Influenza may be in evolutionary stasis in its natural reservoir after all

An objection often raised against the thesis of the genetic entropy of the H1N1 virus is that such a thing is impossible because the virus has existed in its natural reservoir for too long. To counter this objection, Carter and Sanford have suggested That natural reservoir most likely involves a very quiescent viral state, as might occur within a host where there is very little replication, and hence much lower mutation rates
Several people on this site, especially @RonSewell, have categorically rejected this possibility, considering it perfectly disconnected from reality. And yet, while exploring the literature on this issue, I came across 2 articles that support C&S’s conjecture that Influenza is indeed in evolutionary stasis in aquatic birds, its natural reservoir!
https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2001.0997

Thank you for starting this thread; I think that this is indeed a logically inconsistent Achilles heel to Sanford’s ideas, and therefore the concept of preserved viral genomes warrants focused discussion. I do not have time today to much engage, but when I can get back will be arguing both that the life cycle of influenza does not support the idea of stasis, and that the observed extent of variation actually found in natural reservoirs is incompatible with preservation of idealized viral types over millennia.

Could you cite and quote the specific bits that support Sanford’s ideas? It would save time for all of us.

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Gil, neither “asymptomatic” nor “persistent” are the same as “very little replication” in virology. Your claim is extremely disconnected from reality.

From the abstract of the first article:
« In the aquatic birds, influenza is asymptomatic, and the viruses are in evolutionary stasis »

And here is a relevant quote from the second article:
«We now present examples that argue that these acute epidemic agents originate from persistent infections of other hosts.
Influenza A is a strictly acute human virus which does not establish persistence and displays a high genetic variability in order to continually infect human popula-tions that would otherwise have acquired herd antiviral immunity. Yet as noted by Webster et al.(1993), all 14 HAsubtypes of influenza A appear to have originated follow-ing adaptation of a virus that infects aquatic bird popu-lations. In contrast to human infection, infection of waterfowl results in a persistent and generally inappar-ent infection in the gut. This persistent virus maintains a surprising level of genetic homogeneity with few changes having been recorded in the past 67 years. Thus, it is likely that acute human influenza A represents a host species jump of a persisting viral agent of aquatic birds »

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Neither “persistent” nor “asymptomatic” nor “evolutionary stasis” mean “very little replication” and/or “much lower mutation rates.” That’s the problem with scanning for words instead of examining evidence.

And aren’t C&S admitting that genetic entropy isn’t true with this gambit? How can a genome be in a death spiral if the species is in stasis?

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The whole point is that Influenza viruses seem to be in relative stasis in their natural reservoirs, where they have adopted a persistent life strategy that protects them from rapid degeneration due to genetic entropy. But as they jump to other hosts, they can shift to an acute life strategy that expose them more readily to genetic entropy. This is what C&S have reported for the H1N1 outbreaks in human.

Neither stasis nor persistence mean that genomes have stopped replicating and mutations have stopped occurring, Gil. If genetic entropy had any basis in reality, this is where it would be occurring.

They have reported nothing of the sort.

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Have they stopped mutating when they replicate in these hosts, or are they just not under the constant pressure of an evolutionary arms-race against the the host immune system?

Also, if the virus is constantly re-emerging with the capacity to re-infect a host that has evolved immunity against the previous infection, doesn’t that imply it’s also evolving in it’s “natural reservoir”? Otherwise one has to wonder how it gains the ability to infect the host anew.

And on a related note, just how does it acquire this ability to cross from one species to another in the first place? The ability to cross over into another species and colonize a new ecology seems like a gain of phenotypic function to me.

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Influenza is an RNA virus. Viral RNA is quickly chewed up in the cell, so the only way for an RNA virus to exist is to replicate. On top of that, infections only last a few days to two weeks. This means the virus must constantly find a new host. If an RNA virus stops replicating it ceases to exist quite quickly.

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The life strategy of influenza viruses seems to be different in their natural reservoirs than in other hosts such as humans, passing from a persistent state in the former to an acute state in the latter. Your description above pertains to the acute state, not the persistent one. See table 1 of the Minireview by Villarreal & al I referenced in the initial post of this thread.

Sure, but in order to persist, an RNA virus has to either replicate, or reverse-transcribe to DNA.

Influenza doesn’t reverse-transcribe as part of it’s life-cycle (it is not a retrovirus). It carries it’s own RNA-dependent RNA polymerase so it can replicate it’s RNA genome. It doesn’t integrate in the host nuclear genome as part of it’s natural life-cycle, and so never becomes dormant.
It may be able to escape the immune-system (and the associated arms race selective pressure this entails) in certain reservoir species by continuously infecting and replicating in some restricted physiological setting such as the lower intestine of waterfowl. But then it still replicates and evolves there. You appear to have confused the idea of persistent infection strategy with a kind of near-total dormancy where effectively nothing happens.
While dormancy is one way in which some viruses can persist for very long periods of time almost genetically unaltered, Influenza is not among them.

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This paper begs to disagree.

Influenza A viruses from wild aquatic birds, their natural reservoir species, are thought to have reached a form of stasis, characterized by low rates of evolutionary change. We tested this hypothesis by estimating rates of nucleotide substitution in a diverse array of avian influenza viruses (AIV) and allowing for rate variation among lineages. The rates observed were extremely high, at >10−3 substitutions per site, per year, with little difference among wild and domestic host species or viral subtypes and were similar to those seen in mammalian influenza A viruses. Influenza A virus therefore exhibits rapid evolutionary dynamics across its host range, consistent with a high background mutation rate and rapid replication.

the most notable aspect of these results was that the substitution rates estimated for AIV were very high, ranging from 1.8 to 8.4 × 10−3 substitutions per site, per year (subs/site/year). These rates are similar to those previously estimated in human (5.7 × 10−3 subs/site/year in the HA1 domain; Fitch et al. 1997), equine (5.4 × 10−4 and 5.1 × 10−4 subs/site/year for the M and NS genes, respectively; Lindstrom et al. 1998), and swine (1.30 × 10−3 subs/site/year for the M gene; Lindstrom et al. 1998) influenza viruses and therefore indicate that AIV does not evolve anomalously slowly.

The overall picture that arises from our analysis is that rather than forming a static gene pool, the evolution of AIV in all subtypes and species is characterized by the rapid accumulation of mutations, including those at nonsynonymous sites, typical of RNA viruses in general. Far from being in evolutionary stasis, AIV therefore evolves at a rate, >1 × 10−3 substitutions per site, per year, that is comparable to that seen in other RNA viruses (Jenkins et al. 2002; Hanada et al. 2004), including those influenza A viruses isolated from mammals. Further, there is relatively little difference in substitution rates among genes or serotypes, indicating that their intrinsic dynamics of mutation and replication are similar among all species infected. That overall selection pressures are similar in the influenza A viruses sampled from birds and mammals also reveals that the former have not yet reached a global fitness peak characterized by little amino acid fixation.

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The paper you cite by Chen & Holmes was published in 2006. The same group published a new article in 2015 that acknowledges evolutionary stasis of influenza in wild birds, it’s natural reservoir !

Abstract

Background

Wild birds are the major reservoir hosts for influenza A viruses, occasionally transmitting to other species such as domesticated poultry. Despite an abundance of genomic data from avian influenza virus (AIV), little is known about whether AIV evolves differently in wild birds and poultry, although this is critical to revealing the dynamics and time-scale of viral evolution. In particular, because environmental (water-borne) transmission is more common in wild birds, which may reduce the number of replications per unit time, it is possible that evolutionary rates are systematically lower in wild birds than in poultry.

Results

We estimated rates of nucleotide substitution in two AIV subtypes that are strongly associated with infections in wild birds – H4 and H6 – and compared these to rates in the H5N1 subtype that has circulated in poultry for almost two decades. Our analyses of three internal genes confirm that H4 and H6 viruses are evolving significantly more slowly than H5N1 viruses, suggesting that evolutionary rates of AIV are reduced in wild birds. This result was verified by the analysis of a poultry-associated H6 lineage that exhibited a markedly higher substitution rate than those H6 viruses circulating in wild birds. Interestingly, we also observed a significant difference in evolutionary rate between H4 and H6, despite frequent reassortment rate among them.

Conclusions

AIV experiences markedly different evolutionary dynamics between wild birds and poultry. These results suggest that rate heterogeneity among viral subtypes and ecological groupings should be taken into account when estimating evolutionary rates and divergence times.

A question that has been less frequently addressed is whether evolutionary patterns and processes also differ between wild birds and poultry? Indeed, there are a number of factors that could create important evolutionary differences between AIV in wild birds and poultry, notably reflecting differences in the mode of transmission and population structure. In particular, the transmission of AIV between wild birds largely occurs through an indirect faecal-oral route, in which, following excretion, the virus sits in an aquatic environment before infecting another host [2,7,8]. Importantly, there is growing evidence that AIV is able to remain in these water environments for several weeks, although this is dependent on the physico-chemical characteristics of the water source in question, and the presence of microorganisms which limit AIV infectiousness [7-11]. Critically, while present in the environment, AIV will effectively be in a “latent” state, such that there will be no viral replication and no mutational accumulation.

Conclusions

The estimates of nucleotide substitution rate presented here reveal a more complex picture of the evolutionary processes driving the evolution of avian influenza virus than previously thought. Most notably, it is clear that a single substitution rate cannot be applied to wild birds and poultry equally, as the evolutionary rates are consistently lower in the former and which may reflect a greater role for environmental transmission. Hence, it is evidently incorrect to impose a single substitution to AIV sampled from hosts as diverse as wild birds and poultry, and that molecular clock estimates based on a single rate may be erroneous. Similarly, rates differ significantly between the strict and relaxed clock models. It is therefore likely that the evolutionary dynamics of avian influenza virus can only be captured by new models that allow rates to vary in a more complex manner along lineages and which reflect changes in the underlying ecology.

The trick seems to be that influenza viruses can persist in abiotic form in the environment of wild birds, especially in water.

For up to a few weeks, depending on how favorable the conditions are. I don’t see how that helps your case.

No, for up to thousands of years! And this helps my case a lot!

In practice, any duration of a genetic conservation (nonreplicative) phase can be attributed to preservation in environmental ice (particularly that global temperatures heighten). For instance, if a gene of an avian strain isolated in a certain year exhibits maximal nucleotide sequence homology to a gene of an avian strain isolated 30 years earlier, while the degree of homology arithmetically reflects mutational stasis of 10 years, it means that this gene was preserved in environmental ice for 10 years in total, either continuously or discontinuously, during those 30 years. Basically, the genetic conservation phase may last for thousands of years, and one can assume that such a frozen genetic inventory includes certain portions indicating the historical genomic evolution of IAVs, whether in the form of genetic material or viable virions.

Genetically, since influenza gene pool harbored by avian hosts includes human and porcine genes [80–82], the proposed cryobiological apparatus principally allows for such genes as well to undergo the same course and thereafter be contracted by aquatic birds and conveyed onto poultry and pig farms. Intact avian influenza genomes too are most probably prone to resurface and recirculate in that fashion. Perennial preservation in ice may basically last for few up to thousands of years and can thus significantly affect evolutionary, epizootical, and pandemic mechanisms.

Now that is certainly better evidence for the possibility of longer periods of stasis of Influenza A viruses in nature, I have to agree. I also found this article that appears to support a similar phenomenon, though on a shorter timescale:

But it does raise a question about the relative frequency with which different influenza A strains re-emerge after longer periods preserved in frozen waters, and to what extend such phenomena contributes to the evolution of influenza A virus in nature. What is it’s magnitude of influence? How often does it preserve and re-emerge after being frozen for a literal thousand years, compared to seasonal(yearly) or perhaps decade-long periods of dormancy?
We need to know more than mere possibility.

Neither “persistent” nor “evolutionary stasis” mean “non-replicating” or “non-mutating,” Gil. Please stop employing this fallacy of equivocation.

Evolutionary stasis, in fact, contradicts genetic entropy.

No, it doesn’t! A virus being preserved in ice has nothing to do with genetic entropy!

And this abstract


Collectively, our results support surface waters of northern wetlands as a biologically important medium in which IAVs may be both transmitted and maintained, potentially serving as an environmental reservoir for infectious IAVs during the overwintering period of migratory birds.

Influenza A viruses remain infectious for more than seven months in northern wetlands of North America (2020)

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