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Combined analysis of primate and parasite traits reveals new insights on ecological networks

/ Beth Preston / Leave a comment
This blog post is provided by James Herrera, Ph.D., Duke Lemur Center SAVA Conservation Initiative and tells the #StoryBehindthePaper for the paper “Predicting primate-parasite associations using exponentional random graph models”, which was recently published in Journal of Animal Ecology. In their paper they show that large primates in warm climates and sharing the same biogeographic region have more parasites than small species in cool, dry climates. Parasites known from multiple non-primate hosts, especially viruses, protozoa, and helminth worms infect more primates than primate-specific parasites or fungi and bacteria. Advanced social network analyses allowed the first multidimensional analysis of primate-parasite ecological interactions.

After three years of the coronavirus pandemic, we have all become keenly aware of the impacts pathogens have on global systems. Parasites are ubiquitous in nature, including all species that live on or inside another organism – the host – from which they get their resources. Wild animals are often co-infected by multiple parasites at the same time. The chimpanzee, for example, is known to host over 100 parasites; chimps are one of the best studied primates because of their close relationship to people and the relevance of chimp parasites for human health. In contrast, species like the indri, a lemur only found on Madagascar, are only known to host about 10 parasites. Many other primates are so poorly studied, only 1 parasite has ever been recorded.

Chimpanzees (left) are one of the best studied primates for parasite interactions. In contrast, the indri (right) is comparatively poorly known for its parasites. (Photo credits: chimpanzee: Wikimedia Commons; indri: James Herrera)

In a new study published in the Journal of Animal Ecology, we examined which traits of both primates and parasites predict the likelihood of their interactions. Using advanced techniques in social network analysis, called the exponential random graph, we were able to simultaneously test the traits of primates and parasites to determine what predisposes primates to infection and what gives some parasites a unique advantage. For primates, larger species that are found in warmer, wetter climates are more likely to host diverse parasites, compared to smaller species living in drier, cooler climates. Further, species in the same branches of the evolutionary tree and those that live in the same geographic region are more likely to share parasites than more distantly related species found on different continents. Viruses, protozoa, and helminth worms are more likely to infect diverse primates than fungi, arthropods, and bacteria. Parasites that are known to infect non-primate mammals are also more likely to infect diverse primates.

A photo from a microscope slide showing the blood parasite Plasmodium falciparum, one of the pathogens that causes malaria, a devastating disease in people, and also infects 118 other primates. In contrast, there are at least 30 other kinds of Plasmodium that only infect one or a few primates and effects on disease are poorly understood. (Photo credit: Wikimedia Commons)

These new results were made possible by the great advances being made in infectious disease ecology. Over the last two decades, Dr. Charles Nunn at Duke University’s Evolutionary Anthropology and Global Health departments has been working with teams of researchers to compile all published records of primate-parasite interactions. Combing through the literature, almost 600 published sources were obtained to glean which parasites are found in over 200 primates species, with over 2,300 interactions recorded. With the analytical tools in social network science mastered by Duke Sociology professor Dr. James Moody, we were able to systematically test how traits of both hosts and parasites affect the likelihood of their interaction for the first time. While many previous studies used subsets of this database and examined either hosts or parasites in isolation, we were able to make new inferences about the critical links in this unique ecological network.

This work builds on a recent study that showed how extinction of primate hosts could lead to the co-extinction of almost 200 parasite species. While at first this might seem like a good thing, in fact it could have negative impacts on biodiversity as a whole. Many parasites don’t actually cause disease or death in the hosts, and some may even have beneficial properties. We simply don’t know enough about these critical and co-evolved relationships to understand what effects host-parasite coextinctions could have in the long-term.

While it might seem strange to worry about parasite extinctions, they are actually an important part of biodiversity and ecosystem functions. Understanding how primates and parasites interact reveals new insights into coevolutionary theory, and could also contribute to the conservation of underappreciated species richness. While from a public health perspective, we’d like to see some parasites disappear, like corona and ebola viruses, from an evolutionary stance, the sheer diversity of parasites and their intimate relationships with their hosts make them fascinating and crucial components of biodiversity.

Read the paper

Read the full paper here: Herrera, J.P., Moody, J. and Nunn, C.L. (2023), Predicting primate-parasite associations using exponentional random graph models. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13883

Parasites are just the strings: Microbes as the real puppet masters in phenotypic manipulations of parasitized animals

/ Beth Preston / Leave a comment
This blog post is provided by Priscila Salloum, Fátima Jorge and Robert Poulin and tells the #StoryBehindThePaper for the paper “Inter-individual variation in parasite manipulation of host phenotype: a role for parasite microbiomes?“, which was recently published in the Journal of Animal Ecology. They explore how differences in the microbiome of parasites might impact the way that those parasites can manipulate their hosts’ behaviour.

Many parasites have the impressive ability of bending their hosts’ will, manipulating the host’s phenotype or behaviour, like real puppet masters. You have probably heard about the hairworm that makes its cricket host jump into water so that the mature worm can come out in its perfect environment – water. Or you might have seen something about parasitised animals that become less conspicuous and are more easily found by their predators, the parasite’s definitive host (Figure 1). However, there is great variability in host behavioural manipulation induced by parasites, and a real gradation in possible levels of manipulation achieved in individual parasite-host interactions.

Figure 1.  The parasite Profilicollis novaezealandiae infecting a shore crab in New Zealand, for which infection levels seem correlated with changes in hiding behaviour1. (Photo credit: Jerusha Bennett)

When the mechanisms underlying phenotypic manipulation are known, they involve alterations in the hosts’ neural system, hormones, or immune response, or even a direct change in the expression of genes responsible for specific host behaviours. These alterations happen to a different degree in different individuals. If the host’s phenotypic manipulation induced by the parasite had a fixed outcome, we would expect to see most infected hosts with a similar manipulated phenotype. Intuitively, we could be thinking that there is an evolutionary benefit for the parasite in manipulating the phenotype of its host, and that an ‘optimal’ phenotype would be the ideal outcome for the parasite. However, there is not enough evidence in support of such narrow outcomes from phenotypic manipulation in parasitised animals, and in fact, the phenotypic variability after parasitic infection is as broad as in uninfected animals (Figure 2). So, what causes this great variability? To a certain extent, genetic and non-genetic factors such as age or body condition of both the host and the parasite, as well as environmental differences. But much of the variation remains unexplained.

Figure 2. The relationship between infected and uninfected hosts shows highly variable phenotypes also after infection, supporting that there is not a narrow outcome of phenotypic manipulation by parasites, whether the parasite is transmitted by predation of the intermediate host (yes, blue) or not (no, red). (Figure credit: Priscila Salloum, based on data from Nakagawa et al.2)

In an invited perspective piece in the Journal of Animal Ecology, we considered a different take on the reasons for the variation in parasite-induced phenotypic manipulations, proposing a hypothesis and potential research directions for the future. With the growing knowledge of the importance of microbiomes in shaping so many aspects of all organisms on Earth, our hypothesis is that differences in the composition and abundance of specific microbes associated with the parasites may play a large role in the outcome of parasite-induced host manipulation. Embracing the holobiome concept, microbes inhabiting the parasite have their own set of genes which will contribute towards the evolution of parasite and microbes as a whole and unique entity, fine-tuned to getting the best out of their environment (be it microbes getting the best out of their parasites, or both getting the best out of the parasitised host). This means that instead of looking at parasite-host interactions as a two-dimensional system, we should be looking at multi-dimensional interactions happening within the parasite (with its microbiome), between the parasite’s microbiome and the animal host’s microbiome, and between the parasite and the animal host (which also extends to the interactions of the animal host with its own microbiome, but this is not the matter we focus on).

Suppose that, apart from the parasites’ microbiome, all else is similar among parasites and among their hosts (i.e. genes, environment, etc). In this case, the presence or abundance of certain microbes within a parasite would determine the magnitude of the changes induced in the host. The microbes, in symbiosis with the parasite, will benefit from parasitic transmission to their next animal host: if the parasite (which is their ‘home and resource’) is successful, the microbes will also prevail. Thus, the outcome of phenotypic manipulation matters as much to the evolution of the parasite as it matters to the evolution of its microbiome. There are two underlying assumptions to such a statement:

  1. The microbiome of the parasite is different from the microbiome of its hosts, which has been demonstrated before, supporting our hypothesis3,4;
  2. Microbes are transmitted among life-stages (or different generations) of the parasite, which has also been demonstrated before5, so also supports our hypothesis.

The microbiome of different individual parasites has a different composition and abundance of microbes, with great variation even among individual parasites of the same population. This is caused by processes like acquiring microbes from different sources from the previous generation (such as with diet), competition among lineages within a parasite, and because not all microbes from the parent parasite will succeed in being transferred to its offspring. Such variation in the microbiome of individual parasites may be linked to variability in the levels of parasite-induced host phenotypic manipulation (Figure 3). That is, parasites with different microbiomes may have different impacts on the phenotype of their hosts.

Figure 3. Schematic representation of possible changes in the phenotype (colour) of an amphipod host induced by an acanthocephalan parasite (represented by a black outline within the amphipod shades), correlated with microbiome composition and abundance (represented by the small shapes inside the acanthocephalan). (Figure credit: Poulin et al., 20226).

There are examples of individual microbes interacting with parasites in manipulating the phenotype of their hosts7-10. Now consider that many different microbes in the parasite`s microbiome contribute to changes in the phenotype of the parasitised host. Going forward, microbiome characterisations of both parasites and their hosts using -omics approaches can lead to finding relevant molecules in the mechanics of phenotypic change, assigning molecules to specific genes (and their organism), and potentially silencing these genes to assess their importance in inducing phenotypic change. Additionally, modifying the microbiome of parasites with antibiotics treatment, and assessing the phenotypic change of organisms infected with control and treated parasites can lead to more direct evidence of the importance of the many-fold microbial players in parasite-induced host phenotypic manipulation. Should we be calling it holobiome-induced host phenotypic manipulation?

About the authors

Robert Poulin has been at the University of Otago for 30 years, during which his research has explored host-parasite interactions from multiple ecological and evolutionary perspectives, across all taxa and using a broad range of approaches.

Fátima Jorge was a postdoctoral fellow at the University of Otago where she applied a wide range of multidisciplinary approaches to investigate the (co)evolutionary patterns of parasite diversification, and the role and diversity of the microbiota within and across host-parasite-microbe interactions.

Priscila Salloum is a postdoctoral fellow at the University of Otago. She is interested in understanding mechanisms driving phenotypic diversification and adaptation, and is applying her genomics background to uncover the roles of the microbiota in the phenotypic changes linked to parasitic infections.

Find out more about the Evolutionary and Ecological Parasitology Research Group here.

Read the paper

Read the full paper here: Poulin, R., Jorge, F., & Salloum, P. M. (2022). Inter-individual variation in parasite manipulation of host phenotype: A role for parasite microbiomes?. Journal of Animal Ecology, 00, 1– 6. https://doi.org/10.1111/1365-2656.13764

References
  1. Latham, A., & Poulin, R. (2002). Effect of acanthocephalan parasites on hiding behaviour in two species of shore crabs. Journal of Helminthology, 76(4), 323-326. doi:10.1079/JOH2002139
  2. Nakagawa, S., Poulin, R., Mengersen, K., Reinhold, K., Engqvist, L., Lagisz, M., & Senior, A. M. (2015). Meta-analysis of variation: ecological and evolutionary applications and beyond. Methods in Ecology and Evolution, 6, 143–152.
  3. Jorge, F., Dheilly, N. M., & Poulin, R. (2020). Persistence of a core microbiome through the ontogeny of a multi-host parasite. Frontiers in Microbiology, 11, 954. https://doi.org/10.3389/fmicb.2020.00954
  4. Jorge, F., Dheilly, N. M., Froissard, C., Wainwright, E., & Poulin, R. (2022a). Consistency of bacterial communities in a parasitic worm: variation throughout the life cycle and across geographic space. Microbial Ecology, 83, 724–738.
  5. Vaughan, J. A., Tkach, V. V., & Greiman, S. E. (2012). Neorickettsial endosymbionts of the Digenea: diversity, transmission and distribution. Advances in Parasitology, 79, 253–297.
  6. Poulin, R., Jorge, F., Salloum, P. (2022). Inter-individual variation in parasite manipulation of host phenotype: a role for parasite microbiomes? Journal of Animal Ecology, 00, 1-6. doi: 10.1111/1365-2656.13764
  7. Kaiser, W., Huguet, E., Casas, J., Commin, C., & Giron, D. (2010). Plant green-island phenotype induced by leaf-miner is mediated by bacterial symbionts. Proceedings of the Royal Society B, 277, 2311–2319.
  8. Frago, E., Dicke, M., & Godfray, H. C. J. (2012). Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology and Evolution, 27, 705–711.
  9. Goodrich-Blair, H., & Clarke, D. J. (2007). Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Molecular Microbiology, 64, 260–268.
  10. Dheilly, N. M., Maure, F., Ravallec, M., Galinier, R., Doyon, J., Duval, D., Leger, L., Volkoff, A.-N., Missé, D., Nidelet, S., Demolombe, V., Brodeur, J., Gourbal, B., Thomas, F., & Mitta, G. (2015b). Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proceedings of the Royal Society B, 282, 20142773.

International Women’s Day 2021

/ Beth Preston / Leave a comment

This International Women’s Day we look back over the blogs from the last year, and highlight four of our favourites written by women. Celebrate women in science, and the awesome work they’ve done by checking out our favourites below, as well as a brief profile of each of the authors and links to find more of their work.

Tamara Layden

Tamara’s blog post Hidden, but not insignificant – appreciating parasites in stream ecology was one of our favourites this year. A fascinating insight into the lives of parasites, Tamara’s blog will persuade you of the importance of these small and often overlooked creatures.

Tamara (she | they) is an ecologist with over eight years of experience in academia and the nonprofit sector. She currently manages a freshwater ecology lab at Reed College and also serves on the Environmental Professionals of Color leadership team, the Oregon Zoo Community Advocacy Council, and chairs a committee on the Portland Parks & Recreation Advisory Board. Tamara is passionate about supporting ecosystem and community resiliency through scientific research, community development, and social justice and wildlife advocacy. She has a variety of experience in the environmental field and is committed to wildlife conservation and cultivating an inclusive community of scientists, land stewards, and outdoor enthusiasts. Twitter and Instagram handle: @TamaraLayden

Felicie Dhellemes

Felicie’s blog Personality and pace-of-life in free-ranging lemon sharks: a field recipe is a really original blog, and a firm favourite of the year. Felicie presents her study as a recipe, giving you the ingredients and all the steps you need to follow in her footsteps researching lemon shark personality, as well as lots of great photos of sharks and her field site.

On or under the water is where you are most likely to find Félicie Dhellemmes. After a masters in engineering, this young behavioural ecologist spent four years in the Bahamas collecting data for her PhD investigating personality in a coastal shark species: the lemon shark. As a project leader at the Bimini Biological Field Station (www.biminisharklab.com) and the Save our Seas foundation (www.saveourseas.com), Félicie gained extensive field experience and is not scared to get her hands dirty. Some of her most recent work from this project on personality and pace-of-life was featured in our blogs. Her interests are not limited to sharks: She is involved in a project on striped marlin and recently started a post-doc on Northern Pike. She hopes to expand her species range to birds and terrestrial species in the future. Twitter: @FelicieDh (Photo credit: Shin Sirachai Arunrugstichai)

Ana M. Gonzalez

Ana’s blog post A migratory bird’s journey from the Andes of Colombia to North America: Leave early and take it easy or leave late and migrate fast?, another favourite from this year, tells the story of one Swainson’s thrush, Pecas (Freckles). She follows his journey from Colombia all the way to Canada, highlighting the patterns of migration in this species. You can also read her blog in Spanish, here.

Ana was born and raised in the Andean mountains of Colombia. Her passion for birds and migration took her to Canada 13 years ago, where she obtained a M.Sc. and a Ph.D. degree at the University of Saskatchewan. Currently, Ana is a postdoctoral researcher with Environment and Climate Change Canada @ECCCSciTech and a researcher with the Colombian organization “Selva” @Selvaorgco. She has studied migrants across their full annual cycle in Colombia, Mexico, and North America. In her research, she integrates behavioral and demographic field data with state-of-the-art tracking techniques to provide foundational scientific information needed to support international and local conservation strategies for several Neotropical migrants of conservation concern. Twitter handle: @AnaCardellina. Follow hashtags #MotusWTS (operated by @BirdsCanada) #cienciacriolla to see more.

Friederike Gebert

Friederike’s blog Large mammals at Mount Kilimanjaro: the importance of resource availability and protected areas gives a real insight into the story behind her paper, and what inspired her study. Including some lovely camera trap photos of mammals on Mt Kilimanjaro, it’s definitely one to read!

Friederike studied biology at the University of Freiburg and at the University of Leeds. During her studies, she spent two months at the Bilsa Biological Station, Ecuador, and has been fascinated by tropical entomology ever since. After her diploma on epigeal arthropods, she completed an internship in the Coleoptera Department of the Natural History Museum, London. She did her PhD at the University of Würzburg about mammals and dung beetles on Mt. Kilimanjaro. Currently, she is a postdoc at the Swiss Federal Institute for Forest, Snow and Landscape Research (WSL) where she investigates the biodiversity of aquatic and terrestrial insects in Switzerland. Twitter handle: @Freaky_G88. Website: https://www.wsl.ch/de/mitarbeitende/gebertfr.html

Determinants of micro- and macroparasite diversity in birds: the fruits of comparing apples and oranges

/ Sarah Marley / Leave a comment

Identifying the factors shaping variation in parasite diversity among host species is crucial to understand wildlife diseases. A recent paper in Journal of Animal Ecology investigated the role of host life history and ecology in explaining the species richness of micro- and macro-parasites in birds world-wide. Lead author Dr Jorge Sanchez Gutierrez explains more about the study.

The phrase “comparing apples and oranges” is often used in ecological and evolutionary contexts to make the point that differences in the “basic biology” of different taxa make any comparison invalid. Like apples and oranges, haemosporidians (unicellular blood parasites causing malaria-like diseases in birds) and helminths (parasitic worms such as tapeworms, roundworms and flukes) are in different branches of the taxonomic tree. But are they that different?

Unlike the tiny mosquito-borne haemosporidians, helminths are usually visible to the naked eye and do not multiply directly within an infected individual. Instead they produce infective stages that usually pass out of the host before transmission to another host. Unlike blood parasites, helminths tend to produce weaker immune responses in infected birds. It is thus likely that the two classes of parasites would lead to different selection pressures on hosts, and vice versa.

Yet, despite obvious differences in their transmission modes and virulence, they often infect the same host—be it an individual, a population or a species. Surely then, there are valid comparisons that can be made? And would such a comparative approach also identify potential red herrings arising from single group-based approaches? A comparison between these parasitic apples and oranges could help illuminate whether and how bird traits shape the diversity of these two parasite groups.

Cestode

Cestode (Image: Jorge Sanchez Gutierrez)

Avian_malaria2

Avian malaria (Image: Jorge Sanchez Gutierrez)

To answer this question, I teamed up with my colleagues David Thieltges and Theunis Piersma, both senior researchers at the Royal Netherlands Institute for Sea Research with broad and complementary experience in the field of parasite/host ecology. In an earlier study, published in Journal of Biogeography in 2017 (https://onlinelibrary.wiley.com/doi/abs/10.1111/jbi.12956), we (together with Eldar Rakhimberdiev) examined the correlates of helminth richness in Charadriiform birds (waders, gulls, auks and allies). We found that birds that exploit diverse diets and habitats harbour more helminth species, that is, relative to specialist birds.

In the present study in the Journal of Animal Ecology we went one step further and investigated whether these and other host traits (for example, migration distance, longevity or coloniality) correlate with the species richness of helminths and haemosporidians in birds worldwide. Historically, this line of research has focused on mammals, since global databases encompassing both micro- and macroparasites were largely restricted to mammals.

This meant that I had to put my shoulders to the wheel and combined several global-scale datasets on traits of over 300 bird species and the numbers of their blood and worm parasites. After controlling for research effort—some bird species are better studied than others—and bird phylogeny, we found that helminth richness positively correlated with bird longevity, geographic range size, dietary breadth and migration distance. Overall, such results are consistent with epidemiological and biogeographical processes. To our surprise, however, the only factor that explained some variation in the richness of blood parasites was research effort!

Jorge Graphical Abstract

Perhaps the simplest explanation for this lack of association between haemosporidian richness and bird traits is that blood parasites may be more influenced by factors related to the ecology of the arthropod vectors than the traits of the host. Another possibility to explain the non-significant relationship between haemosporidian richness and bird longevity (which we predicted to be negative, as haemosporidians can lower survival rate) is that haemosporidian parasites may lead to effective immune defence strategies, the response destroying what would have initially been an association. On the contrary, we found a positive effect for less pathogenic helminths that seldom kill their host. It might well be that long host lifespans promote the diversity of helminth parasite assemblages over evolutionary time, ultimately resulting in richer helminth faunas.

Although from a statistical point of view it remains open whether there are actual differences between the two parasite groups in the role of host life history and ecology in determining parasite richness of birds, the presence of many significant correlates within helminths but none in haemosporidians is intriguing. We hope that this study will bring renewed attention to the factors that determine patterns of parasitic infections. While writing this blog-post from tropical West Africa, where parasitic helminths are among the most common chronic infections and malaria parasite infection the most deadly, I realize about the importance of investigating the drivers of global patterns of parasite diversity and distribution to anticipate disease emergence risks, in both humans and wildlife.

More info:

Gutiérrez, Piersma and Thieltges (2019) Micro- and macroparasite species richness in birds: the role of host life history and ecology. Journal of Animal Ecology.

Parasitism and Host Diet Quality in Natural Populations

/ Sarah Marley / Leave a comment

Parasite-host relationships can be amazingly complex. Parasites can even alter host diets. But how exactly does this work? Dr Charlotte Narr, a Research Scientist at Colorado State University’s Natural Resource Ecology Laboratory, recently published an article on just this topic in the Journal of Animal Ecology. 

When you’re sick, your relationship with food changes. You might lose your appetite or have trouble digesting certain foods. Pregnancy can have an even bigger effect on what and how much you eat. Now, imagine that you are an organism that feeds constantly to support your continuous investment in reproduction. Then you get sick. And you aren’t alone, just about everyone in your population is constantly eating to produce offspring and, just like you, they’ve gotten sick.

It isn’t good for your offspring, the sickness. You inadvertently ate the parasite with your food, and now it’s stealing the nutrients you ingested with it, repurposing them for its own reproduction, and messing with your digestion. You can’t produce as many offspring, and the ones you do produce are also sick. So your offspring produce fewer offspring, and you can see that your population growth rate is starting to drop.

Daphnia female - Dieter Ebert

Daphnia magna with eggs in brood sac (Photo: Dieter Ebert)

You’re a water flea, Daphnia magna, to be precise, and your relationship with food is legendary. So much so that the shuffling of nutrients between zooplankton like you and your algal food inspired the term ‘consumer-driven nutrient recycling’. Nutrients pass back and forth between you and your food in an elegant cycle. You can’t help but to ‘eat local’, and the nutrients that you don’t absorb from your food go straight back into the ecosystem to fertilize your food. This means that when you and your offspring eat food faster than it can grow, you starve and die. Alternatively, if you don’t eat enough, the food that’s growing around you becomes depleted in nutrients, and that’s not good for you, or the other grazers in the ecosystem that depend on the same food, either. If this parasite alters the way you eat and excrete nutrients, it could affect the entire ecosystem by shifting the nutrient content of primary producers.

Experimental evidence indicates that parasites do alter your relationship with food. Experiments have shown that Daphnia eat less, reproduce less, and excrete more nutrients like nitrogen (N) and phosphorus (P) when they’re infected. But do these shifts translate into real world changes to your ecosystem? And, if so, can these changes make you even sicker or, worse yet, alter your ability to drive nutrient recycling?

According to this new study in the Journal of Animal Ecology, they might. Narr and colleagues sampled rock pools on skerry islands in the Baltic Sea near the Tvärminne Zoological Station.  They quantified the relationship between the prevalence of a microsporidian parasite and the density and nutrient content of its host (Daphnia) and the diet of its host (algae). They also set up a mesocosm experiment to see how increasing the nutrient content (reducing the N:P ratio) of algae affected infected Daphnia populations and the population of the parasite.

Rockpools

Rock Pools on Skerry islands in the Baltic Sea. Dieter Ebert has been studying 100s of populations of Daphnia and their parasites in these pools for decades. Nitrogen and phosphorus concentrations in pools vary based on proximity to the sea and inputs from biotic sources like bird poop. The consequences of these inputs are apparent in the pictures above with some pools exhibiting very high levels of primary production (Left) and others nearly oligotrophic (Right).

As it turns out, algae in rock pools with a higher prevalence of infected Daphnia are depleted in nutrients (have higher N:P ratios) relative to those with a lower prevalence of infection. It’s unclear if this relationship is driven by parasite-induced shifts in consumer-driven nutrient recycling or effects of diet quality on host (and parasite) ingestion rates, but the authors make the case that it could be both. The trends in the field are consistent with parasite-induced shifts in consumer-driven nutrient recycling observed in the lab, but the mesocosm experiment showed that P additions reduce the parasite loads of individual Daphnia.

Mesocosm experiment

Narr and colleagues set up a mesocosm experiment on one of the skerry islands near the Tvärminne Zoological Station in the Baltic Sea. They added phosphorus to infected Daphnia populations in buckets to create ambient, moderate, and high N:P ratios, and then measured the growth of the populations over 56 days and spore loads of individual adult Daphnia at the end of the experiment.

So, there you are, a sick Daphnia with diminished offspring counts. Do you need to worry that your diminished appetite is making you sicker or ruining your ecosystem? That depends on the parasite infecting you and the specific nutrients humans are adding to your ecosystem (read the paper for more details). But it might be time accept that nutrient cycles don’t always revolve around your nutritional needs. Parasites can drive nutrient recycling too.

More Info:

Narr et al. (2019) Nutrient availability affects the prevalence of a microsporidian parasite. Journal of Animal Ecology. doi: 10.1111/1365-2656.12945

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

/ Sarah Marley / Leave a comment

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.

DSC_1126

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.

gyro

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

Frogs and Herbicides: A Gut Feeling

/ Sarah Marley / Leave a comment

Dr. Sarah Knutie led a study to explore whether a commonly-used herbicide affects the gut microbes of frogs and if the gut microbes could mediate the effect of the herbicide on infection risk by the amphibian chytrid fungus. She conducted the work as a Post-doctoral Researcher at the University of South Florida and is currently an Assistant Professor at the University of Connecticut. Here, she shares her #StoryBehindThePaper for: “Do host-associated gut microbiota mediate the effect of an herbicide on disease risk in frogs?”

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Cuban tree frog adult (Photo credit: Jeremy Cohen)

When I started my post-doctoral position at the University of South Florida in Jason Rohr’s lab, I had never worked with frogs, gut microbes, or skin pathogens, which are all the focus of my recent paper in Journal of Animal Ecology. Most of my past research explored the effects of novel parasitic nest flies on birds in the Galapagos Islands. However, I had a keen interest in understanding what factors affect animals’ ability to defend themselves against parasites. With all the new and exciting research on animal microbiomes and the need to understand what factors affect the decline in amphibians, I decided to start my new research program by exploring how gut microbes affect disease ecology in frogs.

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Cuban tree frog adult (Photo credit: Jeremy Cohen)

I assembled an amazing team of undergraduate researchers and we looked at how early-life gut microbes affected later-life resistance to parasitic gut worms. This project started as a test of methods study but turned into ground breaking work, which was published last year in Nature Communications. We found that a disruption in the gut microbes of tadpoles increased infection risk in adult frogs, which had not been demonstrated previously. Furthermore, we suspected that a reduction in the diversity of gut microbes and abundance of bacteria from the phylum Fusobacteria in tadpoles could be responsible for this change in infection risk.

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Left: Former undergraduate researchers from the University of South Florida that participated in the study. Right: Former undergrad Sahara Peters with the experimental frogs.

In the Nature Communications study, we used sterilized pond water to disrupt the gut microbes, which is not a natural disruptor in the environment. Therefore, we wanted to test whether “real-world” environmental insults, such as pesticides, would disrupt the gut microbes of frogs and if the gut microbes could be mediating the effect of the pesticides on infection risk. And thus began the conception of the study published in Journal of Animal Ecology; I was also honored to receive a British Ecological Society Large Research Grant for this study.

tadpole

The two main questions from the Journal of Animal Ecology paper were: 1) does atrazine affect gut microbes of Cuban tree frogs? and 2) does this atrazine-related change in gut microbes relate to higher infection risk by the amphibian chytrid fungus? We designed an experiment in the laboratory with captive Cuban tree frogs. We decided to work with the herbicide atrazine for the study because recent work suggests that tadpoles exposed to atrazine have a higher risk of chytrid-related disease later in life. Additionally, chytrid is an important pathogen because it has contributed, in part, to the global decline of amphibians, which are the most threatened class of vertebrates in the world.

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Graphical abstract for Knutie et al. (2017)

For the main experiment, we exposed tadpoles to atrazine or not then either infected them with chytrid or allowed them to metamorphose (become terrestrial) and infected them with chytrid as adults. We then characterized the gut microbes and quantified infection intensity of chytrid. The main finding was that atrazine did not affect the gut microbes of frogs and that the gut microbes did not mediate the early-life effects of atrazine on later-life disease risk. However, we did find that the gut microbe community in tadpoles predicted infection risk in adult frogs: 1) higher diversity of microbes in tadpoles related to lower infection intensity in adults, and 2) higher relative abundance of bacteria from the phylum Fusobacteria resulted in lower infection intensity in adults. We found no relationship between the gut microbe community and infection risk at the time of infection at either life stage (i.e., tadpole gut microbes did not affect infection risk of tadpoles).

These results were exciting because they corroborate our results from the Nature Communications paper but also show that the early-life gut microbes can affect later-life susceptibility to a skin pathogen. In other words, the gut microbes could be affecting the development of the immune system in a way that not only affects gut parasites, but skin parasites as well! Additionally, the results suggest that bacteria from the phylum Fusobacteria might be important in the development of the immune system, so increasing relative abundances of Fusobacteria might have lasting positive effects on amphibian health.

Although we did not find that gut microbes mediate the effect of atrazine on infection risk in this Journal of Animal Ecology study, we have exciting preliminary results to suggest that this is not the story for all other pesticides. Stay tuned for future papers from my lab group at the University of Connecticut.

SarahKnutie

Sarah Knutie with a Cuban Tree Frog (Photo credit: Laura Domine)

More Info:

Knutie, S. A., Gabor, C., Kohl, K. D., & Rohr, J. R. (2018). Do host-associated gut microbiota mediate the effect of an herbicide on disease risk in frogs? Journal of Animal Ecology, 87: 489-499.

Knutie, S. A., Wilkinson, C. L., Kohl, K. D., & Rohr J. R. (2017). Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nature Communications, 8: 86.