Monday, December 8, 2014

The word paraphyletic still doesn't apply to groups of sexually reproducing individuals (that special issue on paraphyly)

(The following is the third part of a series of posts on an Annals of the Missouri Botanical Garden special issue on “Evolutionary Systematics and Paraphyly”. All posts in this series are tagged with “that special issue”.)

(Updated 29 December 2014 to increase clarity and to make the style a bit less strident.)

Although I have yet to read through all of them, I can already say that the first proper paper in the special issue, Lockhart et al.'s “We are still learning about the nature of species and their evolutionary relationships”, seems a bit out of place. It focuses mostly on one idea: there might be ongoing gene flow between the entities we currently recognise as species, and therefore the currently used coalescent species tree methods might be inappropriate to reconstruct phylogenies in those situations.

If that were it, one could happily agree, all cladists could happily agree, and we could call it a day. However, this paper was submitted as a contribution to a campaign for the recognition of paraphyletic supraspecific taxa, and so the clear implication is that the observation of occasional introgression between closely related species somehow means we should not classify organisms by their relatedness. The other authors of the special issue will surely cite this paper as supportive of that position over the next few years, and Lockhart et al. must be aware of that.

Lockhart et al. themselves are careful to never spell such an argument out. Although several parts of the paper, including the conclusions, discuss the aforementioned limitations of species tree reconstruction methods that assume all conflicts in the data should be explained as incomplete lineage sorting, remarks dealing with classification are limited to a few instances, and they are either vague or conceptually confused (“paraphyletic gene trees” = gene trees on which the gene copies from one species are paraphyletic to those from another?).

To the degree that one can vaguely discern the shape of an argument relevant to classification, it appears to be, and I hope I do not misread the authors, the following:

Species are often paraphyletic, therefore we cannot make everything monophyletic, therefore Phylogenetic Systematics doesn't work.

Again I have to repeat myself: paraphyletic (note the bold part) means an incomplete branch of the tree of life. Imagine a tree, with its many branches, and imagine every terminal twig as one species. Take secateurs and snip off one of its branches. You now have a monophyletic group. Take the secateurs again and snip off one of the sub-branches of your branch, and the partial branch that you are left with is a paraphyletic group. So far, so good.

Now imagine the inside of a sexually reproducing species; it could be New Zealand alpine buttercups as discussed by Lockhart et al., but it might be easier to take humans because we are all familiar with ourselves. Do the relationships between humans look like a tree? Of course not. Whereas a species on the tree of life has only one ancestral species across the vast majority of deep time, I have two parents, four grandparents, eight great-grandparents, and so on until my ancestors number in the tens of thousands. And most of my ancestors had more than one child, and at some point my various ancestral lines overlap. The whole structure is not a tree but a net.

So, as you previously imagined the tree of life as a real tree, now imagine the inside of a species as a fishnet, with each knot an individual. What the authors here are concerned with is hybridisation between two or more of those species. So let us take a second fishnet and, using additional string, make several cross-connections between the two nets. The authors call that situation “paraphyletic species”. But does it look remotely similar to the incomplete tree branch from earlier? Clearly not.

Again, the word paraphyly does not apply to a structure that is completely non-phylogenetic. Consequently, a competent cladist would be the first to concede that no sexually reproducing species is monophyletic; but for the same reason, they aren't paraphyletic either. Phylogenetic Systematics demands that we do not accept partial branches of the tree of life as good taxa. Everything that is net-shaped would be a tip of the tree or, if it happened in the past, a tangle of branches. Cladists are concerned with how to group the tips, and they would generally treat a tangle of branches deeper down as a polytomy, resulting in a classification with, for example, five genera in the same subtribe, same as we always had. The classification does not have to be binary.

In other words, to the degree that the Lockhart et al. paper is relevant to the special issue it is included in that relevance is based on a misunderstanding.

There is one way in which hybridisation would have a major impact on cladism and indeed make it impossible: if hybridisation happened so frequently and across such large phylogenetic distances that there is no tree of life. If all of life were but a fishnet instead of a tree, there would be no clades.

But first we can, once more, observe that this would also mean that there would be no paraphyletic genera and families either, so that the usual argument that reticulation makes the recognition of paraphyla necessary is incoherent. More to the point however, we would have to ask whether hybridisation is really as rampant as to make evolutionary history mostly a net instead of mostly a tree.

Lockhart et al. surely do not make that argument; their paper deals with gene flow between very closely related, very young species. In other words, one cannot do phylogenetic classification on that group of species, but one can still treat it in its entirety as a tip of the tree.

And I simply doubt that gene flow happens (a) across such large distances and (b) to such a degree in most groups of organisms that there is no tree. As for the distances, it is a rare occasion that different genera of plants can be crossed, and usually when it happens it is because the genera are ill-circumscribed (i.e. one of them is paraphyletic to the other, as in the ferns Phyllitis, Ceterach and Asplenium). In a later contribution Tod Stuessy himself writes that hybridisation between different plant families is unheard of. The more distantly related two species are the less compatible their genomes get, and hybrids tend to be increasingly inviable.

As for the degree of gene flow, somebody I respect highly recently argued that chloroplast capture, endosymbiosis and occasional introgression of individual genes have transformed the tree into a net. However, those are rare events transferring only minor amounts of genetic information. It would be like moving a piece of bark from one tree branch to another and then arguing that there are no separate branches any more.

No, unless more convincing evidence comes along it seems reasonable to assume that the tree of life is, indeed, mostly a tree, at least for eukaryotes such as animals and plants. If convincing evidence to the contrary were found, that would be the argument that would make me drop cladism (although, again, that would also make 'evolutionary' classification impossible, and thus we would all have to become pheneticists). The Lockhart et al. paper, however, does not even attempt to provide such evidence, and all its considerations are compatible with cladism, and so I remain puzzled about the purpose behind its inclusion in this special issue arguing against cladism.

In the light of that observation, I have already spent way too much virtual ink on this paper, but there are two other aspects of it that I find interesting. The first is that many of the people arguing for paraphyletic taxa exhibit a misplaced worship of Charles Darwin, and that is very much in evidence even here. Much of the second page (page 7 of the issue) is dedicated to a lengthy discussion of Darwin's views on evolution that reads astonishingly similar to a theological exegesis of scripture; and the last paragraph of the same page implies that not only the authors but we all should deeply care about what Darwin thought on the matter.

This feels like a weird misunderstanding of how scientific controversies should be settled. It is utterly irrelevant what Darwin thought, and it is doubly irrelevant because he died decades before Phylogenetic Systematics was developed and could thus never assess its merits. Using his views as a cudgel against cladism is like using Newton to argue against the Theory of Relativity. But the same argument from authority is used in a few more contributions to this same special issue.

The second is that in one of the cases where Lockhart et al. cite me they completely failed to grasp my point: “while some authors suggest that biological classification should capture more evolutionary information (Hörandl & Stuessy, 2010), others question whether the acceptance of paraphyletic species as units for classification better reflects processes of evolution and patterns of biological diversity (Schmidt-Lebuhn, 2011)”. Quite apart from the fact that this is a false dilemma, my point was and still is that the word paraphyletic does not apply to sexually reproducing species in the first place, so the question of whether they should be accepted or not never arises.

Being used as a reference for B when I wrote A is a first for me, but it is an interesting experience.


Lockhart PJ, Larkum AWD, Becker M, Penny D, 2014. We are still learning about the nature of species and their evolutionary relationships. Annals of the Missouri Botanical Garden 100: 6-13.

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