyword(s):

Behavioral Plasticity ◽

Mating Behaviour ◽

Social Contexts ◽

Disruptive Selection ◽

Behavioural Plasticity ◽

Male Mating ◽

Reproductive Tactics ◽

Developmentally Regulated ◽

Mating Opportunities ◽

Sperm Traits

Male animals are not given equal mating opportunities under competitive circumstances. Small males often exhibit alternative mating behaviours and produce spermatozoa of higher quality to compensate for their lower chances of winning physical contests against larger competitors [1]. Because the reproductive benefits of these phenotypes depend on social status/agonistic ranks that can change during growth or aging [2], sperm traits should be developed/switched into fitness optima according to their prospects. However, reproductive success largely relies upon social contexts arising instantaneously from intra- and inter-sexual interactions, which deter males from developing extreme traits and instead favour behavioural plasticity. Nevertheless, the extent to which such plasticity influences developmentally regulated alternative sperm traits remains unexplored. Squids of the family Loliginidae are excellent models to investigate this, because they show sophisticated alternative reproductive tactics (ARTs) by which small males, known as “sneakers”, produce longer spermatozoa and perform extra-pair copulation to attach their sperm packages near the female seminal receptacle (SR). In contrast, large “consort” males have shorter spermatozoa and copulate via pair-bonding to insert their sperm packages near the internal female oviduct [3]. In addition, plasticity in male mating behaviour is common in some species while it is either rare or absent in others. Thus, squid ARTs display a broad spectrum of adaptive traits with a complex repertoire in behaviour, morphology and physiology [3].

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Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

Scientific Reports ◽

10.1038/s41598-020-77256-y ◽

2020 ◽

Vol 10 (1) ◽

Cited By ~ 1

Author(s):

Gabrielle L. Davidson ◽

Niamh Wiley ◽

Amy C. Cooke ◽

Crystal N. Johnson ◽

Fiona Fouhy ◽

...

Keyword(s):

Problem Solving ◽

Gut Microbiota ◽

Gut Microbiome ◽

Parus Major ◽

Behavioural Plasticity ◽

Wild Populations ◽

Problem Solve ◽

Induced Changes ◽

Host Behaviour ◽

Problem Solving Task

AbstractThe microbial community in the gut is influenced by environmental factors, especially diet, which can moderate host behaviour through the microbiome-gut-brain axis. However, the ecological relevance of microbiome-mediated behavioural plasticity in wild animals is unknown. We presented wild-caught great tits (Parus major) with a problem-solving task and showed that performance was weakly associated with variation in the gut microbiome. We then manipulated the gut microbiome by feeding birds one of two diets that differed in their relative levels of fat, protein and fibre content: an insect diet (low content), or a seed diet (high content). Microbial communities were less diverse among individuals given the insect compared to those on the seed diet. Individuals were less likely to problem-solve after being given the insect diet, and the same microbiota metrics that were altered as a consequence of diet were also those that correlated with variation in problem solving performance. Although the effect on problem-solving behaviour could have been caused by motivational or nutritional differences between our treatments, our results nevertheless raise the possibility that dietary induced changes in the gut microbiota could be an important mechanism underlying individual behavioural plasticity in wild populations.

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Modification of host social networks by manipulative parasites

Behaviour ◽

10.1163/1568539x-00003456 ◽

2018 ◽

Vol 155 (7-9) ◽

pp. 671-688 ◽

Cited By ~ 5

Author(s):

Robert Poulin

Keyword(s):

Social Networks ◽

Social Network ◽

Mating Behaviour ◽

Group Formation ◽

Network Models ◽

Parasite Transmission ◽

Activity Levels ◽

Parasite Infections ◽

Experimental Approaches ◽

Host Behaviour

Abstract Social network models provide a powerful tool to estimate infection risk for individual hosts and track parasite transmission through host populations. Here, bringing together concepts from social network theory, animal personality, and parasite manipulation of host behaviour, I argue that not only are social networks shaping parasite transmission, but parasites in turn shape social networks through their effects on the behaviour of infected individuals. Firstly, I review five general categories of behaviour (mating behaviour, aggressiveness, activity levels, spatial distribution, and group formation) that are closely tied to social networks, and provide evidence that parasites can affect all of them. Secondly, I describe scenarios in which behaviour-altering parasites can modify either the role or position of individual hosts within their social network, or various structural properties (e.g., connectance, modularity) of the entire network. Experimental approaches allowing comparisons of social networks pre- versus post-infection are a promising avenue to explore the feedback loop between social networks and parasite infections.

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Lysophosphatidylcholine: A Novel Modulator ofTrypanosoma cruziTransmission

Journal of Parasitology Research ◽

10.1155/2012/625838 ◽

2012 ◽

Vol 2012 ◽

pp. 1-8 ◽

Cited By ~ 7

Author(s):

Mário A. C. Silva-Neto ◽

Alan B. Carneiro ◽

Livia Silva-Cardoso ◽

Georgia C. Atella

Keyword(s):

Immune System ◽

Chagas Disease ◽

Inflammatory Cells ◽

Parasite Infection ◽

Atheromatous Plaque ◽

No Production ◽

Parasite Transmission ◽

Parasite Invasion ◽

Cellular Processes ◽

Signaling Mechanisms

Lysophosphatidylcholine is a bioactive lipid that regulates a large number of cellular processes and is especially present during the deposition and infiltration of inflammatory cells and deposition of atheromatous plaque. Such molecule is also present in saliva and feces of the hematophagous organismRhodnius prolixus, a triatominae bug vector of Chagas disease. We have recently demonstrated that LPC is a modulator ofTrypanosoma cruzitransmission. It acts as a powerful chemoattractant for inflammatory cells at the site of the insect bite, which will provide a concentrated population of cells available for parasite infection. Also, LPC increases macrophage intracellular calcium concentrations that ultimately enhance parasite invasion. Finally, LPC inhibits NO production by macrophages stimulated by liveT. cruzi, and thus interferes with the immune system of the vertebrate host. In the present paper, we discuss the main signaling mechanisms that are likely used by such molecule and their eventual use as targets to block parasite transmission and the pathogenesis of Chagas disease.

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Host location, survival and fecundity of the Oriental rat flea Xenopsylla cheopis (Siphonaptera: Pulicidae) in relation to black rat Rattus rattus (Rodentia: Muridae) host age and sex

Bulletin of Entomological Research ◽

10.1079/ber2002184 ◽

2002 ◽

Vol 92 (5) ◽

pp. 375-384 ◽

Cited By ~ 5

Author(s):

S. Mears ◽

F. Clark ◽

M. Greenwood ◽

K.S. Larsen

Keyword(s):

Sex Ratio ◽

Rattus Rattus ◽

Host Choice ◽

Host Age ◽

Xenopsylla Cheopis ◽

Black Rat ◽

Host Seeking ◽

Host Sex ◽

Host Behaviour ◽

Age And Sex

AbstractHost choice and fecundity are two factors that may contribute to the variation in flea counts observed when assessing the potential risk of flea-borne transmission of pathogens from rodents to humans. Using the black rat, Rattus rattus Linnaeus, as host the effects of age and sex on host choice and fecundity of the Oriental rat flea, Xenopsylla cheopis Rothschild, were examined experimentally at 25°C and 80% rh. During the first two days of emergence from cocoons, female fleas dominated the sex ratio by 4:1 but from the third day onwards this switched to a male-dominated sex ratio of 4:1. The sex of the flea did not influence their host-seeking behaviour. Newly emerged fleas of both sexes were not influenced by the rat‘s presence and at seven days old both sexes demonstrated similar levels of attraction toward the rat host. The sex of the rat did not affect flea host-seeking behaviour. There was a 50–70% decline in the initial number of adult fleas during the first week after their release onto a rat host, and this decline was greatest on juvenile rats. Flea fecundity was also significantly lower on juvenile rat hosts but no differences due to the sex of the rat were observed. This experimental study supports the hypothesis that differences in flea count due to host sex, reported in field surveys, result from sexual differences in host behaviour and not from discriminatory host-seeking behaviour by X. cheopis. Differences in flea count due to host age may be affected by differences in X. cheopis fecundity, which may itself be mediated by host behaviour such as grooming.

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Horizontal transfer of parasitic sex ratio distorters between crustacean hosts

Parasitology ◽

10.1017/s0031182098002820 ◽

1998 ◽

Vol 117 (1) ◽

pp. 15-19 ◽

Cited By ~ 13

Author(s):

A. M. DUNN ◽

T. RIGAUD

Keyword(s):

Sex Ratio ◽

Sex Determination ◽

Host Specificity ◽

Host Species ◽

Horizontal Transfer ◽

Parasite Infection ◽

Parasite Transmission ◽

Ratio Distortion ◽

Sex Ratio Distortion ◽

Crustacean Host

Parasitic sex ratio distorters were artificially transferred within and between crustacean host species in order to study the effects of parasitism on host fitness and sex determination and to investigate parasite–host specificity. Implantation of Nosema sp. to uninfected strains of its Gammarus duebeni host resulted in an active parasite infection in the gonad of recipient females and subsequent transovarial parasite transmission. The young of artificially infected females were feminized by the parasite, demonstrating that Nosema sp. is a cause of sex ratio distortion in its host. In contrast, we were unable to cross-infect Armadillidium vulgare with the feminizing microsporidian from G. duebeni or to cross-infect G. duebeni with the feminizing bacterium Wolbachia sp. from A. vulgare.

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Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

10.1101/827741 ◽

2019 ◽

Cited By ~ 1

Author(s):

Gabrielle L. Davidson ◽

Niamh Wiley ◽

Amy C. Cooke ◽

Crystal N. Johnson ◽

Fiona Fouhy ◽

...

Keyword(s):

Problem Solving ◽

Gut Microbiota ◽

Gut Microbiome ◽

Parus Major ◽

Behavioural Plasticity ◽

Wild Populations ◽

Problem Solve ◽

Induced Changes ◽

Host Behaviour ◽

Problem Solving Task

ABSTRACTThe microbial community in the gut is influenced by environmental factors, especially diet, which can moderate host behaviour through the microbiome-gut-brain axis. However, the ecological relevance of microbiome-mediated behavioural plasticity in wild animals is unknown. We presented wild-caught great tits (Parus major) with a problem-solving task and showed that performance was weakly associated with variation in the gut microbiome. We then manipulated the gut microbiome by feeding birds one of two diets that differed in their relative levels of fat, protein and fibre content: an insect diet (low content), or a seed diet (high content). Microbial communities were less diverse among individuals given the insect compared to those on the seed diet. Individuals were less likely to problem-solve after being given the insect diet, and the same microbiota metrics that were altered as a consequence of diet were also those that correlated with variation in problem solving performance. Although the effect on problem-solving behaviour could have been caused by motivational or nutritional differences between our treatments, our results nevertheless raise the possibility that dietary induced changes in the gut microbiota could be an important mechanism underlying individual behavioural plasticity in wild populations.

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