Creator of species: How
what lives on us and in us drives evolution.
Cover article in New Scientist: The
other you, 12 January 2013. Carrie Arnold
This is a must for all who attended John Spicers lectures on
evolutionary biology. This article touches on one of the deepest philosophical
problems that has plagued man since self-reflection became a tool available to
us, who are we? The article, by Carrie Arnold, highlights some key examples
where microbiota may be key players in the evolutionary process. Most
recognisable among these, is the holobiont hypothesis put forward by Eugene Rosenberg
for the interaction between corals and their micro-organisms. What I was
unaware of was that Rosenburg had also conducted work on fruit flies in the
field of evolutionary biology. Inspired by Rosenburgs belief that there is a
Lamarckian aspect to the hologenome hypothesis, that is, that sometimes animals
evolve via acquired characteristics, Eugene and his wife set about to find
evidence in the literature that this may be the case. The pair came across a
paper by Diane Dodd, a post Doc at the University of Yale, who found that
changing the diet of a fruit-fly could alter the flies mating choice. Rosenburg
then set Phd student Gill Sharon to work to try and replicate this
experiment. After two generations of flies
fed on molasses it was observed that they would no longer mate with flies fed
on regular starch. Next, Sharon gave flies rifampicin to kill off their gut bacteria.
Following this, the flies fed previously on starch copulated with those fed on
molasses, showing that bacteria were responsible (Dodd et al, 1989).
Another interesting study put forward as evidence for the
role of bacteria in the evolution of their larger ‘hosts’ was conducted on the
development of mice. The 2011 study suggests that mice need their gut flora for
their brains to develop normally (There was no reference for this study but I
am searching for it).There are other studies highlighted in the article, but I
don’t want to ruin it for you.
The two key players highlighted in this article are Richard
Jefferson and Eugene Rosenburg, who, as the article explains, were working individually
on the impacts of the microbiome in evolutionary biology independently until
Jefferson made contact in 2010.
The purpose of this blog was not to inform on a specific
piece of published literature, but more, to spark discussion among the members
of the blog. I have had several stimulating conversations on this topic with
members of BIOL 3309 and I encourage members to read this article (I’ll try to
upload it to the blog) and join in the discussion. I believe that the best
thing about this article is that ‘the case remains to be proven’ and I am sure that
there are good models in the marine environment to enhance the evidence for
this way of thinking. One thought I had on this subject is the implications for
laboratory cultures, for example, the pond snail, Lymnea stagnalis. It is common to feed these pond snails lettuce or
spinach during culture. Can we be sure that this alien diet is not effecting
development or behaviour of the species in some way by modifying the gut
bacteria as exemplified by Dodd et al (1989) in fruit flies? Do these snails
have microbial gut flora that is passed on purely from the parent, or is some bacteria
brought in from the environment post hatching? Will this aspect bias any
experiments, I’m not sure, but I think it highlights the message I’m trying to
get across. Also, could microbiota have enough of an impact on an organism to
be considered a functional trait when looking at the impacts functional
diversity in ecological studies? Personally, I really believe that this will be
a revolutionary, and controversial, area of research that will redefine our
thinking on how to see evolution, and ourselves.
So on that note, I leave the door open for
discussion. Do you believe we are ‘I’ or we are ‘us’?
It is interesting that although the microbes colonise in the gut, they have an effect on the brain. Presumably this is due to the production of some form of metabolite, or toxin, that can gain access via the bloodstream in order to interact with the brain more directly. As stated in the lectures, behaviour and mating choice can be affected by toxins. I wondering if this could be considered an infection, or a kind of disease, that does not result in mortalities but instead acts as a driving force for evolution.
ReplyDeleteAlso, I wonder what implications this has for organisms higher up the food web: is it possible for a toxic level to be reached through accumulation? If the microbes can continue to proliferate once in the gut, could mortality be induced in the organisms that you mentioned ingest the food types?
Matt,
ReplyDeleteGreat find!! I'm just posting a URL for the article for now, I shall ponder on this one before I engage in discussion...
http://bordensteinlab.vanderbilt.edu/picts/Hologenome.011213.pdf
Matt - great stuff - from Microbes Rule the Waves to Microbes Rule the World! there is so much evidence coming out of the Human Microbiome project now that is pointing to the impact that our resident microbes have on development and behaviour. There has been a lot of research on gnotobiotic (germ-free animals) pointing to the same thing, but now we are beginning to unravel the interactions and signalling at a molecular level. We will see this in all animal evolution and development - think this is going to be one of the BIG new areas of biology.
ReplyDeleteIn response to Megan's comment, there are indeed some examples of how the gut microbiota affects the brain. This study pack that I use with the first year students highlights some work showing how alteration of the gut microbiota (in mice) using probiotics can affect brain development and mental states like anxiety.
https://tulip.plymouth.ac.uk/Module/MBIO100/ADDITIONAL%20RESOURCES/STUDY%20TOPICS/Microbes%20and%20the%20Human%20Body.pdf [available via intranet]
Hi Matt!
ReplyDeleteIt would be interesting to get the reference for the mouse-gut-brain development paper, because I'd like to see how they tested this hypothesis. I mean, we know that the intestinal flora is important during digestion, so absence of microbes will result in poorer absorption of nutrients (rather than production of toxins as Megan suggested) and hence poor brain development, no? Similarly a ruminant without microbial flora in its gut would die because it wouldn't be able to digest cellulose. So microbes must have played an important evolutionary role that allowed the cow-ancestor to be herbivorous.
Apparently there is now way around fruit flies (perfect model organisms?), but is the mechanism of mate choice known for them? Does it work through olfactory cues?
If the bacteria are so important and possibly shape mate choice, why do we not have more examples? If we apply the Drosophila experiment, let's say, on amphipods, our hypothesis would be that amphipods fed on carrots do not mate with amphipods fed on algae (assuming the diet infuences the production of pheromones and mate choice is driven by olfactury cues in this species...). Sounds like a doable experiment ;)!
I can see how bacteria could potentially influence mate choice and allow exploitation of new resources (e.g. cellulose in ruminants), do you think they shape any other behaviours?
Microbes: the sixth sense?!
(Apologies for the lack of structure (and sense?) in this comment)
Hi,
ReplyDeleteThankyou everyone for your excellent comments. Megan, I think it is possible that continual low level exposure from bacterial toxins could drive evolutionary change. I suppose it is a disease in way, but what if it imparts adaptive advantage instead of deleterious effects?. There is good evidence of trophic transfer of bacterial toxins from shell fish to humans (Paralytic shellfish poisonig), but little is known (I think) about the chronic exposure to shellfish, that could drive evolutionary change.
Anna, I think your right about reducing bacterial levels leading to poor nutrient uptake. If this leads to decrease in the physical/behaoural state of an organism it may have suttle to changes in apperence that may deter a potential mate. There was no evidence provided for how the authers distinguished between the effects of lack of nutrients over reduction in bacterial population. It would be an interesting experiment to look at how accumulated bacterial presence/toxins infleunce mating choice and if it is related to the olfactory system. I found this review 'A review of cyanobacterial odorous and bioactive metabolites: Impacts and managment alternatives in aquaculture', that might be interesting. I think it is likley that bacteria have influence over all aspects of behavour in some way, I think, as Colin remarked, that this will be a big area of rsearch in the future.
Hi All!
DeleteHana (and Matt) – I understand that the impact on nutrition absorption varies depending the species (and possibly even strain) of microbe in question, considering the variation they cannot all induce the same result. Of course, many marine organisms have been found to rely on symbiotic relationships in order to survive, with the interactions in each case being unique.
Here’s a paper outlining the impact of microbes on the mating preference in fruit flies by another author, for those interested (although these are now not marine microbes!):
http://www.pnas.org/content/107/46/20051.full
Megan
Hi all,
ReplyDeleteI have finally had time to digest all the information in the article and think about this topic properly. In my opinion the hologenome hypothesis is an absolute sure runner and I would be very surprised if it isn’t the next BIG paradigm shift in evolution theory.
The “germ free” examples in Dr Daniel Merrifield’s lectures last week surely provide solid evidence for this. Higher organisms simply don’t exist without microbes! I think it’s fair to say that there is a great deal of work to do in this area in order to understand microbe-host interactions and the selection pressures that might act on microbe specific phenotypes.
The bottom line is selection acts on the phenotype, bugs and all. As you’ve discussed above, some examples may be extreme and cause lethal selection pressure, for example ruminants without bacteria would starve and die or the bobtail squid without its bioluminescent bacteria would be predated. Others examples might be sub-lethal, drosophila with the wrong diet and microbes won’t get to mate and pass on their genes to the next generation. The more we look for these examples the more we’ll find them. Marine biologists are going to have a crucial role to play in developing an articulate, succinct and clear explanation of this hypothesis as the most well studied examples of symbiosis are marine. Whilst the hologenome hypothesis isn’t at all restrictive to symbiotic microorganisms, it’s a good place to start. I think collaborations with behavioural ecologists would also benefit this field as in the past they have done a good job of revealing the evolutionary significance of behaviour and could lend a hand in explaining how microbes affect behaviour and so on.
It’s an exciting time to be a marine microbiologist interested in evolution!
Hi Vicky! You summarised this very nicely :)
ReplyDeleteI think the hologenome theory should also be discussed when talking about plasticity. Since plasticity is defined as "the potential for an organism to produce a range of different, relatively fit phenotypes in multiple environments", different clades of zooxannthellae, that potentially increase resistency to different temperature regimes, form a primary source for plasticity in corals. And one could discuss the costs and limits behind favouring a particular Symbiodinium clade over another. Now all we need is a good gastropod example to convince Simon about the microbial importance ;)
Hi All,
ReplyDeleteWow! It is great to see the holobiont theory getting so much coverage. Although coral biologists have been getting their heads around this for some time, I believe that the necessity of including an organism’s microbiota in any consideration of its overall phenotype is going to upset many an evolutionary apple cart!
As Vicky and Anna have pointed out, many examples of microbial symbioses that we have been introduced to over this term appear to shout out the importance of macro-micro interactions. Yet the inclusion of any microbial work in studies on the physiological evolution of metazoans seems conspicuous by its absence.
With fast and cheap next generation sequencing now possible, I wonder if surveying the microbiota of different treatment groups would actually be that difficult to integrate into evolutionary studies? Although we have a lot to learn about the function of such microbes, this seems like a good way to start investigating the microbial part of any phenotype under consideration.
Jo
Even Brian Cox is cottoning onto the hologenome theory, well as much as is reasonably possible in an hours episode on evolution ...
Deletehttp://www.bbc.co.uk/programmes/b01qrxpc
Anna, I’m sure as soon as biologist start looking they will find examples everywhere, including the mighty gastropods to keep Simon and plasticity with a look in.
Hi all, I have to agree that Dan Merrfields lectres helped to afirm the role microbes might play in evolution. I have'nt found any papers yet that make any link between what is being done with microbes in aquaculrute and its implications for evolutionary biology, has anyone else? I have found an excellent paper that highlights the intergration of microbiology and behviour in terms of evolution. It involves a baceria affecting mate choice in birds. The presence of the bacteria difines the vibrence of the colour in the male feathers. the more vibrant the feathers, the more likley the male was to reproduce. I'm sure that this must also happen in the marine environment.
DeleteHi all!
ReplyDeleteI have just found this review, recently published in PNAS:
McFall-Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H. V, Domazet-Loso, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., Hentschel, U., King, N., Kjelleberg, S., Knoll, A. H., Kremer, N., Mazmanian, S. K., Metcalf, J. L., Nealson, K., Pierce, N. E., Rawls, J. F., Reid, A., Ruby, E. G., Rumpho, M., Sanders, J. G., Tautz, D. & Wernegreen, J. J. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, early edition.
available here: http://kinglab.berkeley.edu/wp-content/uploads/2007/11/PNAS-2013-McFall-Ngai-121852511011.pdf
I strongly encourage you to read this review if you are interested in the topic. All examples discussed in this post are mentioned along with many more in various fields, as for example microbial influence in the origin of multicellularity, microbes driving radiation of several animal groups, microbes providing metabolic add-ons, microbial induction of settlement and metamorphosis of many marine invertebrate larvae,...
The authors claim that "the weight of evidence supporting this view has finally reached a tipping point" and that microbiology will present a particular challenge to the species consept, as formulated by Ernst Mayr in 1942, and to the concept that vertical transmission of genetic information is the only motor of selectable evolutionary change.
It is concluded that "because of advances describes here, we foresee a day when microbiology will be a centerpiece not only of biological research, but also of high school, undergraduate, and graduate biology education."
Interestingly they don't even use once the term hologenome theory...
Hi all sorry to join in on this discussion so late. Most has already been said but i think there is a huge potential for marine organisms to play a prominant role in this research as most of the best and most studied examples are marine. I highly recommend reading Annas review, it gives alot of great examples, this is another good review which can be couples very well to matts article..
ReplyDeletehttp://www.uni-kiel.de/zoologie/bosch/pdf/2010/fraune_bosch_bioessays_32_2010.pdf