Biogeography, cryptic species and amoebae

If you are lucky enough to know a protistologist, you have certainly heard her (or him) utter the statement: “not much is known about protist _________”, where the blank can be filled with your choice of a biological subject, such as “meiosis”, “ecology”, “paleontology”, and many others. The statement gets staggeringly truthful when the blank is filled with the word “biogeography”.

To me this has always been very interesting because biogeography is one of the most intuitive biological concepts: anyone knows that there are some biological species that simply won’t show up in their backyards. If you live in South America, you can expect to see a Capibara, even (or specially) in a large metropole like Sao Paulo. This is not true for London, Berlin, or Moscow, unless you are at the local Zoo. Similarly, people living in Sao Paulo know that they won’t see a Grizzly Bear, or any bears at all – leading to the very intuitive notion that animals have restricted geographical ranges. This is also true for plants, one of my personal dreams is to see a Baobab, but I would have to travel to one of the other pieces of Gondwana to see it.

Which brings us to the first thing that may influence how species are distributed on the planet: the geological history of the place where a given biological species had first appeared. If you check the following map, depicting what the supercontinent Gondwana must have looked like in the past, you can understand how different iconic fossils were distributed. The logical assumption by looking at these ancestral distributions is that the descendants of these biological species will inhabit the same places. The difference is that by now, those continents have moved apart.

ImageSource: Wikipedia

The same kid who knows that they won’t find a bear in Sao Paulo also knows that they will not find a Great White shark roaming the streets (although that would certainly be a cool sight). But that is because Great Whites are exclusively marine animals that can not survive on land. Although this may seem like a simplistic analogy, it illustrates a distinct issue altogher: ecological requirements. Besides the geological history of the biological species distributions, ecological requirements will also restrict the places on earth where a given species can be found.

Therefore, biological entities should be distributed across the globe according to geological history and ecological requirements, right? No. Protists are more difficult. Firstly, you generally can’t see them without a microscope. So, people need to get trained on microscopy to start seeing protists. Even then, it may be difficult to identify species among them. Take a look at the following images:

ImageImage

Source: micro*scope

Although very similar, these are two distinct genera of amoebae. If you know who they are, you certainly have a few of years of protistology under your belt. This is the first difficulty in protist biogeography – we must live with the possibility that different species live in different places, but we can’t tell them apart because trained morphologists are hard to come by [1]. To overcome this difficulty, people came up with the concept of “flagship species”: these would be easy to identify, large and abundant species [2]. That way, if the organisms are somewhere in the world that has ever been sampled by a human being, those organisms have a high probability of having been recorded. This is where the testate amoebae come into play. I use the following example in classes:

Image

Quadrulella symmetrica. Source: Ferry Siemensma.

This is a Quadrulella symmetrica. If you can’t remember the look of an amoeba that lives inside a shell she made herself out of internally mineralized square pieces of glass, then maybe biology isn’t for you. Testate amoebae are really good models to ask biogeographical and ecological questions, because they are so conspicuous. The problem is that we do not know much about their taxonomy, but that is quickly changing.

These easily identifiable, large and abundant species, are found everywhere that present their ecological requirements. So in the protist world, the sentence in bold above is generally translated to everything is everywhere, the environment selects. A simplistic way to explain this paradigm is that because protists are small, they should be able to disperse to all places, which seems to be a reasonable assumption [3]. This basically destroys the assumption that geological history must have an effect on the distributions of organisms, simply because they can potentially override this constraint. The second part of the paradigm, is quite similar to the shark analogy, and is to me the least understood part, not only in protist biology (well, not the extreme example of sharks on land, but more sutile things like pH gradients).

Recently, Thierry Heger and colleagues published a very intriguing study dealing with these questions [4]. They chose a single “morphospecies” to test some of these predictions — the testate amoeba Hyalosphenia papilio, a quite “flagshippy” species.

Image

Hyalosphenia papilio. Source: Dan Lahr.

They sampled 42 Sphagnum dominated locations in 11 northern countries, obtaining over 300 individuals! They then went on to sequence a marker gene from each of these individuals and tried to correlate the genetic divergences with either geographical or ecological factors.

It may be surprising to some that even though Heger and colleagues sampled individuals that look almost exactly identical, they actually found 12 distinct genetic lineages. Now, the people who performed this work are experienced testate amoebae researchers, so we can rule out the possibility that they lumped together a bunch of morphologically distinct taxa. This may be a typical case of a “cryptic species”, lineages have diverged but the morphology has not yet changed. There is a small possibility that each of these 12 lineages actually have a distinguishing characteristic, but these would be so minimal that would not be of much help.

Even more surprising may be the fact that geographical distribution, or rather vicariance, cannot be an explanation to the divergence of these 12 distinct lineages. The following map is a figure from their paper, and shows how the different lineages were spread in the globe.

ImageAlthough you can already see that a particular place in the world doesn’t contain a single type of Hyalosphenia papilio, they went further ahead and tested this statistically, also testing if environmental variables they collected in specific sites could explain the distribution pattern.  They found out that climatic factors alone were responsible for 21% of the variation, while spatial factors (geography) were responsible for 3% of the variation.  The two combined factors explain an additional 13%.

Amazingly, this means that 63% of the variation is due to unkown factors.  In my view, this is solid proof that when a protistologist tells you that “not much is known about protist __________“, you should take them very seriously, because we can still learn a whole lot from the wee-beasties.

Literature

[1] Mitchell EAD, Meisterfeld R. 2005. Taxonomic confusion blurs the debate on cosmopolitanism versus local endemism of free-living protists. Protist 156(3): 263-267.

[2] Foissner, W. 2006. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozoologica 45(2): 111-136.

[3] Wilkinson, D. M., Koumoutsaris, S., Mitchell, E. A., & Bey, I. (2012). Modelling the effect of size on the aerial dispersal of microorganisms. Journal of Biogeography, 39(1), 89-97.

[4] Heger, T. J., Mitchell, E. A., & Leander, B. S. (2013). Holarctic phylogeography of the testate amoeba Hyalosphenia papilio (Amoebozoa: Arcellinida) reveals extensive genetic diversity explained more by environment than dispersal limitation. Molecular ecology, 22(20), 5172-5184.
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