Beating the dead horse Paraphyly.

I know I said I was going to cut back on the ICZNerdery. But this letter by Jaroslav Flegr to Zootaxa this week was too weird to pass up. Morgan Jackson summed it up nicely:

Sometimes I wonder if I could submit some of my blog posts to journals. Then I read stuff like this http://t.co/Ezy6niv5pn & realize I could
— Morgan Jackson (@BioInFocus) November 26, 2013

Summary (tl;dr): There is not one shred of anything new here. There's not even anything nomeclature related. The author is using Zootaxa to opine about paraphyletic inclusive classification, that is it, there's nothing else to this "paper" if it could even be called that. (Though, note: the link above only contains the first page and references if you don't have a subscription.)


The title, "Why Drosophila is not Drosophila anymore, why it will be worse and what can be done about it?", suggests this is going to be about the Drosophila melanogaster ICZN case last year. I never wrote a proper post about it, and given the complicated nature of the case I'd prefer not to repeat it here. So check out Kim Van Der Lin's summary in the link if you need a reminder. 

But the title is deceptive. Flegr starts off discussing the case, and he gets one thing wrong immediately. Molecular taxonomic studies have not shown that "the correct name of this species should be Sophophora melanogaster". What they have shown is that Drosophila as it stands now is a paraphyletic taxon. The actual raising of the subgenera to genus level is something that has yet to happen. And when, inevitably, someone revises the genus and raises them, the rest of us can dispute that action. That's right, you heard me correctly. Changing a taxon's rank, changing it's genus, etcetera, are subjective decisions, and unlike the fixation of types are not regulated under the Code. Someone else can come along later and challenge it without getting the Commission involved. D. melanogaster is also not "the fly that eats their fruit". Though they are often called "fruit flies", the common name is "vinegar flies" because they feed on fermenting fluids.

The rest of the "paper" is devoted to supporting a paraphyly friendly classification system, something that seems quite strange to the Cladist majority of taxonomists. Now, mind you, there's nothing in the Code prohibiting paraphyly, but the majority reject it because we've become devoted to a classification system that is descriptive, predictive, and explanatory. We've discovered that when our biological classification is based upon evolutionary descent, and in particular on monophyletic groups (groups that contain a common ancestor and all of it's descendants), it is a powerful general reference system. And when that system includes paraphyletic groups (which contain a common ancestor and only some of it's descendants), it looses predictive and explanatory power.

Flegr moves to his point in a roundabout manner, first starting with an utterly confusing explanation of paraphyly. (Note: Taxonomists are overwhelmingly visual. Reading a long list of possible relationships between Taxon A and Taxon B is about like trying to decipher one of my grandfather's differential equations.) Fer Linneaus sake, use a real life example!  He blames molecular systematics for the multiplication of paraphyletic taxa in recent years, which is a common enough theme in the literature that I don't pay it much attention. All it tells us is that the author is a traditional taxonomist who probably uses physical structures of the organism exclusively.

His statements about "inner and outer similarity" reflect a real problem in systematics, sometimes called the phenotype/genotype conflict. When we infer evolutionary relationships, often times the physical and DNA characters deliver us a differently shaped tree, and we're unable to tell whether one or either of these reflects reality better. But calling it a "conflict" is a misnomer. As one of my committee members recently told me, there is no real conflict between between the morphological and molecular characters. The conflict is in the methodology, and how we analyze the data. Flegr writes "nothing might be possible to guess from a system that would not reflect the inner similarity of the species", as if morphology is doomed to forever represent convergence and DNA is innately neutral to selection. Neither of these are right. 

The deep and real problem that he is reaching for but missing, is that many traditional classifications are based upon obvious physical characters rather than evolutionarily meaningful ones. There are, for example, many characters that place birds as a therapod lineage. But since these are not as obvious as "has feathers" and "is warm blooded", and since this uniqueness is part of a traditional classification, people continue to place them in a separate lineage from other archaeosaurs. Why? Because tradition, because, as Flegr puts it, "secondary school biology teachers are far much more numerous than theoretical taxonomists."

I'll refrain from commenting upon this except to say that allowing high school biology teachers to dictate how we should classify organisms is ridiculous.

Flegr's solution is to allow paraphyletic groups to stand. Of course. What better way to solve a problem than to ignore that it exists? Then you don't have to go through the messy route of educating people. And while we're at it, why don't we just throw out this whole evolution thing? It's so much easier to classify organisms based on obvious characters like, for example, lacking wings. The insect order "Aptera" worked out so well.

There are also some fairly ugly diagrams which are not at all convincing. 

Throughout, Flegr tries to make his case using the prevalence of punctuated equilibrium in major radiations rather than gradual change. Somehow this is evidence for rejecting reciprocal monophyly. I don't see it. There's also the opinion that these phylogenies will make our classification system inherently unstable. To which I reply: They are unstable now. Classifications that are based upon obvious similarities rather than evolutionarily relevant characters will forever be subject to the whims of authority opinions. What Flegr wants is to go back to the days of evolutionary taxonomy, where if Dr. Smith was the expert on so and so group, then whatever he said goes. NOPE NOPE NOPE. 

This is all very much a Dubois-ism, in the spirit of the last paper I wrote about. He concludes,

It is, of course, probable that most of the current theoretical taxonomists, who spent a large part of their active professional life fighting the fuzzy eclectic phylogenetics and taxonomy, would not be very enthusiastic about the recurrent more and more urgent suggestions of rehabilitating the paraphyletic taxa (Hörandl, 2006; Hörandl & Stuessy, 2010; Podani, 2010a; Zander, 2010). The change, fuelled by practical taxonomists who mostly use a ‘wrong’ eclectic taxonomy in their everyday practice anyway, will be probably slow and painful. It is, however, necessary to start the change as soon as possible. Otherwise, we might soon have to say farewell not only to drosophilas but to the whole taxonomic system.

I suspect these authors he cites are all in the same boat, a bunch of "taxonomic reactionaries" who can't cope with their authority being overturned and their traditional taxa being reshaped by evolutionary understanding. They call it "practical taxonomy"; I call it the easy way out. Flegr also shows himself to be a doomsayer by the last line. It's the end of the world as we know it, apparently.

In closing, no, wait. I don't think this mess merits a wrap up. Flegr leaves us one last gift, a tagline. 

"Australopithecus sapiens, possibly Reptilia, Pisces"

1. Australopithecus does not have priority over Homo. 
2. Reptilia is a paraphyletic group.
3. So is Pisces.

Trichoptera to Tachinidae

Well, it has been a while, hasn't it? I just recently got back into the swing of posting regularly. Before that there was a long silence, a diapause (as Bug Girl recently characterized her absence from blogging). And to be honest, the things I was posting about weren't terribly interesting. Minutia of The Code is a technical activity at best, a lawyerly pursuit at worst (reading the backlog for the ICZN-listserv shows this), and not something for general audiences.

I started this blog in 2008 during the first semester of my Master's degree, in part inspired from Bug Girl's Blog and the few other insect blogs around at the time. I wanted to improve my writing, and I wanted to relate my interest in caddisflies, a group I had just begun to investigate. Caddisflies will forever be my first love, no doubt, but in the denouement of my master's thesis I became interested in other groups. It was both temporary burn out and lack of funding in that direction; I was without a "real" job, working in a restaurant, trying to pay back some of my student loans. I had a brief, unpaid internship at Chicago Field Museum (which has had it's own recent financial difficulties), still operating under the assumption that if I just got enough practical experiences in museums one would actually hire me.

It was half way through that valley year that I discovered I was really missing research, and I was missing universities and academia. The long term revision of the North American Keroplatidae that I had been planning seemed like the perfect project for a PhD thesis. Unfortunately, the programs I applied to didn't agree with me, or more likely they didn't have the space or money for that sort of research.

Cutting to the point: I finally found a PhD assistantship! But the work was in neither caddisflies nor fungus gnats. This was an entirely new to me group of insects, an important and diverse group of flies called tachinids. 

A Plethora of Tachinids: Most look like the gray and silver ones at the right side of the third row.

Tachinid flies (Family Tachinidae) are a worldwide distributed, ultra-diverse family of true flies with around 8,000 described species, and many more yet to be described. And we think that all this diversity is relatively recent, with the stem group branching out around 30 to 40 million years ago. The really special thing about tachinids is that they are all endoparasitoids of other arthropods. By which I mean, they all do the 'Aliens' thing. Yeah, that thing. The young get into their hosts by some means, and there the larvae grow and slowly eat the host out from the inside. When they pupate, they burst out and metamorphose inside their last larval skin (called a puparium), leaving behind the empty husk of their host. Endoparasitoids (or the techinical term, koinobionts) do not make a good bedtime children's story (The Very Hungry Caterpillar,  this is not), but they are a great platform for studying evolution and evolutionary interactions. Parasitoids can be ultra specialist, like many tiny braconid wasps that have only one host species, or super generalist like the tachinid Compsilura concinnata, which feeds on over 120 species and across several insect orders. Most tachinids are in the middle range, with a few to 10s of host species. Why they aren't particularly host limited like other groups will be the subject of a future post.

The majority of tachinids attack plant feeding insects, especially moth caterpillars, sawfly larvae, and beetle larvae, and are probably a significant factor in controlling agricultural pests. A few species have even been mass released as active biological controls. And there are some tachinids which are pests in their own right, including the Uzifly which attacks silkworms and causes millions in damages to sericulture every year. Some of the more unique tachinid groups have unusual hosts, like crickets or stick insects, or ant queens, or stink bugs. There is even a tachinid that attacks trapdoor spiders (Antrodiaetidae).

It's a little funny to me that as important and ubiquitous as tachinids are, they don't really have a common name. The family name, Tachinidae, comes from the Greek word tachys meaning 'swift', so I guess we could call them swift flies. Other names people have used include: parasitic flies, hairy parasitoid flies, hedgehog flies, and bristle flies. None of those names have really stuck, despite being wonderfully descriptive, so people continue to use the abreviated form of the family name. In general, tachinids are small to large sized dark colored, hairy house fly like insects, often with patches of silvery wax, and sometimes with bright orange, yellow or metallic coloration. The hairyness is probably the thing that stands out the most about tachinids, and many of the individual bristles are used in identifying and classifying these flies. A good number of tachinid adults are flower feeders, and some are striking bee and wasp mimics.

If you want to learn more about tachinids, the best place to start is the Homepage for Tachinid Resources. There's also the Tachinid Times, an annual newsletter for tachinid research. This year's issue just came out yesterday, and it's a particularly nice one. Dr. O'Hara (the editor) was kind enough to allow me a full page to describe my intended PhD research, which I will be outlining more in detail next week. There are also lots of pretty pictures, so go check it out!

Limnocentropodidae: The Tethered Casemakers.

Limnocentropodidae is a small family of case making caddisflies distributed throughout the East Palearctic, from Nepal to Japan, to India and Indonesia in the South. The family consists of a single genus, Limnocentropus, containing 15 described species (Trichoptera World Checklist, 2012). Larvae are filter feeders in streams and rivers (sometimes torrential currents), facing head and legs first into the current much like the common Nearctic genus Brachycentrus (Brachycentridae), but it is there that any similarities to other casemaking caddisfly families end.

A Limnocentropus insolitus larva, from Haiya, Kyoto Prefecture, Japan. The photographer calls it a "kita gami", the Japanese name for the group. (© 2011 hir**amiyam*)

Both the larvae and adults are aberrant among other casemaking caddisfly families in their morphology and the odd architecture of the cases. As can be seen partially in the photo above, the case is a tapered tube of rock and leaf fragments, tethered to the substrate via a tough, silken stalk nearly as long as the case, and coated in tiny silk denticles. These predatory larvae extend their stout, hairy legs into the current like a net, snagging drifting insect larvae and other aquatic invertebrates. When it comes time to pupate, the larvae narrow the posterior end of the case, shorten the stalk, and build a wide collar around the anterior opening, possibly to help funnel water through the case. Some species will form their pupal houses in long chain like aggregations, with the stalks attached to the preceding cases (Wiggins 2004). Adult limnocentropodids are unique in retaining hardened mandibles; most caddisflies have only a sponge-like haustellum (Latin for "little suck") much like that of a house fly. (Kjer 2010).

A Limnocentropus himalayanus male. Despite being present, the mandibles are quite small and nearly undetectable in this photo. (Kjer 2006, Public Domain)

Because these stalk-casemakers are so weird, trichopterologists have had a hard time classifying this family. Glen Wiggins and Henry Frania (1997) placed Limnocentropodidae as a sister family to the rest of the case making caddisflies based in not possessing characters placing them in either the Brevitentoria (Herbert Ross's "long-horned-caddis-like" group) or the Plenitentoria ("northern-casemaker-like" group). More recent work using molecular characters (Kjer et al. 2002) and combined molecular and morphological characters (Holzenthal et al. 2007) supports placement within Brevitentoria, but any deeper classification has been unstable (Kjer 2010).

References

Frania, H. E., and G. B. Wiggins. 1997. Analysis of morphological and behavioural evidence for the phylogeny and higher classification of Trichoptera (Insecta). Life Sciences Contributions, Royal Ontario Museum, 160, 1–67.

Holzenthal, R. W., R. J. Blahnik, K. M. Kjer, and A. L. Prather. 2007. An update on the phylogeny of Caddisflies (Trichoptera). Proceedings of the XIIth International Symposium on Trichoptera. Bueno-Soria, R. Barba-Alvearz and B. Armitage (Eds). pp. 143-153. The Caddis Press.

Kjer, K. M. 2010. Limnocentropodidae. Limnocentropus. Version 20 July 2010 (under construction). http://tolweb.org/Limnocentropus/14593/2010.07.20 in The Tree of Life Web Project, http://tolweb.org/ [Accessed 17 February 2012].

Kjer, K. M., R. J. Blahnik, and R. W. Holzenthal. 2002. Phylogeny of Caddisflies (Insecta, Trichoptera), Zoologica Scripta 31(1) :83-91.

Morse, J. C. (ed.) 2012. Trichoptera World Checklist http://entweb.clemson.edu/database/trichopt/index.htm [Accessed 17 February 2012]

Wiggins, G. B. 2004. Caddisflies: The Underwater Architects. University of Toronto Press, Toronto, ON. [ed: includes detailed drawings of larval and case morphology]

The hollow curve, lumpers versus splitters, and arbitrary (yet useful) ranks.

Yesterday, science journalist Ed Yong asked "which genus has the largest number of living species" as a Google+ thread. He admitted that it was a trivial question of curiosity, and he's right. While the wood boring genus Agrilus (Coleoptera: Buprestidae) may have the most described number of species (~3000), this is not a particularly important or interesting question when it comes to taxonomy or systematics in general. However, the question spawned an energetic argument over the arbitrariness of taxonomic groups in terms of size and content, and I wanted to speak my piece about it.

[If you graph] the number of genera contained in any group [of organisms] against the number of species contained in those genera, using one axis for genera and the other for species, we get, apparently regardless of the group we are dealing and the quality of the systematic work done upon the group, a curve of a characteristic form. This has been called the "hollow curve of distribution". (from Ferris (1928) The Principles of Systematic Entomology)

In modern ecology the hollow curve describes the relative species abundance within a community, but it also describes the distribution of species within genera. A small number of genera will have a large number of species relative to the whole, and a greater number of genera will each have a relatively small number of species. Unlike ecology, this was an probably an artifact of human taxonomy and the continuous disagreement between "lumpers" and "splitters".

An exaggerated "hollow curve of distribution" for visualization, with numbers of species on the Y axis and number of genera on the X axis.

The general consensus in systematics is that species are real groups of organisms, and for the purposes of this post I would not like to argue over that point, or about genetics or species concepts. Likewise, monophyletic groups, that is, groups of species which share a single common ancestor, are also real. After the modern evolutionary synthesis and the description of classification as the depiction of evolutionary relationships and not overall similarity (regardless of relationship), monophyletic groups became the standard for describing taxa.

A simplified version of the Linnean Hierarchy (© Tutor-Vista)

However, taxonomic ranks (e.g. family, genus, tribe) above species and the decision to place a particular group as a genus or a tribe, for example, is completely subjective and somewhat arbitrary. The hollow curve of distribution was due to the choice of some taxonomists to make large genera ("lumpers"), and of others to whittle those large genera down to smaller genera over time, or to raise a genus to tribe and the subgenera within to genera ("splitters"). This is sometimes called "taxonomic inflation" by those who see this tactic as an attempt by the taxonomist to raise the public importance of his or her group of interest. These split up genera are all monophyletic groups, just much smaller, more manageable monophyletic groups. (ETA: other hypotheses in the comments)

Still, the Linnean ranking system remains useful in relating hierarchy. It is unambiguous that a tribe belongs to a family, that a subgenus belongs to a genus (ETA: though not necessarily to the genus you /think/ it belongs to, or including the members you would expect: see comment by Christopher Taylor below). If I tell you a species is of the Tribe Hydropsychini, it is taken for granted that the tribe contains genera, and is contained by a family (in this case Hydropsychidae). This makes it easy to organize the general reference system. Ranks also make it easier for taxonomist to communicate their phylogenies. (ETA: Again, see comment by Taylor below)

Unfortunately there are some taxonomists who are uncomfortable with the Linnean system of ranks. Among these are the people responsible for the Phylocode. The Phylocode eliminates the Linnean ranking system and replaces it with a hierarchy of unranked "clades", while species names are still described under the rules of the already established codes of nomenclature. This to me seems like hierarchical obfuscation. While it is very easy to communicate a hierarchy using ranks, it is very difficult to do so without them. Anti-ranking advocates complain there are not enough ranks to properly describe all the monophyletic groups, but the code doesn't prohibit the creation of new ranks above and within family level ranks, they just are not covered under the rules. If you want to talk about a semi-infra-tribe, or a super-kingdom, that's perfectly acceptable. Any other criticisms, like the issue of hybridism, are best addressed within the individual codes. To collapse and remake the entire general reference system just to eliminate rankings (which are useful in their own right) is preposterous. Enough people were upset over the Drosophila case that there may be rioting in the universities if Phylocode is ever successful.

So, while the arguments that taxonomic groupings are arbitrary is false, ranks are somewhat arbitrary and yet useful. The important notion is to not rely on them as indicators of importance. And that questions like "what's the largest genus" comes down to a trivial contest of lumpers versus splitters. In this case the winners are probably beetles (is anyone surprised?).

Agrilus derasofaciatus (CC Encyclopedia of Life)

The uses and folly of DNA 'barcoding'.

According to Wired, DNA barcoding has gone mainstream. I fail to see how this is possible since sequencing technology, as cheap as it is becoming, continues to only be available to few and not the public. It's not like, for example, you can pick up a PCR kit and "Sony Deluxe Pirosequencer XL" on Amazon (though you can make your own gel eletrophoresis setup).

If you aren't familiar with the concept, a DNA 'barcode' is a short length of DNA sequence that can distinguish between closely related species. In most cases when people talk about it, they mean the mitochondrial gene Cytochrome C Oxidase subunit I (or COI for short). COI is found universally in all organisms that have mitochondria, so people talk about it being a "universal barcode", that could be potentially used to identify any (eukaryotic) organism on the planet.

The process for getting a sequence is relatively simple, assuming you have the technology. A small piece of the organism in question is broken down and run through a polymerase chain reaction cycle to amplify the COI gene fragments. Then it is sequenced, either through dye-terminator sequencing or the more fancy, faster, more expensive pirosequencing. The sequences are uploaded to a general reference database such as Bold Systems, which anyone can use to compare their sequences to a known set. The expectation is that the more species sequenced, the more likely you are to get a match.

And to the credit of the IBOL team, some of these applications are really cool, like using the sequence library to catch mislabeled fish in markets and restaurants. That's awesome, one more tool in the diagnostic toobox, albeit an expensive one. Since there are so many copies of mitochondrial DNA in most organisms, far more than nuclear DNA, you only need a very small fragment to obtain a sequence. If the specimen is just a slab of meat at market, no problem! Even holotype specimens can be sampled nondestructively.

But identification is really where the utility of DNA barcoding ends, and given the time and expense for obtaining each sequence, it is and will continue to be far easier to use traditional diagnostic methods in most cases. It is not a magic bullet, and it's certainly not a replacement for taxonomy or systematics. Thinking that an entire species can be reduced to a single, definitive sequence length of 500 base pairs from a few individuals is insane. It would be the same as claiming it's alright to dam up Yosemite Valley because we have some photographs. As I pointed out before, the goal of taxonomy is to track characters and their relationships, and assemble a general reference system which is descriptive, predictive and explanatory. The COI gene is one character, out of millions. Reducing species to this one character is pure folly.

The other problem is the definitive nature of these barcodes. They fail to address the temporal variation in a species as it changes over time, much less the spacial variation or level of variation within a single population. Not to mention, the individual base pairs, not the entire sequence pattern or some portion, are used as defining differences in an analysis. How can we use a few individuals to define an entire species, when we know that variation in the defining character, the sequence, exists even between those few individuals? At least taxonomists recognize this variability and only choose character consistent for all known individuals as definitive.

Species are hypotheses, and these hypotheses are going to change over time, but it seems the DNA barcoding proponents may still hold to immutable species concepts despite 150 years of evolutionary revolution in biology.

Phryganeidae: The Giant Casemakers.

The Phryganeidae are a small family of caddisflies distributed throughout North America, Europe, and Asia. Wiggins (1996) lists the total as 15 genera and ~75 species; by my count from the World Trichoptera Checklist (Morse 2011) there are 80 extant and 37 fossil species. This family includes the largest known caddisflies. The larvae are case makers (as the common name suggests), and fashion tube cases of spiral or circular wrapped vegetation.

Oligostomis pardalis larva (© D.S. Chandler / Discover Life)

The genus name Phryganea has a long history of use, starting in the 10th edition of the Systema Naturae (Linnaeus 1758). Carl von Linne included 17 species of caddisflies in this work, all under the genus Phryganea (from the French word for caddisflies). Needless to say, most of these species have been removed to other families and genera. At the time, caddisflies, stoneflies, dragonflies and mayflies were all included under the order Neuroptera; it wasn't until 1813 that the Order Trichoptera was erected. Due to the original status of the genus, there are many nomenes dubius and synonyms that by far outnumber the species now in the entire family.

Banksiola dossuaria (© Trichoptera Barcode of Life)

In addition to large size (often greater than 25 mm), the adults are characterized by colorization ranging from the black and white checkers of Banksiola to the fall leaf orange of Ptilostomis to the yellow and dark purple of Eubasillissa. The largest species, Eubasillissa regina, is over 4 cm with an 7 to 8 cm wingspan. Dr. John Morse, who has spent much time collecting and studying aquatic insects in Southeast Asia, told me they look like a small bird with a strange flight pattern from afar.

Eubasilissa regina, the worlds largest caddisfly.

The larvae often have contrasting patterns of orange and black stripes on head and thorax, and are just as impressive as the adults in size. One of the most curious larval tendencies is the ease at which they leave their cases behind when disturbed. If one larva looses it's case and other of a similar size is occupied nearby, the two larvae will fight over the case (as illustrated in this video). Though they inhabit a wide variety of aquatic habitats, they are found most often around the roots and stems of aquatic vegetation, and in root balls of woody plants, with a diet of mostly aquatic invertebrates.

The definitive guide for the family is an eponymously named book by Glen Wiggins (1998), and despite being over ten years old is still in print and in demand. The book includes genus keys and diagnoses for all the species know at its publication, including all 28 North American species. Wiggins splits the family into the Yphriinae (which includes a single species of Yphria from Western North America), and the Phryganeinae, though the separation is drawn due to 'primitive characters' possessed by Yphria is to me not particularly convincing, and may be paraphyletic.


References

Morse, J.C. (ed.) 2011. Trichoptera World Checklist. http://entweb.clemson.edu/database/trichopt/index.htm [Accessed 24 October 2011.]

Wiggins GB. 1977. Larvae of the North American Caddisfly Genera. University of Toronto Press, Toronto, ON.

Wiggins, G.B. 1998. The Caddisfly Family Phryganeidae (Trichoptera). University of Toronto Press, Toronto, ON.