Monophyletic species yet again: a recent example

Recently I received a publication alert for Ja soon to be published manuscript. It gave me reason once more to write about the issue of "monophyletic" species.

I do not want to give the impression I am deliberately picking on this particular paper. On the one hand, for all I know its data are completely awesome and its conclusions are valid; the issue I am writing about here is somewhat tangential to the paper anyway, its main focus being on genus level phylogeny. On the other hand, this same issue can be seen in many, many other papers in the field, as all too many systematics lectures at universities seem to leave it at "stuff must be monophyletic", without explaining the relevant background like the various relationships that OTUs can have to each other and, crucially, that different classification approaches apply to different relationships. So the occasion here is really only that the present paper showcases the issue in an extremely compact format, all condensed down to a mere three sentences in the discussion.

In full they run as follows:

However, while cladists debate whether higher level taxonomic groups should be monophyletic (e.g. Horandl and Stuessy, 2010; Schmidt-Lebuhn, 2012), it is conceivable that species need not be monophyletic, as different modes of speciation may have different phylogenetic outcomes (Rieseberg and Brouillet, 1994); non-monophyly is an expected intermediate state as taxa diverge (Avise and Ball, 1990). Indeed, in a morphology - based survey of 206 Australian plant species and subspecies (Proteaceae and Fabaceae), Crisp and Chandler (1996) estimated that 21% were paraphyletic. In addition, eucalypt taxonomists generally follow the ecological species concept that allows for hybridisation between taxa (Johnson, 1976), and such reticulation can cause non-monophyly and incongruence between morphological and genetic markers (e.g. Rutherford et al., 2016).

So what do I find problematic about these three sentences? Going through again in order...

However, while cladists debate whether higher level taxonomic groups should be monophyletic (e.g. Horandl and Stuessy, 2010; Schmidt-Lebuhn, 2012),

First, Hoerandl and Stuessy are not cladists. Second, of course cladists do not debate if supraspecific taxa should be monophyletic, because a cladist is defined as somebody who has already decided that supraspecific taxa should be monophyletic. If you still debate it you are by definition Not A Cladist. Compare "vegetarians debate whether they should stop eating meat".  If they are still pondering that question they are Not Vegetarians.

it is conceivable that species need not be monophyletic,

This is where we get to the real issue: monophyly of species. Admittedly we first have to ask, are we talking about sexually reproducing species here? But I assume we are, because the article is about eucalypts, and they are mostly sexual. And the thing is, if that is the case then the concept of monophyly just simply does not apply. It is a word that describes a group of terminals on a rooted tree graph, like so:

A good analogy to describe what is going on is this. Imagine you have a real tree in front of you, and you are taking a group of twigs off using secateurs. To get a monophyletic group, you need to cut exactly once. To get a non-monophyletic group, you need to cut more than once. (If after cutting off a non-monophyletic group you have kept only one piece in your hand, it is paraphyletic; if you have kept several pieces but thrown out what used to connect them, it is polyphyletic. But that just as an aside.)

Within a sexually reproducing species, AKA a breeding group, there is no tree structure but a network structure, as individuals have numerous ancestors in each generation as opposed to one. That looks like this:

How do you get a monophyletic group? Well, you cannot, it is impossible. You could argue that my secateurs analogy would work for paraphyly even in a network, but only by jumping over the "imagine you have a real tree in front of you" part. You don't have a tree, you have a fishnet.

So to me this fragment - and everything that follows - makes as much sense as "it is conceivable that songs need not be yellow with purple stripes". Of course they don't - Amy Winehouse's Rehab, for example, is not yellow with purple stripes and yet it is a perfectly acceptable song. But then again I have no idea how it could be yellow with purple stripes, even if one were to try and make it so.

as different modes of speciation may have different phylogenetic outcomes (Rieseberg and Brouillet, 1994); non-monophyly is an expected intermediate state as taxa diverge (Avise and Ball, 1990).

Opponents of Phylogenetic Systematics regularly make the argument that "non-monophyly is an expected intermediate state as taxa diverge" at all taxonomic levels. At the supraspecific level, this constitutes a rather clear example of circular reasoning. A cladist would argue that a subclade cannot diverge from the larger clade it is part of, ever, because it is by definition part of that clade. That is what the sub- part of subclade means.

At the species level, on the other hand, the above fragment makes sense if we think of incomplete lineage sorting. Barring recombination, the copies or alleles of an individual gene do indeed evolve in a tree-like fashion, and the alleles found in one species will at first generally be paraphyletic to the copies found in its sister species. Only over time will selection or even loss through purely stochastic processes (genetic drift) make the alleles from each species monophyletic on the gene tree, a process known as lineage sorting.

It is possible that this is what the authors are referring to. But to me it still does not mean that it makes sense to call a species paraphyletic, because the components of a species are not gene copies but individuals, and individuals of the same sexually reproducing species stand in a network-relationship to each other, so that the word paraphyletic does not apply.

Indeed, in a morphology - based survey of 206 Australian plant species and subspecies (Proteaceae and Fabaceae), Crisp and Chandler (1996) estimated that 21% were paraphyletic.

Although I would not use the terms as they did (see above), the conclusions of the Crisp & Chandler paper are completely in accord with what I am saying here: species are special, because they are the level at which and from which on downwards it does not make sense any more to try and make stuff monophyletic. That being said, however, the paper does show species as paraphyletic on several morphology-based trees. How did it arrive at that result? Or in other words, given what I wrote earlier, what is the difference in perspective?

First, the terminals on the trees in Crisp & Chandler, the OTUs, are not actually individuals but groups of individuals, such as populations or subspecies; second, the authors conducted phylogenetic analyses on these OTUs. What that means is that the OTUs are forced into a tree-relationship even if the true relationship is net-like, because that is what phylogenetic analyses do. But if we are really talking about structures within a breeding group, within a sexually reproducing species, then in my eyes that analysis was just not appropriate because yes, the true relationship is net-like instead of tree-like. (And if the OTUs are not in a net-like, reticulating relationship, but instead genetically isolated, separate evolutionary linages, then why aren't they recognised as species?)

For example, I can jot down some morphological traits of a bunch of fellow humans, make a data matrix, and do a phylogenetic analysis. Because I do a phylogenetic analysis, the analysis will invariably return a tree. But does that mean that each of my OTUs - individual humans - had only a single parent, and only a single grandparent? Of course not, because we humans do not have a branching, tree-like relationship to each other either. The analysis simply made assumptions that do not hold up against reality.

In addition, eucalypt taxonomists generally follow the ecological species concept that allows for hybridisation between taxa (Johnson, 1976), and such reticulation can cause non-monophyly

Unfortunately it is left unclear what items are forming a non-monophyletic group in those situations. If it is alleles, see a few paragraphs further up; if it is individuals, see the immediately preceding section.

and incongruence between morphological and genetic markers (e.g. Rutherford et al., 2016).

That is true, but we could also mention several other processes, like aforementioned incomplete lineage sorting, meaning that we can have such incongruence even in the complete absence of hybridisation.

To close this post I would like to present a little paragraph that shows how the three sentences discussed above read to me:

However, while opponents of Scottish independence debate whether Scotland should be independent, it is conceivable that citizens need not be independent nations as different ways of acquiring citizenship may have different political outcomes; not being a geographic entity is an expected intermediate state as nations become independent countries. Indeed, in a survey of 206 individual citizens, Doe & Average (2010) estimated that 21% of them were not independent nations. In addition, political scientists usually follow a concept of citizenship that allows dual citizenship, and such reticulation can cause nations not being independent from other nations and incongruence between native language and nationality.

Again, this could be part of a great article on the Scottish independence movement, just like the present paper presents interesting genomic data on its study genus. But does this read as if the author was just a tiny bit confused about the difference between nations and the citizens that nations consist of? Quite so.

A lot of unproductive controversy and confusion among systematists and evolutionary biologists could be avoided if it became a bit more widely known what even ur-cladist Willi Hennig himself had in mind when he came up with the idea of "making stuff monophyletic". He was only arguing that supraspecific taxa should be monophyletic groups of species; the concept of species being monophyletic groups of individuals would not have made any sense to him, as he was very clear on the difference between usually tree-like (phylogenetic) relationships between species and net-like relationships within them.

Reference

Crisp MD, Chandler GT, 1996. Paraphyletic species. Telopea 6(4): 813–844.