Host genetic variation shapes distribution of virus diversity in nature

Plants can be infected by multiple viruses at the same time. The composition of the pathogen community varies between individuals of the same species, even within the same population. Ecologists at the University of Helsinki and Zurich have now shown that these differences are primarily due to the genetic variation among the hosts. This strongly suggests that the loss of genetic diversity could render species more vulnerable to infections and extinction.

Viruses are ubiquitous across plant and animal kingdoms – but most of them are still unknown to science. Only recently scientists have developed improved analysis techniques and statistical tools to investigate one of the key questions: Why are some individuals more susceptible to viruses, while others remain unharmed?

Combination of pathogens is important

It is already known that genetic differences can make animals or plants more resistant against a specific virus. However, it is becoming increasingly clear that most organisms do harbour not only one kind of pathogen but complex communities composed of different microbes. "Accounting for this diversity of infection is necessary to understand and predict disease dynamics and costs of infection for the host," says Professor Anna-Liisa Laine. For example, the first arriving pathogen could confer resistance to second pathogen. But so far, little is known about the factors that shape the composition of the virus communities.

With her research team located in both Zurich and at University of Helsinki, Laine has now shown that genetic differences have a major impact on the diversity of the virus community each individual supports. "This suggests that depletion of genetic diversity within a species can have significant consequences for the risk of virus infection," says Laine. This research is supported by European Research Council (ERC) funding awarded to Laine to investigate how host resistance functions and evolves under diverse virus attack.

Identical plants in different environments

For their study the team used the common weed Plantago lanceolata, also known as ribwort plantain. Individuals of this plant can be cloned by propagation of the roots – resulting in genetically identical offspring. With this method the researchers generated 80 clones from each of four different genetic variants of ribwort plantain and placed them among populations of naturally occurring ribwort plantain at four locations in the Åland archipelago in the Baltic sea. Thus, the cloned plants were exposed to virus attacks under natural conditions. "By placing identical plants in different environments and keeping everything else constant, we could rigorously test the role of genetics," explains Laine.

After two and seven weeks, respectively, the researchers collected leaves and determined which of five frequently occurring plant viruses had infected the clones. They found that about two thirds of the plants were infected with at least one virus, while almost a quarter of those carried more than one virus. Altogether they found 17 different combinations, ranging from two to five viruses per plant.

Hereditary factors most significant

Sophisticated statistical modelling then allowed to tease apart how strongly the various factors − genetics, location, plant size, damages by herbivores, and interactions among the viruses – influenced the composition of the virus communities. The results revealed that host genetic differences explained most of the observed variation. "Although we had suspected that genotype would play a role, we were very surprised that it turned out to be the most important determinant," says Laine.  Also important was the local environment, whereas other factors such as plant size and herbivores showed only minor effects.

"This demonstrates for the first time that genetic differences, most likely in immunity genes, are critical for how these diverse pathogen communities assemble inside hosts," so Laine. "One of the next steps will now be the identification of the underlying genes."

Genetic diversity makes species stronger

The results highlight the importance of genetic diversity within a species. The loss of diversity makes species much more susceptible to virus infections with far-reaching consequences for biodiversity. The genetic diversity of natural populations is already being increasingly depleted due to human destruction of natural habitats. 

According to Laine the findings could also find application in agriculture to improve the pathogen resistance of crop plants: "Incorporating genetic diversity to crop systems should be embraced as a sustainable means of controlling disease in agriculture. Not only individual pests, but entire communities of pathogens."

Literature:

Suvi Sallinen, Anna Norberg, Hanna Susi and Anna-Liisa Laine. Intraspecific host variation plays a key role in virus community assembly. Nature Communications. 05 November 2020. doi:10.1038/s41467-020-19273-zDOI: https://doi.org/10.1038/s41467-020-19273-z