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!!
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