Guppies only avoid infected shoalmates when they pose the highest risk of transmission

Jess Stephenson is a new Assistant Professor at the University of Pittsburgh, USA. She is interested in factors affecting the spread of infectious diseases through natural populations, and how these ecological factors might affect the evolution of both host and parasite. Here, she describes her most recent paper on the role of host behaviour in disease transmission and shares the #StoryBehindThePaper.

Across animal taxa, individuals tend to avoid conspecifics infected with contagious diseases. In fact, these ‘social barriers’ to disease transmission are well recognised and can be as important as physiological immune defences in avoiding or reducing the costs of an infection. However, avoiding conspecifics, infected or not, carries its own costs; group living individuals of many species can enjoy increased defence against predators and some parasites, increased mating opportunities, help with parental care, increased foraging efficiency… the list goes on. So, while avoiding infection is clearly desirable and a commonly observed behaviour, there is likely to be a trade-off with the costs incurred by avoiding conspecifics.

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Are guppies gullible? Or do they know an infected conspecific when they see one? (Photo: Jessica F Stephenson)

Another commonly observed phenomenon is that not all infected individuals are equally likely to transmit their infection. In fact, many epidemics conform to the 20:80 rule, in that 80% of the transmission events are due to only 20% of the infected individuals in a population, referred to as ‘super-spreaders’. The majority of infected individuals may therefore pose no or very little risk of transmission to the uninfected individuals in a group. So, if uninfected individuals are able to identify and selectively avoid only those infected group members that may become super-spreaders, they might reduce the chance of becoming infected (a often cited cost of group living), while continuing to enjoy the benefits of remaining with the group.

While I would love to say we set out to test whether guppies could show risk-sensitive infection avoidance behaviour when collecting the data for our recent paper in the Journal of Animal Ecology … we didn’t. The original idea for this project was a very simple one – can guppies smell or see infection in conspecifics? The parasite we used, Gyrodactylus turnbulli, is an ectoparasite of just under 1mm in length. The worms grow exclusively on the fins and skin of the fish, and tend to wave around a bit when the fish is still. In other words, they should be screamingly obvious to other fish. Additionally, a paper had just come out showing that guppies can smell the reproductive status of females, indicating a sophisticated olfactory system that again, should intuitively be able to discriminate between healthy and sick guppies.

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Waving worms – Gyrodactylus turnbulli is an ectoparasite that grows exclusively on fish fins and skin, and tend to wave around a bit when the fish is still (GIF: Jessica F Stephenson)

Serendipitously, and largely because of the logistics of behavioural trials, I collected data from fish exposed to conspecifics infected for varying periods of time, up to 19 days. From the data it was clear that something about the duration of the infection on these ‘stimulus fish’ was really important – we only saw evidence of infection avoidance behaviour after about 15 days of infection. While even a fish with a single worm represents a potential transmission risk (the parasite has no specific transmission stage, and it only takes one worm to initiate an infection), at this stage (late in the process, I know!) I began to wonder whether the test fish were responding to increasing transmission risk through the duration of infection.

While I was mulling over these data, Jo Cable and Sarah Perkins (my co-authors on this paper) were running a transmission experiment using this system that shed light on the factors involved in determining a guppy’s probability of transmitting the parasite. These were the guppy’s ‘infection load’ (how many parasites it was infected with at the point of transmission), its ‘infection integral’ (the area under the curve of infection load over the duration of infection), and how long it had been infected. How long a fish has been infected is therefore important in determining transmission risk both on its own, and because in this system infection load changes rapidly over time: the parasite reproduces directly on fish skin with a generation time of 24 hours, so an individual fish infected initially with two worms might have an infection load of over 100 after 10 days.

The critical importance of duration of infection in the transmission experiment indicated that the infected stimulus fish in the behavioural experiment may indeed pose very different levels of transmission risk on different days of infection. To quantify this variation in transmission risk, I used the models built to explain variation in how many parasites transmitted and how quickly transmission occurred in the transmission experiment to predict how many parasites would transmit, and how quickly, from the stimulus fish in the behavioural experiment. Excitingly, there is a striking pattern – the days on which the models predict transmission risk to be highest are those days on which avoidance behaviour is strongest. Therefore, whether or not guppies can detect infection in conspecifics before 15 days of infection, they only show avoidance after this point, which corresponds to when the parasite is most likely to transmit.

Work in my new lab at the University of Pittsburgh is aimed at understanding how this risk-sensitive infection avoidance behaviour at the individual level may affect disease dynamics at the population level, and hence the evolutionary responses of both host and parasite. For example, if infection avoidance behaviour is effective at reducing transmission, and only occurs after 15 days of infection, can the parasite evolve to transmit earlier in infection? Indeed, from our data it appears that early in infection the infected fish were marginally preferred over uninfected fish based on visual cues – why? Whatever the mechanism, could it be an adaptation to ensure transmission before this critical 15-day threshold is reached?

In summary, what started out as a simple experiment at the beginning of my PhD grew and grew into what is now a really exciting research programme. Thanks to the unique properties of the guppy-Gyrodactylus system, we have a rare opportunity to test the predictions of sophisticated theoretical work and begin describing how host behaviour, transmission risk, and their interaction combine to affect disease dynamics in natural populations.

More Info:

Stephenson, J.F., Perkins, S.E., and Cable, J. (2018) Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies. Journal of Animal Ecology, 87: 1525–1533. https://doi.org/10.1111/1365-2656.12885

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