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I've heard that there are a number of viral illnesses that humans can get from animals, which cause no symptoms in the animals. If there was such a virus in humans, which was very widespread but caused no symptoms, would we know about it?

As far as I know most pathogens have only been discovered when people were specifically looking for the cause of some disease. With bacteria, I think we know / can discover any that can be found in a human body, though we don't necessarily know what each type does. But viruses are much smaller.

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With the modern rise of meta-genomics, symptom-less viruses can be identified by the presence of their genomes. Certainly, there is more interest in pathogenic viruses than in harmless passengers, but today it's not necessary to have symptoms to identify viruses. For example:

Investigators can now go beyond pathogenic viruses and have access to the thousands of viruses that inhabit our bodies without causing clinical symptoms. By studying their interactions with each other, with other microbes, and with host genetics and immune systems, we can learn how they affect health and disease. This article reviews current knowledge of the composition and diversity of the human virome in physiologically healthy individuals. It focuses on recent results from metagenomics studies and discusses the contribution of bacteriophages and eukaryotic viruses to human health.

--Metagenomics and the Human Virome in Asymptomatic Individuals.

Even prior to metagenomics, some "silent viruses" were identified:

Viruses are the most abundant obligate intracellular entities in our body. Until recently, they were only considered to be pathogens that caused a broad array of pathologies, ranging from mild disease to deaths in the most severe cases. However, recent advances in unbiased mass sequencing techniques as well as increasing epidemiological evidence have indicated that the human body is home to diverse viral species under non-pathological conditions.

--Describing the Silent Human Virome with an Emphasis on Giant Viruses

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  • $\begingroup$ So it's not just true that we could discover such a virus, but we already have discovered many of them in humans. That's fascinating! $\endgroup$
    – KWeiss
    Commented Jan 26, 2017 at 15:16
  • $\begingroup$ It's still a very new field, and many of the newly-discovered silent viruses are bacteriophages that infect the normal gut bacteria, but there are a handful of apparently non-pathogenic viruses that infect humans. $\endgroup$
    – iayork
    Commented Jan 26, 2017 at 15:17
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    $\begingroup$ I would add that the silent virome might not have been silent upon the infection of the first animal acquiring it. $\endgroup$ Commented Jan 26, 2017 at 15:19
  • $\begingroup$ Sure, but in some cases that first acquisition may have been millions or hundreds of millions of years ago (consider spumaviruses of primates) -- so it becomes questionable if it's even the same virus, or host, as in the first acquisition. $\endgroup$
    – iayork
    Commented Jan 26, 2017 at 15:21
  • $\begingroup$ @iayork - That's exactly my point. $\endgroup$ Commented Jan 26, 2017 at 23:52
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Theoretically, I think we can. We are able to identify viruses in humans that are asymptomatic or have yet to produce symptoms (e.g. HIV, Zika Virus). However, unless this virus causes an impact on humans, like causing death in cattle, I don't see why people in our society would invest in finding out about it. Most organisations award grants for research that they could profit off in some way.

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