Two Animal Nervous Systems?

Why would anyone ever care about a phylogeny? Why on Earth should we care which species are each others' closest relatives?

The reason boils down to traits. If two species share a very similar trait, but they are distantly related phylogenetically, then something interesting has happened in evolution. Perhaps that trait has evolved twice separately, and if that is true, perhaps we could predict that under similar conditions, another species would also evolve that trait. Alternatively, maybe the trait in question was lost multiple times in intervening groups - were the genes also lost? Now this is the interesting stuff, trait evolution!

Unfortunatley, I think that phylogeneticists sometimes short change traits. Phylophiles' papers can tend to get wrapped up in the relationships of a particular group, to the point of forgetting why anyone would ever care, forgetting what those relationships might mean (anyone else attend an Evolution meeting during the heyday of molecular phylogenetics, circa 1995? You know what I mean).

Symptomatic of this focus on the tree and not on the traits are cases where a paper spends an enormous amount of energy (mental and computational) on inferring the best tree; but then makes claims about the evolution of traits without a single statistic.

A paper this week by Shierwater et al, published in Plos-Biology precisely illustrates this point. The authors do an admirable job of resolving the major branches of the animal tree of life. They present a large dataset and compare many approaches and models with a statistical rigor that would make Willi Hennig, RA Fisher and Reverand Bayes proud. The authors end up with a well-supported, and fascinating result: Animals are divided into two epic clades - the bilaterians (e.g. flies, clams, and humans) on one hand and all other animals (sponges, jellies, and the enigmatic Trichoplax) on the other. But why might we care where Trichoplax falls on the tree? It's because of the traits.

It's in the traits that the paper disappoints me. After putting the computational pedal to the metal to estimate the tree and check its sensitivity to different statistical approaches, the paper simply asserts the paradigm-shifting claim that organ, nervous, and sensory systems must have evolved in parallel in the two epic clades. Here is how they stated it:

"We conclude that the higher animals (Bilateria) and lower animals (diploblasts), probably separated very early, at the very beginning of metazoan animal evolution and independently evolved their complex body plans, including body axes, nervous system, sensory organs, and other characteristics."

in the press:

"Nervous systems are found in both groups (among the lower animals, jellyfish have nervous systems), so the new arrangement means that these systems must have evolved twice in the history of animal evolution..."

and also in the paper:

"Most notable of these aspects is the evolution of the nervous system, which in the hypothesis in [the figure showing their tree], can only be explained by convergent evolution of Cnidaria and Bilateria nervous system organization."

So, what about the possibility of loss? Let's examine this possibility with the most rudimentary, and intuitive of phylogenetic methods, parsimony. Let's also assume that the phylogeny presented in the paper is the correct tree.



panel a and b show the phylogenetic tree supported by the recent paper. Panel a shows two separate gains of nervous systems (black vertical bars). Panel b shows an alternative hypothesis, not mentioned in the paper (unless it's in the supplement, which I haven't read yet). In the alternative, nervous systems originated with animals, and were lost (white vertical bars) in the lineages leading to Trichoplax and sponges.

Yes, two changes is fewer than three, and this is the story the paper and the press went with. But is it really more parsimonious (OED definition "the simplest state, process, evolutionary pathway, etc")? Can we really argue that it is simpler to evolve a nervous system twice than it is to gain it once and lose it twice? Maybe we can? This is what we are left with when using parsimony. (Likelihood and Bayesian methods often get us only slightly farther when dealing with characters).

That said, perhaps we can use these two alternative evolutionary pathways - two gains versus one gain and two losses - as alternative hypotheses (of course there are other possible pathways, but I'll ignore those for now). Do these hypotheses make alternative predictions? (Self promotion: please cite Oakley and Cunningham, 2000 if you buy this alternative hypothesis bit. You only have to read the last paragraph).

If the bilaterian and jelly nervous systems are independently evolved, we might expect them to be quite different, and use mostly different genes. This is not the case. We know of many similarities of the nervous systems of jellies and bilaterians.

Alternatively, if nervous systems were lost, we might expect to find remnants of nervous systems littering the genomes of sponges and Trichoplax. In fact, this is exactly what is found. Sponges and Trichoplax have many genes homologous to genes used in bilaterian nervous systems. (Shameless self promotion: please cite Sakarya et al 2007 which shows many synaptic genes are present in the sponge Amphimedon. We mostly assumed sponges as sister to other animals for that paper. But we still mentioned the possibility that the sponge lineage could've lost synapses).


Of course, in the end a "nervous system" is not one thing. Therefore, the question of homology becomes a bit of a red herring. Everything, except protein domain homology is partial homology! Instead, it becomes much more interesting and instructive to break down multi-part systems like nervous systems into components and to trace the evolutionary history of those components. Do these components evolve in a concerted way? Do components come and go? What processes drive divergences of these genes?

I know Shierwater et al are aware of these issues, but I'd have appreciated a more balanced discussion of alternative possibilities (what if Trichoplax is reduced, and not the ancestral animal? See Ryan, Chuck, and Bart on this one.) In the end, the traits are the interesting bit, so we should analyze them with the same statistical rigor as the tree, and treat interpretaions with the same caution and balance!!


Refer

Bernd Schierwater, Michael Eitel, Wolfgang Jakob, Hans-Jürgen Osigus, Heike Hadrys, Stephen L. Dellaporta, Sergios-Orestis Kolokotronis, Rob DeSalle (2009). Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis PLoS Biology, 7 (1) DOI: 10.1371/journal.pbio.1000020

Phylogeny, evolution, biodiversity and ecology

We are in the midst of massive upheaval in the world’s ecosystems, driven by species invasions and the sixth mass extinction in Earth’s history. How will these changes in biodiversity affect the functions of ecological communities? Will the functions of ecological systems that humans rely on for survival, such as production of oxygen, be impacted by all this upheaval?

Answering these questions requires that biologists have a good metric for biodiversity. New research by Marc Cadotte, Brad Cardinale and I, and published this week in Proceedings of the National Academy of Sciences, indicates that one particular metric of biodiversity - evolutionary diversity - is a particularly strong predictor of the biomass produced in plant communities: The more biodiversity present (measured as evolutionary diversity), the more productive the community. In fact, for the datasets we examined, evolutionary diversity was a better predictor of productivity than raw species number or number of functional groups in the community. This suggests that the most evolutionarily diverse communities may function best, and that the most evolutionarily distinct species might be the best targets of conservation efforts aimed at maximizing ecosystem productivity.

Measuring Biodiversity
One common theme in current ecological research is to ask questions about how changes in biodiversity impact or influence ecological systems or communities. This has obvious importance when we know that many species are going extinct, and that many species are being shipped around the world by human transportation. Often in ecological research, a measure of biodiversity is placed on the X-axis, and some predicted response is placed on the Y-axis, to test if there is a strong relationship. For example, one might predict that less diverse and simpler communities are more susceptible to invasive species compared to more diverse and complex communities. One might also predict that more ecological diversity leads to a healthier ecosystem, as measured by higher production. Namely, a higher diversity of organisms could make more efficient or more complete use of available resources, ultimately leading to a healthier, better functioning ecosystem.

These types of ecological studies usually use a measure of biodiversity referred to as “species richness” as the X-axis variable. “Species richness” is simply a count of the number of species. However, simply counting species makes the assumption that, say, two very closely related grass species contribute the same amount to the diversity measure as two much more distantly related species, such as a grass and a magnolia. In contrast to this implicit assumption of “species richness”, phylogeneticists often think of biodiversity in terms of evolutionary relationships, assuming that differences between species (one way to conceive of diversity) accumulate over the time since they last shared a common ancestor. To a phylogeneticist then, species that share a very recent common ancestor – like the two similar grasses mentioned above – should be nearly identical and therefore represent less total diversity compared to the much more distantly related grass and magnolia species.

We wondered if evolutionary diversity really does matter for predicting how much biomass a community produces, one measure of the health of ecological communities. Decades of experiments have already established that species number (“species richness”) is in fact correlated with productivity – the more species of plants growing together, the more biomass is produced. We extended these studies, weighing different species by how closely related they are evolutionarily. Could we better predict biomass production by also accounting for evolutionary (phylogenetic) diversity? Based on our analyses, the answer was a clear “yes”. Incorporating evolutionary distances into our biodiversity metric resulted in better predictive power of the productiveness of experimental plant communities. The metric including evolutionary history was better than “species richness” and better than the number of functional plant groups, two commonly used metrics of biodiversity.

Our data set was a collection of 40 different previously published experimental studies, conducted around the world using a total of 177 different species of flowering plants. Researchers planted experimental ecological communities, using many different combinations of plant species, and using different numbers of species. Then they let the communities grow, and measured the biomass produced by the different combinations. We added an analysis of the phylogenetic relationships of the plants using publicly available genetic data from four different genes commonly used in other studies of plant phylogeny.

Phylogenetics and Nihilism

Do all ecologists now need to become phylogeneticists? This question is similar to one asked of comparative biologists in the mid 1980’s.

In 1985, Joe Felsenstein wrote a landmark paper introducing the method of phylogenetic independent contrasts, which is now standard in comparative biology. The core message is that we cannot treat species as independent entities because they share a nested set of common ancestors. In other words, species are similar because of descent, not only because of adaptations, and traits might be correlated across species because of shared evolutionary history. At that time, comparative biologists were told they must consider phylogeny when testing for correlations among traits. Felsenstein addressed the question, “What if we do not take phylogeny into consideration [in comparative biology]?” His answer:

“Some reviewers of this paper felt that the message was “rather nihilistic,” and suggested that it would be much improved if I could present a simple and robust method that obviated the need to have an accurate knowledge of the phylogeny. I entirely sympathize, but do not have a method that solves the problem…. Comparative biologists may understandably feel frustrated upon being told that they need to know the phylogenies of their groups in detail, when this is not something that they had much interest in knowing. Nevertheless, efforts to cope with the effects of the phylogeny will have to be made. Phylogenies are fundamental to comparative biology; there is no doing it without taking them into account.”

-Felsenstein (1985)

Although other systems and other questions might differ from our study in how diversity relates to ecological processes, it seems to me that counting species is far too simplistic of a metric of biodiversity. If adding phylogenetic information was valuable in one case, it seems worthy of strong consideration any time a metric of diversity is below the X-axis in a graph. To paraphrase Joe, ecologists may understandably feel frustrated upon being told that they need to know the phylogenies of their groups in detail, when this is not something that they had much interest in knowing. Nevertheless, the evolutionary history of their focal communities or systems will often have a lot to tell them. Species are not independent entities, and biodiversity cannot be measured as if they were.

M. W. Cadotte, B. J. Cardinale, T. H. Oakley (2008). Evolutionary history and the effect of biodiversity on plant productivity Proceedings of the National Academy of Sciences, 105 (44), 17012-17017 DOI: 10.1073/pnas.0805962105