Pssst. Your holobiont is showing.

Here’s a sad story: Species A mates with Species B. They succeed in making a Hybrid Baby but their Hybrid Baby dies before it can fully develop. (I warned you it was sad.) Why did that happen? Sure, sometimes two genomes are just too different to successfully coexist – both the stars and the chromosomes must align to make a baby. Other times, as recently reported by Brucker and Bordenstein, the Hybrid Baby’s microbiota is the problem.

I think (or rather Google thinks) this is a Nasonia wasp.

In Nasonia wasps, there are three closely related species that all diverged less than one million years ago: Nasonia vitripennis (who I’m going to refer to as the V wasp), N. giraulti (the G wasp) and N. longicornis (the L wasp). When L and G mate and their LG offspring are mated to other LG offspring, 8% of the males die. When V and G mate and their VG offspring are mated to other VG offspring, 90% of the males die.

The phylogeny of the three Nasonia wasps (left) and the crosses that result in hybrid male lethality.

The phylogeny of the three Nasonia wasps (left) and the crosses that result in hybrid male lethality.

Brucker and Bordenstein hypothesized that microbes were responsible for the hybrid lethality of the the VG hybrids. Through DNA sequencing, they found that the gut microbes of the VGxVG wasps were unlike either parental type (in abundance or diversity), whereas the LGxLG wasps were. So, when a hybrid’s gut microbiota is like one of the parental species, the hybrid males live. When the gut microbiota is unlike a parent, the hybrid males die. They further found this could be boiled down to a change in the single dominant species: whereas a Providencia bacterium was most abundant in both V and G parents, a Proteus bacterium was most abundant in VGxVG wasps.

But that doesn’t conclusively show that microbes are responsible for the hybrid lethality. Brucker and Bordenstein then compare germ-free hyrbids to conventional hybrids – in other words, if we remove the germs (the microbiota, that is), do the hybrids still die? The short answer is no. Under normal conditions, about 80% of the pure Vs and pure Gs survive, whereas only 10% of the VGxVGs survive. Under the germ-free conditions, about 70% of the pure Vs and pure Gs survive and 60% of the VGxVGs survive. That’s a pretty significant increase in living hybrids! And to strengthen the case even more – when the germ-free wasps were fed a mixture of Providencia and Proteus bacteria, the hybrid survival rates went down to about 30%.

The authors perform other experiments for this study that include analysis of wasp genomic loci that were previously linked to hybrid lethality and a transcriptomic analysis, where they find immune genes to be a significant player. However, I’m going to switch gears a little bit and talk about the context the authors frame their discoveries in: the HOLOGENOME concept.

Most evolutionary biologists probably consider the individual as the fundamental unit of natural selection. We think about the genes of one mother or one father being passed on to one descendant. But is this view too constrained? The “hologenome” is all the genomes that belong to the “holobiont” – an organism and all its microbes. The Hologenome Theory of Evolution posits that the holobiont is the fundamental unit of natural selection, not just “the big organism”. Generally speaking, this makes a lot of intuitive sense, I think: we macros are pretty dependent on micros to get our genes to the next generation. But is the reverse true? To be THE fundamental unit of selection, the holobiont must pass its hologenome to its offspring – and I’m not sure this assumption universally holds. Certainly some macro-organisms always pass specific micro-organisms to their offspring (coprophagy in mammals might be a good example). But in most cases, where our microorganisms come from is a mix of vertical transmission (from our parents) and horizontal transmission (from the environment). I just can’t make this distinction make sense with what I think I know about heredity and selection. Natural selection depends on traits that make an organism more fit being passed on to its offspring and if some – or most? – of our microbiota is randomly acquired from the environment, natural selection can’t act on it. On the other hand, it’s very possible reality doesn’t abide by our definitions: perhaps only a few microbial taxa need to be passed directly from parent to offspring and these “founders” get microbial communities off on the right track and the rest of the communities fall into place from the environment.

Regardless – Brucker and Bordenstein pretty conclusively turned that sad story into a science story by showing that in Nasonia wasps, gut microbes play an integral role in hybrid survival. And if the Hologenome Theory of Evolution applies anywhere, I’d say it does here!

A healthy viable Nasonia holobiont (top) and an unhealthy, inviable Nasonia holobiont (bottom). From Brucker and Bordenstein (2013), figure 1B.

The sad story told in pictures: A healthy, viable Nasonia holobiont (top) and an unhealthy, inviable Nasonia holobiont (bottom). From Brucker and Bordenstein (2013), figure 1B.

Brucker, R. M. & Bordenstein, S. R. 2013. The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341: 667-669.

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