Evolutionary question regarding animal gut microbiomes

Hi all,

I am working on a large comparative dataset of gut microbiomes and I want to make a statement regarding the importance of sampling both fish gut microbiomes and mammalian gut microbiomes.
I basically want to stress the importance of sampling host taxa so distantly related but am unsure how to word it correctly. Would this be a correct statement?

Fish represent one of the most distantly related vertebrate taxa in terms of evolutionary divergence from terrestrial vertebrates, and preside in an aquatic environment that more closely resembles the environment and ecology likely inhabited by vertebrate ancestors circa 365 mya.

I also cannot seem to find any papers discussing this as it seems to be unresolved when fish and terrestrial vertebrates diverged.
Any info would be much appreciated.
Cheers,
Sam

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Goodmorning Sam,

This sounds like a cool study! Can you tell me more about the scope of the study and the major claim you are providing evidence to support?

When I read your question, my main concern was a question of timescale. :hourglass:

If I read your summary correctly, it sounds like you are using current fish as a proxy for the fish-frog-bird-mammal last common ancestor from 365 mya and that's a lot of time and evolutionary distance. Reviewer three is going to remember that. :upside_down_face:

Maybe you could focus on evolutionary pressure on host-associated aquatic microbiome being similar across time. The goal would be to sidestep issues of timescale by focusing on similar evolutionary pressure exerted on the microbiome by 1) a vertebrate host and 2) an aquatic environment at any point in time.

This really depends on the argument made in this paper. I would love to hear how other folks would answer this.

Colin

P.S. :fish: :frog: :bird: :elephant:

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Hi Colin,

Thanks for the reply.

So if I am understanding you correctly you are referring to convergence rather evolutionary conservatism? I agree that convergence between fish and mammals does seem like the simplest solution and this is actually going to be the main argument.

The main goal of the study is a comparative analysis on reef fish gut microbiomes (~500 samples, 20 species) to understand how they're shaped by host diet and host phylogeny. However, I am also comparing them to mammals and have found some striking similarities, specifically between members of the same feeding guild (herbivore vs. carnivore).

So just to clarify, you are suggesting the safest route would be to claim that the evolutionary pressure by the host and water has converged (likely for millions of years?) but whether this gives insight into our most common vertebrate ancestor is impossible to say.

My gut still tells me there is something to be said about the ubiquitous nature of the gut microbiome (especially Firmicutes) among vertebrates, but I guess when you're not working with genes its even harder to talk about evolutionary processes.

Thanks for the interesting thoughts.
Sam

Very cool!

This makes sense. I would expect feeding guild to have a strong effect, regardless of host.


I'm still trying to figure out my argument, and I'm not an evolutionary expert so I could be wrong or missing a stronger approach. My background is in high-throughput genomics with a bit of numerical ecology, so I'm trying hard to say nothing about the history at all.

Neither. Convergence is becoming more similar over time, while conservatism is staying consistent over time, and I don't know enough to claim anything about the past.

My premise is that microbiomes are shaped by selective pressure. My argument is that we can see evidence of selective pressure in communities that have converged more than you would expect by chance alone.

Well said. I guess I would frame this as 'evidence of having converged by the present day' instead of 'evidence of having converged over the course of >1m years,' if that makes sense. I am foregrounding selective pressure and it's current result, without speculating on the timescale needed to get there.

If history is a big part of your paper, you might need some historic DNA and a more qualified colleague! :joy_cat:

Well the only other advice I've gotten is "go talk to a phylogeneticist" :rofl:

So basically microbiomes don't tell us anything concretely about the past-- which I agree with. I remember I had this thought when Moeller et al. (2014) came out trying to show "rapid changes in the gut microbiome during human evolution" which I thought was kind of a stretch.

And yes I would love to conduct a study on preserved fecal/gut samples from museums to see how stable gut microbiomes have been over time. One can only dream.
Thanks again for the thoughts. The selective pressures way of thinking is makes more sense than trying to grasp at evolutionary stories that may or may not be true.
Sam

Thanks for the great discussion, Sam! I think we have reached a consensus, and you summed it up really well.

If you want to focus the investigation on selective pressure, these papers show how to use phylogeny to show evidence selective pressure working to shape a ecological community.

https://www.nature.com/articles/ismej201330

https://www.nature.com/articles/s41396-019-0396-x

The core idea is to compare the phylogenic composition of taxa against a random one, and if the taxa are pulled closer together or pushed further apart, then this provides evidence that there is selective pressure pulling or pushing on these clades.

Very cool. So almost like a co-occurrence analysis with phylogeny involved. Thanks for this. I'll let you know if end up applying this to my dataset. Would be interesting to see if similar patterns hold up in fish guts.

Cool, cool :sunglasses:

Full disclosure, I contributed to that last paper. Here's the code for calculating beta NTI / betaMNTD and the code for doing the regression analysis against other taxa or environment variables.

Here's how I described the method three years ago:

A positive slope (high abundance with high betaNTI), means that the microbe is most successful in a stochastic, high turnover environment. A negative slope (high abundance with negative betaNTI), means that the microbe is most successful in a stable environment with low turnover.

You can also look for selective pressure associated with environmental variables, like time.


The samples start with random selective pressure near day zero, and shift to
strong, homogenous selection by day 80.

Very interesting. I'll definitely try this out (when I get some extra time :sweat_smile:). But I am very curious how applying this model to a large comparative analysis might reveal some interesting patterns of phylosymbiosis and diet etc.
Thanks for the code!

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