The Amazing Stinkbird

The hoatzin is an amazing bird. Look at it:

It’s awesome. The hoatzin is the only bird in the family Opisthocomidae and its taxonomic position amongst other birds is unresolved. It’s a weak flier and it smells bad (think cow manure) and both of these traits are due to the awesomest thing about the hoatzin: it’s a foregut fermenter.

The hoatzin has an enlarged crop for the purpose of fermentation (see figure below). A “crop” is an anatomical structure in throat of some animals (including most birds) that primarily stores food. In the hoatzin, however, it does much, much more. Foregut fermentation is a digestive strategy where microbes living in or before the stomach break down vegetation for their host. Microbes are required by foregut fermenters because only the microbes are capable of breaking down the cell wall of plants, a barrier that confines most of the nutrients found in plant cells. The hoatzin is the only bird to use foregut fermentation and is the smallest known foregut fermenter. It’s a weak flier because of the anatomical accommodations the enlarged crop requires. And it stinks because fermentation is an odoriferous process. (The bright side to being the Stinkbird is that the hoatzin is not eaten by humans and this probably contributes to the fact it is NOT endangered!)

Figure 1 from Godoy-Vitorino (2008); "Bacterial community in the crop of the Hoatzin, a Neotropical folivorous flying bird"

Figure 1 from Godoy-Vitorino (2008); "Bacterial community in the crop of the Hoatzin, a Neotropical folivorous flying bird"

And this brings us to today’s paper. Previous work from the Dominguez-Bello research group has characterized the crop microbiota (and by that I mean, sequenced the DNA of and taxonomically identified the bacterial species present). The goal of the current study was to compare the microbiota at a population level. Godoy-Vitorino et al. (2012) sampled three birds at two populations in Venezuela roughly 500km apart (6 birds total). At each site, they performed vegetation surveys (to identify potential food sources) and recorded about 30 hours of hoatzin foraging behavior. To compare the microbial communities, Godoy-Vitorino et al. used a PhyloChip – a microarray specifically for identifying bacterial species in a complex sample.

SIDE NOTE ON MICROARRAYS: A microarray is basically a chip that has probes of known DNA sequence printed on it. You can then douse the chip with a DNA sample, induce the sample-sequences to bind to the matching chip-sequence, then visualize which sequences have found a match. It’s a really useful tool for quick characterization of a DNA sample (given you know enough about what you’re working with to make the chip in the first place).

The cartoon at the left is how I think of microarrays: Columns represent unique sequences that were printed to the chip 10 times each. We hybridize red and blue samples to the chips and then compare how many matched probes there are from each sample. In this imaginary example, we see A and J are way higher for the red sample and F is way higher for the blue sample. From this “data”, we can reasonably conclude that something about sequences A, F and J may be important for the differences found between the red and blue samples.

The microarray data from the 6 hoatzins identified 42 bacterial phyla (as a reference ALL vertebrates and some invertebrates belong to one phylum, the Chordata). A total of 1639 taxa were detected and of these, 60 differed significantly between the two populations. Additionally, almost half of the bacterial taxa were found in at least 4 of the 6 birds. It seems intuitive that all the hoatzins MUST share SOME bacterial species, but the concept of a “core” microbiome as an inherent property of a species is complex. For example, it might be that the “core” is actually an important set of functions instead of species. That’s a whole other topic though. The main result from the paper is that the crop microbiota of birds from a given population were more similar to each other than to the other population.

So riddle me this: WHY are these two populations, separated by only 500km (or ~310 miles), distinct? The authors show that the diets of the two populations are slightly different and they focus on diet as the main explanatory factor for the composition of crop bacterial communities. And maybe that’s 100% correct. But the birds within each population are probably closer genetic relatives to each other than to the other population. Could host genetics play a role in shaping the crop microbiota? Or how about nesting material composition? The immediate environment after birth could have a significant effect on microbial composition. Or what if it’s even more complicated – like crop microbiota is affected by the microbes found on the feathers of its parents and feather microbiota is governed by how big the parents home territory is? Maybe? OK – probably not.

Back to the point: The microbial communities found on or in host organisms are super important and super complex (for a refresher, see my first post about microbiota affecting mate choice in flies). My dissertation is about understanding some of the ecological and evolutionary factors that govern microbiota assembly and determining what, if anything, we can learn about a host based on its microbes. This study shows that populations have distinct microbial communities –that’s an important first step when trying to understand what differentiates groups, both within and across species. The underlying reasons are the next step.

PS –  baby hoatzins have claws on their wing digits! How cool is that?

Godoy-Vitorino F., Leal S.J., Díaz W.A., Rosales J., Goldfarb K.C., García-Amado M.A., Michelangeli F., Brodie E.L., Domínguez-Bello M.G. (2012) Differences in crop bacterial community structure between hoatzins from different geographical locations. Research in Microbiology:1-10. DOI: 10.1016/j.resmic.2012.01.001.

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6 comments on “The Amazing Stinkbird

  1. kstagaman says:

    Very cool paper. I’m also studying microbiota assembly, but in zebrafish. I find it odd that they decided to use a microarray for looking at microbiota composition when, as far as I can tell, the standard methods have become high-throughput sequencing. Think of the things they could be missing! Also, only three birds from each population is a really small number. If we’ve learned anything from human and mouse studies, it’s the the microbiota composition can be wildly different between people even in similar environments. The differences found here might just be a result of sampling error. Also, I wonder if the stink birds feed their young in a similar fashion to other birds, i.e. regurgitation. If that’s the case, then there may be a lot of vertical transmission of microbes directly from crop to crop, which could cause differentiation between the populations due to either selection or just drift.

  2. Ah, kstagaman (Keaton? Hi!) beat me to the punch on the mode of parent-offspring transmission. BUT! I can add that, if it’s true, it suggests a way to test for effects of host genetics on the biota: use crop contents from parents at one site to feed chicks from another, and see if the “foreign” biota takes hold. Using, I don’t know, a turkey baster? Hoatzins would totally hold still for that, right?

  3. Hird says:

    @kstagaman – i agree that next-gen sequencing seems like the norm these days, but i actually liked that they used a microarray. i think it allows them to standardize the results: if a sequence is missing from an NGS experiment, you’re not sure if it’s actually not in the environment or if it was missed by the method. with the microarray, it’s looking for specific things, so if it’s there, it’s there and if not, it’s more likely because it is actually missing from the sample. also, hoatzins do regurgitate food to their young – my guess is that vertical transmission is almost certainly happening in this way. that’s part of what i was trying to get at by saying that the underlying reasons for the differentiation is the next step. there are so many questions here!

    @Jeremy – definitely a cool idea. some similar-ish experiments have been done in other organisms but i don’t think there’s an emergent clear answer. for example, in one study, blue tits and great tits were switched and raised by different parents – they found parenting/nesting environment/diet controlled microbial assemblages. researchers have also transplanted whole gut contents into germ-free mice and the “foreign” microbiota totally took hold.
    i think another cool experiment (in a magic land where we can do anything) would be to do that sort of transplant/turkey baster experiment and then figure out if the “mismatched” hoatzins are somehow less fit than the others. would coevolution be an appropriate word to use then?

    Lucas F.S., Heeb P. (2005) Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings. Journal of Avian Biology 36:510-516.

    • Yoder says:

      @Sarah, finding a fitness cost to establishing a “foreign” gut microbiota would be hella cool. Whether it’d be coevolution is an interesting question. I want to say yes, but in some sense it’d be like arguing that a herbivore is “coevolving” with the plant community in which it lives–if the herbivore could also change the plant community in which it lives …

      There’s only one way to settle this. All we need is a turkey baster, a couple dozen hoatzins, and some next-gen sequencing capacity.

      • Hird says:

        shoot! i have 10 pregnant hoatzins and an illumina hi-seq at my house, but no turkey baster. too bad…

    • kstagaman says:

      @Jeremy – yes, it’s me, Keaton, the one and only!

      @Sarah – I agree being able to standardize is a good argument for using the microarray, if you’re not interested in finding things we are not yet familiar with.
      I assume when you’re mentioned the researchers transplanting whole gut contents into germ-free mice and “foreign” microbiota taking hold that you’re referring to the “humanized” mice from Jeff Gordon’s lab. This research is pretty awesome (though there are some skeptics out there that wonder how “humanized” the mice really are). But, if one takes community structure into account (i.e. more than presence absence), the issue is more complicated. In 2006, John F. Rawls at UNC Chapel Hill transplanted microbiotas from CONV mice to GF zebrafish and from CONV zebrafish to GF mice, and found that, “The transplanted community resembles its community of origin in terms of the lineages present, but the relative abundance of the lineages changes to resemble the normal gut microbial community composition of the recipient host.”

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