Why greater diversity – even of parasites – might decrease infections

Pieter T. J. Johnson, Daniel L. Preston, Jason T. Hoverman, and Bryan E. LaFonte. 2013. Host and parasite diversity jointly control disease risk in complex communities. PNAS. Early view.

(Host competence - the tendency of host species to become infected and maintain infection.)

There is often a disconnect between the reality that communities and ecosystems are diverse assemblages with numerous, often complicated and variable interactions, and ecological research, which (perhaps necessarily) focuses on interactions between at most two or three species at a time. Disease ecology similarly has often considered interactions between particular host/parasite species pairs. Some researchers have considered the diversity of host species as an important factor in explaining disease transmission and mortality, but the reality is that parasites also interact, and most hosts harbour multiple parasites. Studying disease dynamics in the context of multi-parasite, multi-host interactions is increasingly recognized as key to understanding disease transmission and severity in communities.

With this in mind, a new paper from Pieter Johnson and colleagues attempts to combine research into the effects of both parasite and host diversity on disease. Two possible hypotheses predict the effect of diversity on disease transmission: the ‘dilution effect’ suggests that the presence of multiple hosts should decrease transmission risk, if the result of additional species is a decline in community competence. It is also hypothesized, somewhat contradictorily, that increased host diversity should support a greater variety of parasites, and parasite life cycles. Both these hypotheses take a host-centric view: understanding how changes in host diversity alter disease risk also requires that we understand how changes in parasite diversity affect disease transmission.

Mutations caused by Ribeiroia infection.
From:http://www.nature.com/scitable/knowledge/library/ecological-consequences-of-parasitism-13255694

The authors looked at the contribution of host and parasite diversity to parasite transmission success using field data and laboratory experiments. First, they looked at existing data on infections of the pathogenic trematode Ribeiroia ondatrae, in amphibian species. Observations showed a positive correlation between larval trematode diversity (parasites) and the richness of free-living species (hosts). Of course the two diversities might be correlated for many unrelated reasons, like site isolation, evolutionary history, or habitat productivity. But a closer analysis showed what appeared to be an interaction between Ribeiroia infection in Pseudacris regilla (Pacific tree frog, the most common amphibian in the survey) and the total number of amphibian species at a site (figure below). Infection by Ribeiroia was highest when there was low amphibian richness and low parasite richness. It dropped significantly lower when amphibian richness was high and/or parasite richness was high.

From Johnson et al. 2013 PNAS. Results of field observations.

In addition to these observations, the authors manipulated both parasite and host species richness, first in small laboratory microcosms and then in larger and more realistic outdoor mesocosms. Results from the laboratory microcosms showed that increases in both amphibian richness (one vs. three species) and parasite richness (one vs. five species) reduced the average number of Ribeiroia in Pseudacris regilla as well as the total infection rate in the amphibian community. The mesocosms had similar results, with both host and parasite diversity negatively influencing Ribeiroia infection. In support of the generality of these results, effect sizes were comparable between the two experiments. These effects were also quite large: for example, in the mesocosm high-host, high-parasite richness treatment there were 52.4% fewer Ribeiroia per P. regilla and 38.2% fewer Ribeiroia overall compared to the low-host, low-parasite richness. Clearly multi-species interactions are crucial for understanding infection by Ribeiroia.

From Johnson et al. 2013 PNAS. Results of the microcosm and mesocosm experiments,
 showing the effects of host and parasite diversity on transmission.

The results make it clear that if you want to understand disease transmission in communities, both host and parasite diversity should be considered. To some extent, both of the initial hypotheses were supported – host and parasite diversity were correlated in the wild, but (in agreement with the dilution effect) infection rates declined as host diversity increased. One factor missing from these hypotheses is the dynamics of the parasite community: in the paper, the authors found models of transmission that included both host and parasite richness were superior. Further, past and future studies that consider only host richness may be inadvertently accounting for the effects of parasite richness on transmission as well, if those two host and parasite diversities are correlated.

There are a number of possibilities for why both host and parasite communities alter parasite transmission success. If host diversity changes the susceptibility of the community to infection (i.e. as diversity increases, the number of low competence/susceptible species increases) then low-competence hosts could act as sinks for parasite infections. Increases in parasite diversity could result in inter-parasite competition and interactions via host immunity.

One future step will be to move beyond simple measurements of species richness to understanding how species identity or characteristics are tied to the putative mechanisms. For example, how do communities of host species vary from low to high diversity sites? Do sites in fact tend to assemble with increasing numbers of low competence host species? The implications are also of interest to other types of studies of community ecology – after all, host-parasite interactions are not very different from predator-prey interactions, and similarly, despite knowing that interactions are complex and involve multiple species, we tend to focus on two or three species examples.

The demise of peer review?

Scientists are often inundated with numerous requests to submit their papers to 'open access' journals with no track record, no editor-in-chief, and dubious sounding promises. Why this explosion in dubious journals? -simple, there is money to be made. Many of these journals are scams meant to maximize profits. As it turns out, they don't even bother with peer review. In a recent, fascinating story in Science, John Bohannon sent fatally flawed bogus articles to hundreds of open access journals, with more than half being accepted with little or no peer review. This article is a must read for anyone concerned about science publishing.

Struggling (and sometimes cheating) to catch up

Scientific research is maturing in a number of developing nations, which are trying to join North American and European nations as recognized centres of research. As recent stories show, the pressure to fulfill this vision--and to publish in English-language, international journals--has led to some large-scale schemes to commit academic fraud, in addition to cases of run-of-the-mill academic dishonesty.

In China, a widely-discussed incident involved criminals with a sideline in the production of fake journal articles, and even fake versions of existing medical journals in which authors could buy slots for their articles. China has been criticized for widespread academic problems for some time, for example, 2010 the New York Times published a report suggesting academic fraud (plagiarism, falsification or fabrication) was rampant in China and would hold the country back in its goal to become an important scientific contributor. In the other recent incident, four Brazilian medical journals were caught “citation stacking”, where each journal cited the other three excessively, thus avoiding notice for obvious journal self-citation, while still increasing their journal’s impact factor. These four journals were among 14 having their impact factors suspended for a year, with other possible incidences that were flagged but could not be proven involved Italian, a Chinese, and a Swiss journal.

There are some important facts that might provide context to these outbreaks of cheating. Both Brazil and China are nations where to be a successful scientist in the national system, you need to prove that you are capable of success on the world stage. This is probably a tall order in countries where scientific research has not traditionally had an international profile and most researchers do not speak English as their first language. In particular it leads to focus on values which are comparable across the globe, such as journal impact factors, as measures of success. In China, there is great pressure to publish in journals included on the Science Citation Index (SCI), a list of leading international journals. When researcher, department, and university success is quantified with impact factors and SCI publications, it becomes a numbers game, a GDP of research. Further, bonuses for publications in high caliber journals can double a poorly-paid researcher’s salary: a 2004 survey found that for nearly half of Chinese researchers, performance based pay was 50+ percent of their income. In Brazil, the government similarly emphasizes publications in Western journals as evidence of researcher quality.

It’s easy to dismiss these problems as specific to China or Brazil, and there are some aspects of the issue that are naturally country-specific. On the other hand, if you peruse Ivan Oransky’s Retraction Watch website, you’ll notice that academic dishonesty leading to article retraction is hardly restricted to researchers from developing countries. At the moment, the leading four countries in retractions due to fraud are the US, Germany, Japan, and then China, suggesting that Western science isn’t free from guilt. But in developing nations the conditions are ripe to produce fraud. Nationalistic ambition is funnelled into pressure on national scientists to succeed on the international stage; disproportionate focus on metrics of international success; high monetary rewards to otherwise poorly paid individuals for achieving these measures of success; combined with the reality that it is particularly difficult for researchers who were educated in a less competitive scientific system and who may lack English language skills, to publish in top journals. The benefits of success for these researchers are large, but the obstacles preventing their success are also huge. Combine that with a measure of success (impact factor, h-index) that is open to being gamed, and essentially relies on honesty and shared scientific principles, and it is not surprising that system fails.

Medical research was at the heart of both of these scandals, probably because the stakes (money, prestige) are high. Fortunately (or not) for ecology and evolutionary biology, the financial incentives for fraud are rather smaller, and thus organized academic fraud is probably less common. But the ingredients that seem to lead to these issues – national pressures to succeed on the world stage and difficulty in obtaining such success; combined with reliance on susceptible metrics  – would threaten any field of science. And issues of language and culture are so rarely considered by English-language science (eg.), that it can be difficult for scientists from smaller countries to integrate into global academia. There are really two ways for the scientific community to respond to these issues of fraud and dishonesty – either treat these nations as second-class scientific citizens and assume their research may be unreliable, or else be available and willing to play an active role in their development. There are a number of ways the latter could happen. For example, some reputable national journals invite submissions from established international researchers to improve the visibility of their journals. In some nations (Portugal, Iceland, Czech Republic, etc), international scientists review funding proposals, so that an unbiased and external voice on the quality of work is provided. Indeed, the most hopeful fact is that top students from many developing nations attend graduate school in Europe and North America, and then return home with the knowledge and connections they gained. Obviously this is not a total solution, but we need to recognize fraud as problem affecting and interacting with all of academia, rather than solely an issue of a few problem nations.

Can common tradeoffs predict your supervisor’s functional type?

With Lanna Jin

If you’re a graduate student, the most important question (even more important than who you’re writing your paper with) is who is running your lab. New graduate students everywhere are settling in and getting to know their supervisors are little better. Supervisors come in all types, and hypothesizing a priori what their style is can be difficult. Fortunately, a couple of common tradeoffs underlie most functional styles...

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1)

The invisible man/woman: The ultimate laissez-faire approach. You have the freedom to choose the ideas and projects that interest you, and the responsibility to make them work. Freedom can be replaced by frustrations when you need a signature, some support, or a manuscript commented on.

El generalissimo: "Here's my idea, now go do it." These labs are usually run in a top-down manner. Day to day operations are fairly hands off though, giving you room to work through those problems on your own. El generalissimo will reward their supporters well for good work.

The coach: The coach provides you the best of both worlds: enough rope to explore your ideas, but not so much to hang yourself. They are available for troubleshooting and brainstorming, but you ultimately have responsibility for your project. But if you rely on them to much, it's going to be hard to function without them.

The micromanager: These supervisors expect regular presence, frequent meetings, records of progress, and milestones to be met promptly. If you like working from home, leaving early or starting late, or need lots of freedom to be most productive it could be a poor fit. For students who thrive on structure and prefer set goals though, this might be an ideal environment.

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2)

The skeleton: This supervisor has established themselves in their career and been active for some time, but now other interests consume them. The scientific meat that made their name seems to be gone, and all that's left is the skeleton of their earlier career. They are happy to chat with you about the many things they are interested in, but supervising your science doesn't seem to be a priority. They often see you as a person who has with non-academic interests and responsibilities, which can be a nice feeling.

The superwoman/superman: This career superstar has made their name, possibly quite early, and they are passionate about their science. This can make for an exciting and successful lab experience, as new ideas and opportunities are always on the horizon. But since they have so many demands on their time, sometimes their capes (and they) are feeling a bit ragged.

The silverback: Labs of influential individuals can be an amazing opportunity for a graduate student. Silverback experiences might be quite variable, depending on how involved they are in day to day lab activities, their travel schedules, and the size of the lab. When they are available, they have a lot to teach a student about making a successful academic career.

Bad idea: This corner of the tradeoff (low interest in science, poor establishment in the career) probably doesn't exist in tenure-track faculty. If you do manage to find such a person, run away.

The unknown: A motivated but still unestablished supervisor is a blank slate. Their early career state means that they might have time and energy to devote to you and be especially motivated to see you and the lab succeed. On the other hand, they may not yet know how to manage people and their supervisor style could morph into anything - the coach, the micromanager, el generalissimo. A bit of a gamble.