Field of Science

A New Stem-Bird and Publication in the Digital Age


Scansoriopteryx heilmanni, as reconstructed by Stacey Burgess.


First off, notification of the focus of this post came via the Dinosaur Mailing List.

It is almost a truism that the internet has changed the face of scientific publishing. Online versions of journals have become the first port of call for many, if not most, researchers. The paper reprint has become an endangered species, and articles are exchanged via e-mail as pdfs. Online-based journals such as BMC Biology and the PLoS collection have abandoned the standard journal format with articles collected into issues, and release articles as and when they become available. Even among those journals that still release regular issues, many have begun offering advance online releases of upcoming articles. For most branches of science, these advances are mostly all for the good. Good science, after all, is largely dependent on access to information, and there is much to be said for allowing the dissemination of new information as quickly and easily as possible. However, at least one branch of science, taxonomy, remains firmly attached to the printed page, and has good reasons for doing so.

As alluded to here before, taxonomy differs from other sciences in that it provides the means for communication between biologists working in other disciplines as well as being a target of investigation in its own right. In order to facilitate communication, it makes sense that (a) the taxonomic system should be as stable as possible*, and (b) when conflicting taxonomies do arise, then the means for determining the correct nomenclature to use should be as simple and automatic as possible. It is to satisfy this second requirement that taxonomic systems employ the principle of priority - if two separate names exist for the same taxon, then the correct name to use is the one that was published first.

*Though, as with governments, "stable" in this context does not necessarily mean "unchanging". Rather, it means "not prone to change without proper cause".


Scansoriopteryx again, this time by Matthew Martyniuk.


Of course, saying that the first name to be published is correct immediately raises the question of what counts as publication. The International Code of Zoological Nomenclature (Article 8) requires that a published work must be issued in a permanent format, and must be generally made available upon publication. These are pretty broad criteria, but any work (and any new names within) cannot be considered published until they are met. The date at which these criteria are met becomes the official date of publication. Release of an article online (such as in a pre-print) does not count as publication in this sense because a webpage is not permanent. While a book requires little or no attention once it has been accessed in a library and can sit there more or less indefinitely*, a webpage requires continual upkeep to remain available. The ICZN does allow a name to be published online if some form of permanent copy (such as a print-out or CD) of the webpage is deposited in a number of major public libraries (such as the American Library of Congress). As far as I know, the Botanical Code still insists on printed publication.

*Okay, theoretically a book may be at risk of decaying after a few hundred years, but that's still pretty permanent compared to a website.

In June last year, the Nature group launched Nature Precedings, an online repository for preliminary findings and manuscripts, allowing researchers to share data of interest that might or might not be sufficient for an eventual completed paper, obtain feedback on said preliminaries that might improve the final manuscript, and just generally keep other researchers informed on what was going on. Entries on Nature Precedings are not peer-reviewed before becoming available, and are generally not regarded as completed publications. A few days ago, a new entry was loaded on Nature Precedings by Zhang et al. describing a decidedly interesting new dinosaur species, complete with attached name. Officially, this taxon is not yet published. Because of the interest that surrounds any new dinosaur discovery, you can bet your ass that that won't stand in the way of its becoming widely known.


The new scansoriopterygid, which I'm calling Les. Figure from Zhang et al.


As I said, there's a name attached to the new taxon. It's a very nice name, too - kind of rolls off the tongue. But because I'd rather avoid using an unpublished taxon name, I'm keeping shtum (of course, click on the link and you'll find the name right away, so my protest is really pretty pointless). Because the new species is a member of the family Scansoriopterygidae, I'm going to call it LES (standing for "Looks like Epidendrosaurus or Scansoriopteryx"). Les was a small bird-like theropod about the size of a pigeon, and represented by a very nice nearly-complete skeleton, complete with preserved feathers including a tail of four long ribbon-like feathers that were about as long as the rest of the animal. Phylogenetically, Zhang et al. position Les as more closely related to modern birds than the dromaeosaurs (Velociraptor et al.) but less closely related than Archaeopteryx. Les is exactly the sort of thing that might eventually be published in Nature, and its appearance in Nature Precedings gives the impression of leading into doing so.

The family Les belongs to, Scansoriopterygidae, has become something of a poster child for the issues surrounding online publication. Two genera have previously been named for scansoriopterygids, Scansoriopteryx and Epidendrosaurus, but most researchers suspect that these two names refer to the same animal. Unfortunately, determining which of the two names has priority is not a straightforward question, as discussed by Harris (2004). Both names were published in 2002, but the book naming Scansoriopteryx was probably less widely read than the journal naming Epidendrosaurus. Epidendrosaurus appeared in an online preprint on the 21 August, but the printed version didn't appear until 30 September. The exact date of publication of Scansoriopteryx is a little debatable, but it seems to have become available by 2 September - after the name Epidendrosaurus became widely publicised online, but before the official publication of Epidendrosaurus. Technically, Scansoriopteryx has priority, even though Epidendrosaurus was the name that became known to the public first.

The lesson from cases such as Scansoriopteryx is that the time has well and truly arrived for us to re-evaluate what it means for a name to be "published" in the digital age. In the past, the first a public would generally hear of a manuscript and its contents was when the finished publication arrived in all its official glory. Now, as demonstrated by Les, it may be possible for a manuscript to appear online as a rough draft, as a polished pre-print, as the final official product. Should these early appearances be regarded as valid publications? When the manuscript first appears, or only as it approaches its final form? The initial format for publication of Epidendrosaurus may not have been permanent, but should we regard the later appearance of a permanent printed edition as having validated that initial appearance? The rules of the game are changing. It is time to decide whether we should keep playing.

REFERENCES

Harris, J. D. 2004. 'Published works' in the electronic age: recommended amendments to Articles 8 and 9 of the Code. Bulletin of Zoological Nomenclature 61 (3): 138-148.

Pig's Toes and Water Nymphs


The Wabash pigtoe, Fusconaia flava, a widespread species of freshwater bivalve found in both the Mississippi and Great Lakes Basins, and the effective type species of the genus (i.e. the actual type species is a synonym of this one). Photo from Mussels of Illinois.


Despite my aforementioned anti-bivalve bias, the time has once again come for a bivalve to hold the coveted position of Taxon of the Week. What, I hear you ask, is the lucky, lucky bivalve so favoured? None other, I reply, than the North American freshwater genus Fusconaia.

In contrast to the great diversity of freshwater gastropods, surprisingly few groups of bivalves have really made a go of things in the freshwater environment. The superfamily Unionoidea is therefore very distinctive in not only including the largest number of freshwater bivalves, but in fact being only found in freshwater. Fusconaia is a genus of Unionoidea, usually included in the family Unionidae and subfamily Ambleminae, found in many river basins of North America. Members of Fusconaia are rather unfairly lumbered with the vernacular name of "pigtoe", evidently a reference to the shape of the shell. For some reason, North American unionids have garnered more than their fair share of memorable names - Motley (1933) gives us "heelsplitter", "elephant's ear", and for one particularly unfortunate Fusconaia species, F. ebena, "niggerhead". Thankfully, that last name seems to have been universally replaced in the present day by "ebonyshell". Those more charitably disposed towards the family might refer to them as "freshwater pearly mussels" or "naiads". "Naiad" derives from a classical Greek term for a class of water spirit, so Fusconaia would mean 'brown nymph'. 'Brown nymph' is arguably a slight improvement over 'pigtoe'.

Other than their memorable names, unionids are most famed for their distinctive life cycles. After fertilisation, female naiads (unionids have separate males and females) brood their eggs in the gills until they hatch out into bivalved larvae with big teeth on the shells called glochidia. Upon release, glochidia attach themselves to the gills of a passing fish and live as parasites, forming a cyst until they hatch out and develop into a mature mussel. At least some unionids actually develop fleshy outgrowths of the gills that mimic a small fish in order to attract a suitable host for their glochidia - I haven't established whether Fusconaia is one of the unionids that does so. Speaking speculatively, perhaps the biggest advantage unionids gain from this life cycle is overcoming the hurdle of dispersal in fresh water environments. Most marine bivalves have larvae that disperse as plankton, but this is obviously not a suitable option in fresh water, where currents are either more or less non-existent (lakes) or would inevitably carry the larvae into an unsuitable environment (rivers). [Is this why there are so few freshwater bivalves?] Attaching to a fish potentially allows the unionid larva to disperse upstream. Once they do settle down, most unionids grow very slowly - Bruenderman & Neves (1993) found that Fusconaia cuneolus, the fine-rayed pigtoe of Virginia, grew an average of five millimetres per year for the first ten years of its life, then slowed down to a more sedate two millimetres per year. Because of their slow growth, vulnerability to environmental pollutants and changes (they are sessile filter feeders, after all) and reliance on the presence of suitable fish to act as glochidial hosts, many unionid species are critically endangered. About one-eighth of Recent North American amblemine taxa are believed to have become extinct, and another quarter are endangered or threatened (Campbell et al., 2005).


The longsolid, Fusconaia subrotunda. Photo by Gary Peeples.


Establishing exactly which species are threatened is another matter. Taxonomically, unionids can only be described as evil. Graf & Cummings (2007) listed fifteen species in the genus Fusconaia, but many widespread unionid species are decidedly variable. Prior to the beginning of the 1900s and the revisionary work in North America by Simpson and Oortman, a large number of species and subspecies were erected based on what are now regarded as ecological variants of other species. According to Graf & Cummings (2007), no less than 4955 species-group names are available to unionoids for 840 currently-recognised valid taxa, giving an average of nearly five synonyms for every valid species*. Graf (1997, in an unpublished thesis) listed no less than forty species-group names of relevance to the taxonomy of Fusconaia flava, the widespread Wabash pigtoe. Even after narrowing the field down to valid species only, the confusion is not yet over. Campbell et al. (2005) suggested based on molecular analysis that many, if not most, of the currently recongised North American unionid genera are polyphyletic. Fusconaia, originally established by Simpson in 1900 primarily on the basis that its species incubated their eggs in all four gills, included representatives of no less than three tribes of Unionidae.

*More than 1000 of these were introduced for supposed European (mostly French) taxa by the so-called Nouvelle École of Jules-René Bourguignat and his successors in France in the late 1800s (Graf, 2007). So extravagant were the efforts of the Nouvelle École that C. T. Simpson, when reviewing the world's unionid fauna, simply refused to consider them, complaining in 1900 that, "Life is too short and valuable to be wasted in any attempt at deciphering such nonsense".

REFERENCES

Bruenderman, S. A., & R. J. Neves. 1993. Life history of the endangered fine-rayed pigtoe Fusconaia cuneolus (Bivalvia: Unionidae) in the Clinch River, Virginia. American Malacological Bulletin 10 (1): 83-91.

Campbell, D. C., J. M. Serb, J. E. Buhay, K. J. Roe, R. L. Minton & C. Lydeard. 2005. Phylogeny of North American amblemines (Bivalvia, Unionoida): prodigious polyphyly proves pervasive across genera. Invertebrate Biology 124 (2): 131-164.

Graf, D. L. 1997. Morphology, Zoogeography, and Taxonomy of Fusconaia flava (Rafinesque) (Mollusca: Bivalvia: Unionidae) in the Upper Mississippi, Great Lakes, and Nelson River Basins. MSc thesis, Northeastern University, Boston.

Graf, D. L. 2007. Palearctic freshwater mussel (Mollusca: Bivalvia: Unionoida) diversity and the Comparatory Method as a species concept. Proceedings of the Academy of Natural Sciences of Philadelphia 156: 71-88.

Graf, D. L., & K. S. Cummings. 2007. Review of the systematics and global diversity of freshwater mussel species (Bivalvia: Unionoida). Journal of Molluscan Studies 73 (4): 291-314.

Motley, H. L. 1933. Histology of the fresh-water mussel heart with reference to its physiological reactions. Journal of Morphology 54 (2): 415-427.

What's in the Shrubbery?

The latest edition of Berry Go Round, the monthly blog carnival celebrating plant life, has arrived at Gravity's Rainbow, so go take a look! And don't worry, I can assure that this Gravity's Rainbow is a lot easier to read than that other Gravity's Rainbow.

Also, the next edition of Linnaeus' Legacy will be hosted within the week by the Podblack Cat. Get your posts directly into Ms. Cat (podblack at gmail.com) or use the submission form.

The Empty Sea

This is actually a pretty old video (it dates back to 1991) but I thought I'd put it up because:

     (a) John Clarke is a very, very funny man (trust me, this isn't even him at his best), and

     (b)even seventeen years later, the attitude parodied here is still all too common.



Of course, what holders of such attitudes don't realise is that those who desecrate the open ocean are sentenced in the afterlife to be devoured by the Great Tomopterid.

Mite-in-a-Box


Nothrus truncatus, a member of the holoid Desmonomata. Photo by Agriculture and Agri-Food Canada.


Mites are pretty remarkable creatures. I don't know if any other group of animals can rival mites for ecological diversity. There are mites burrowing in the leaf litter of forests, there are mites living in the sediment at the bottom of the sea, there are mites living off the secretions in your hair follicles, there are are mites that live as parasites of other animals. Whatever freakish thing you can think of an animal doing, odds are that there is a mite doing it right now. Mites also include one of the few groups of terrestrial arthropods to have developed a mineralised exoskeleton - the oribatids or beetle mites. Our newest Taxon of the Week is one of the subgroups of oribatids, the Holonota.

The Holonota include the most heavily armoured of the oribatids, with most of the body encased in hardened plates. Morphologically, Holonota are distinguished from other oribatids by having the entire body covered by two dorsal plates, with the division between the two plates between the positions of the second and third pairs of legs. Technically speaking, various Holonota may be dichoid, holoid or ptychoid (Norton, 2001). In dichoid forms, a non-hardened zone runs around the body between the second and third pairs of legs, allowing the body to bend at that position. Holoid forms only have this articulation dorsally, with the ventral surface fused to a solid plate. Ptychoid forms, on the other hand, have reduced the ventral hardening and are actually able to withdraw the legs and close the anterior dorsal plate over them - the mites' answer to ostracods.

Norton (2001) suggests that the development of heavy armour in the oribatids may be related to their lifestyle. Most oribatids are long-lived (at least for mites) and have low reproductive rates, a situation that may result from their usual diet of low-nutrient decaying vegetation and fungi. Slow growth and replacement rates may result in the selective favouring of features that extend the life expectancies of individuals.


The ptychoid mite Atropacarus striculus (Phthiracaridae), showing how the legs can be withdrawn and covered over. Photo from Oribatid Mites of Alberta.


Morphologically, Holonota have been divided between three groups, the Mixonomata, Desmonomata and Circumdehiscentiae (Maraun et al., 2004). The Mixonomata includes dichoid and ptychoid forms, and has been suggested to be paraphyletic to a holoid clade formed by the other two taxa. In turn, the Desmonomata are probably paraphyletic with regards to the Circumdehiscentiae. The holoid Circumdehiscentiae are one of most speciose groups of oribatids, and show the highest degree of plate fusion, with the armour of almost the entire underside fused with the anterior dorsal plate (Norton, 2001). Molecular analyses, in contrast, have been divided in their support for this arrangement. Maraun et al. (2004) failed to support the morphological view, and did not even recover monophyly for the Holonota as a whole or for the Circumdehiscentiae. More recently, however, the morphological phylogeny with monophyletic Holonota and serially paraphyletic Mixonomata and Desmonomata was supported by the results of Domes et al. (2007).

In light of the repeated evolution of ever-greater degrees of sclerotisation within the Holonota, it might seem surprising if one lineage was to do a complete volte-face and lose all trace of armour, but exactly this possibility has been suggested (Norton, 2001). The Astigmata are a lineage of mites related to the Oribatida, but ecologically distinct. While oribatids are armoured, slow-living, litter feeders, astigmatans are unarmoured, fast-breeding and mostly live in close association with other animals, often as parasites. Astigmata include such luminaries as Sarcoptes scabiei, the skin-burrowing monstrosity that causes scabies*. Despite these differences, it has been suggested that Astigmata are actually derived from oribatids through paedomorphosis (retention of juvenile characters as adults) - and specifically from Desmonomata, one of the most heavily armoured groups of oribatids. However, support for Astigmata as derived desmonomates remains equivocal. While supported by some morphological characters and gland chemistry, the suggestion has not garnered molecular support. Mauran et al. (2004) supported an oribatid ancestry for Astigmata, though not necessarily from Desmonomata (they also only included a single species of Astigmata in their analysis). Domes et al. (2007), analysing a larger selection of astigmates, rejected a position for Astigmata within Oribatida.

*Offhand, if you had to invent a name for a revolting skin condition, could you ever come up with a more appropriate-sounding term than 'scabies'?

REFERENCES

Domes, K., M. Althammer, R. A. Norton, S. Scheu & M. Maraun. 2007. The phylogenetic relationship between Astigmata and Oribatida (Acari) as indicated by molecular markers. Experimental and Applied Acarology 42 (3): 159-171.

Maraun, M., M. Heethoff, K. Schneider, S. Scheu, G. Weigmann, J. Cianciolo, R. H. Thomas & R. A. Norton. 2004. Molecular phylogeny of oribatid mites (Oribatida, Acari): evidence for multiple radiations of parthenogenetic lineages. Experimental and Applied Acarology 33 (3): 183-201.

Norton, R. A. 2001. Systematic relationships of Nothrolohmanniidae, and the evolutionary plasticity of body form in Enarthronota (Acari: Oribatida). In Acarology: Proceedings of the 10th International Congress (R. B. Halliday, D. E. Walter, H. C. Proctor, R. A. Norton & M. J. Colloff, eds.) pp. 58-75. CSIRO Publishing: Melbourne.

Open Lab 2008



Submissions are currently being accepted for OpenLab 2008, an anthology of the best science-blog writing of 2008. So if there's anything here at the Catalogue that has particularly impressed you in the past year, click on the logo above or on the sidebar and nominate it for inclusion. I missed out last year - maybe this year will restore my fragile ego.

Life in the Palaeocene - We Don't Need No Placentalia?


The pantodont Coryphodon, as reconstructed by Heinrich Harder. At the time of their existence, pantodonts were the largest herbivorous mammals. According to Wikipedia, Coryphodon reached about a metre in height and a weight of half a tonne, and also had the dubious distinction of having the smallest brain/body weight ratio of any mammal living or extinct.


Sixty-five million years ago last Tuesday, the mighty dinosaurs went extinct. Well, they didn't all go extinct, but that's how it's usually expressed because "the mighty dinosaurs went extinct except for a number of volant clades that actually continued to do pretty well for themselves, really" somehow just doesn't have quite the same ring to it. What remains a fact is that something pretty significant happened to the ecosystem at the end of the Cretaceous, leading to a major turnover that's usually represented as out with the dinosaurs, bring in the mammals. It is true that the mammals showed a significant rise in diversity during the Palaeocene, the time period immediately following the Cretaceous. However, few of the prominent mammalian groups of the time would be recognisable today.

Modern mammals are divided between monotreme, marsupials and placentals. It is the Placentalia (the group we ourselves belong to) that have been the most successful of the three groups overall, a success that has generally been attributed to their reproductive system of nourishing developing foetuses for longer periods and giving birth to more developed young*. When the fossil record is actually taken into account, Placentalia are a subset of a larger group called Eutheria. Eutherians are the total group containing placentals and all fossil mammals more closely related to placentals than marsupials, while placentals are the crown group of the eutherian lineages that have survived to the present.

*Whether this is really the secret of the placentals' success is more debatable than generally let on. For instance, it has been suggested that in highly unpredictable environments such as the arid centre of modern Australia, marsupials, with their lower nutrient commitment to developing offspring, may actually have the edge reproductive system-wise.


Skull of the taeniodont Psittacotherium, from Matthew (1937) via Paleocene Mammals. Late Palaeocene taeniodonts developed massively powerful jaws and cutting teeth. Psittacotherium was one of the most extreme forms, and at a weight of about 50 kg would have been comparable in size to a medium dog.


The eutherian and marsupial lineages had separated from each other by the early Cretaceous, but the question of when the modern placentals arose has been a hotly debated topic. While a number of Cretaceous lineages have been suggested to belong to the Cretaceous crown group - Zhelestidae as relatives of the ungulates (hoofed mammals), while Zalambdalestidae were close to rodents and lagomorphs (Archibald et al., 2001) - recent analyses have placed these taxa outside the placental crown, and the fairly comprehensive analysis by Wible et al. (2007) suggested that none of the fossil eutherians known from the Cretaceous are placentals. This stands in fairly stark contrast to molecular dating studies, which are fairly unanimous in suggesting that the modern placental orders diverged from each other during the Cretaceous. Either the molecular dating is all wrong for some reason, or the placentals were around in the Cretaceous and we just haven't found them yet.

Still, whether it was the ancestors of the placentals or a number of lineages that survived the end of the Cretaceous, the fossil evidence indicates at least four eutherian lineages survived into the Palaeocene. The Cimolestidae and Leptictidae, families present in both the Cretaceous and the Palaeocene, were placed by Wible et al. (2007) outside the placentals, while the Taeniodonta, a eutherian lineage of unknown relationships, was represented in the late Cretaceous by the species Schowalteria clemensi (Fox & Naylor, 2003). Whether the various other lineages known from the Palaeocene diverged from these lines after the end of the Cretaceous or also survived from earlier times is a decidedly open question.

As already indicated, few of the Palaeocene eutherians can be related directly to modern placental orders. Instead, the Palaeocene was the time of a number of lineages that are no longer with use - herbivores such as the pantodonts and dinocerates, small insectivores such as apatemyids and leptictids, carnivores such as creodonts and arctocyonids. Martin Jehle's Paleocene Mammals website has detailed coverage of many such groups. Palaeocene mammals were also quite distinct from modern taxa in the overall range of morphologies - for want of a better way to put it, Palaeocene eutherians tend to look - well - lumpier than modern species. The broad grasslands that currently dominate the terrestrial part of the world were not yet in existence, and the Palaeocene was a time of forests. As a result, the grassland-adapted cursorial morphologies like modern horses and antelope were also absent, and the low-slung waddler was king.


The early dinocerate Prodinoceras xinjiangensis, as reconstructed by Stanton Fink.


So how did these Palaeocene waddlers relate to the modern taxa evolutionarily? The only answer we can really give at this point is, who knows? The relationships between the Palaeocene and the modern eutherian orders remain almost completely unknown, and those few connections that have been accepted in the past have been profoundly shaken. For instance, many of the Palaeocene families have been included in the 'condylarths', a heterogeneous assemblage believed to be related to the modern ungulates. However, it has become well established in recent years that the ungulates represent at least three separate lineages, with the artiodactyls (even-toed hoofed mammals), perissodactyls (horses and rhinoceros) and paenungulates (elephants and hyraxes) all arising from separate ancestors in the placental tree. Which condylarths are related to which modern ungulates? For that matter, are they related to any of them? If the ungulate morphology arose at least three times in lineages that survived to the present, why should we assume that it couldn't have also appeared independently in extinct lineages? Similar issues surround Palaeocene 'insectivoran' families, whose association with possibly polyphyletic modern insectivorans should be regarded as doubtful.

In light of the findings of Wible et al. (2007), we might even doubt whether many of the Palaeocene eutherians even represent placentals. The classification of McKenna and Bell (1997) united many early eutherians such as Cimolestidae, Pantodonta and Taeniodonta (as well as the modern pangolins) into a group called Cimolesta, which was then included in the Ferae with creodonts and Carnivora. While pangolins may indeed be related to carnivorans, Cimolestidae, as referred to above, are not even placentals. What then becomes of the rest of the "Cimolesta"? Are they also stem-eutherians like Cimolestidae, or are they true placentals?

Such questions are not mere curiosities - the answer could have significant effects on our understanding of Palaeocene ecology. At least some stem eutherians such as the Zalambdalestidae possessed epipubes, bones that support the pouch in marsupials but are absent from placentals (Kielan-Jaworowska, 1975). Because of the restrictions epipubes place on the expansion of the abdomen, they may be incompatible with a placental reproductive system. As a result, we cannot assume that stem eutherians bore well-developed young like modern placentals do. Did pantodonts walk around with pouches slung from their bellies?

REFERENCES

Archibald, J. D., A. O. Averianov & E. G. Ekdale. 2001. Late Cretaceous relatives of rabbits, rodents, and other extant eutherian mammals. Nature 414: 62-65.

Fox, R. C., & B. G. Naylor. 2003. A Late Cretaceous taeniodont (Eutheria, Mammalia) from Alberta, Canada. Neues Jahrbuch für Geologie und Paläontologie – Abhandlungen 229 (3): 393-420.

Kielan-Jaworowska, Z. 1975. Possible occurrence of marsupial bones in Cretaceous eutherian mammals. Nature 255: 698-699.

Wible, J. R., G. W. Rougier, M. J. Novacek & R. J. Asher. 2007. Cretaceous eutherians and Laurasian origin for placental mammals near the K/T boundary. Nature 447: 1003-1006.

Eureka! It's an Ant!

But not as we know it.

Rabeling, C., J. M. Brown & M. Verhaagh (in press). Newly discovered sister lineage sheds light on early ant evolution. Proceedings of the National Academy of Sciences of the USA.


Martialis heureka Rabeling & Verhaagh in Rabeling et al., 2008, as reconstructed in the original description by Barrett Klein. Scale bar on this and the following image represents 1 mm.


I have learnt through Alex Wild of a paper currently in press for PNAS describing a new species of ant. With more than 12,000 ant species already on the books, this may sound like something of a non-event, but trust me, it's not. This new ant, Martialis heureka, has been placed not only in a new genus, but in a whole new subfamily. In fact, Martialis appears to be the sister group to all other living ants. A quick request later, and the lead author, Christian Rabeling, was kind enough to send me a copy of the paper*.

*For those without ready journal access, don't be afraid to contact authors of articles you might be interested in and ask if they have spare copies. Most researchers will be all too happy to help you.

As yet, Martialis is known only from a single worker specimen collected in 2003 in leaf litter from the Brazilian Amazon. One of the authors had found two workers in a soil sample five years previously, but these specimens were subsequently lost. The species name heureka (Greek for "Give me a towel!") reflects this history of disappointment and elation. The genus name Martialis refers to the unusual appearance of the specimen which looked like it may as well have come from Mars. Martialis is a pale-coloured, eyeless ant with long, thin, pincer-like mandibles. Because of the absence of eyes and its being found in litter and soil samples, the authors infer that Martialis lives hypogaeically (under the ground) or in some other low-light habitat such as within logs. However, the new species lacks any noticeable adaptations for digging, so it may inhabit pre-existing cavities such as rotting roots or burrows made by other animals. The fine mandibles, unlike those of any other ant, may be used for drawing out soft-bodied burrowing prey such as insect larvae. Features such as the presence of a sting indicate that Martialis belongs to the basal grade of ants, and molecular analysis of the specimen indicated Martialis to be sister to all other ants.


Type specimen of Martialis heureka in side view. From the original description.


Interestingly, Rabeling et al.'s analysis also corroborates an earlier analysis by Brady et al. (2006) in finding the basalmost clade in the ants other than Martialis to be the Leptanillinae, another small hypogaeic subfamily. If this topology is correct, it is possible that the ancestor of all ants was hypogaeic. However, the current analysis was unable to statistically reject a number of alternative rootings.

The earliest fossil record of ants from the Cretaceous consists of the extinct subfamily Sphecomyrminae and a single species of the basal subfamily "Ponerinae" (Dlussky, 1999 - recent analyses indicate that the Ponerinae as previously recognised should be divided into a number of subfamilies, and I don't know whether the Cretaceous species would belong to the Ponerinae in the stricter sense). Dlussky (1999) recognises a separate family Armaniidae from the Cretaceous closely related to Formicidae, but Wilson (1987) argued that the "armaniids" are most likely winged castes of Sphecomyrminae. While the basal lineages of living ants might be hypogaeic, cryptic forms, the Sphecomyrminae, previously identified by its morphology as sister group to living ants, were wasp-like, probably epigaeic forms. Alternative positions for Sphecomyrminae within the crown clade seem unlikely in light of the absence of other ant fossils from the Cretaceous. I personally suspect that despite their basal position, there is a strong possibility that the hypogaeic lifestyle was acquired independently in Leptanillinae and Martialis rather than being ancestral for living ants as a whole.

REFERENCES

Brady, S. G., T. R. Schultz, B. L. Fisher & P. S. Ward. 2006. Evaluating alternative hypotheses for the early evolution and diversification of ants. Proceedings of the National Academy of Sciences of the USA 103 (48): 18172-18177.

Dlussky, G. M. 1999. The first find of the Formicoidea (Hymenoptera) from the lower Cretaceous of the Northern Hemisphere. Paleontologicheskii Zhurnal 1999 (3): 62-66 (transl. Paleontological Journal 33 (3): 274-277).

Wilson, E. O. 1987. The earliest known ants: an analysis of the Cretaceous species and an inference concerning their social organization. Paleobiology 13 (1): 44-53.

Fantastic Mr Fox


The Tibetan fox (Vulpes ferrilata), a distinctive fox species restricted to the Tibetan Plateau. Photo from the BBC via Lioncrusher's Domain.


Foxes are a widespread assemblage of canid predators, found through most of the Holarctic and drier Africa and also here in Australia, where the red fox Vulpes vulpes was introduced quite successfully. Too successfully, in fact - foxes are one of the most significant invasive species in Australia, and a dire threat to many native species. Of the slightly more than ten species in the fox genus Vulpes, the red fox is undoubtedly the most familiar, being both the most widespread species overall as well as the most abundant in developed countries. However, the familiarity of the red fox is a little misleading, as Vulpes vulpes is actually one of the more distinctive species in the genus, being considerably larger and arguably more dog-like than other foxes.

The morphological analysis of the Canidae by Tedford et al. (1995) supported a division of the living members of the family between two lineages, the Vulpini containing Vulpes, and the Canini including Canis (the genus including the domestic dog) and the South American canids. This early division is consistent with the early appearance of fossil species assigned to Vulpes, with V. stenognathus coming from the Late Miocene (Lyras & van der Geer, 2003). The majority of Vulpini were included in Vulpes except for the bat-eared fox (Otocyon megalotis) and the two species of grey foxes (Urocyon). Two species in the Vulpes clade, the fennec fox (Vulpes zerda or Fennecus zerda) and the Arctic fox (Alopex lagopus) have been regarded as separate genera, but it seems pretty well-established that doing so renders Vulpes paraphyletic (Zrzavý & Řičánková, 2004). More recent analyses using both molecular and morphological data have continued to support the Vulpes-Canini division (Zrzavý & Řičánková, 2004; Bardeleben et al., 2005), but results differ about the relationships of Vulpes to Urocyon and/or Otocyon, which may fall in a Vulpini clade or may be basal to the Vulpes + Canini split. Still, all recent authors seem to agree that, contrary to many older sources, the grey foxes should not be included in Vulpes.


The Indian fox (Vulpes bengalensis), the species nominated by Macdonald (1984) as the most representative of the genus. A nice atmospheric shot by Jon Hall.


Relationships within the Vulpes clade are fairly uncertain. Zrzavý & Řičánková (2004) tentatively suggested a division between two major groups that both may or may not be monophyletic, an 'Afro-Asiatic' clade and an 'Holarctic' clade. The 'Afro-Asiatic' group includes the fennec and pale fox (V. pallida) of northern Africa, the Cape fox (V. chama) of southern Africa, Blanford's fox (V. cana) of central Asia and probably the Indian fox (V. bengalensis), with the fennec and Blanford's foxes forming a clade. Within the 'Holarctic' group, Rüppell's fox (V. ruppelli) inhabits northern Africa, the red fox can be found across the entire Holarctic, and the corsac (V. corsac) and Tibetan foxes (V. ferrilata) are found in central Asia. The circumpolar Arctic fox forms a clade in the Holarctic group with the V. velox/V. macrotis complex, the swift and kit foxes, of North America. All fox species seem to inhabit temperate or dry climates - note particularly the wide geographical division between the Cape fox and all other species of the genus.

While foxes are generally characterised as solitary animals, and certainly do not form packs in the manner of Canis and closely related genera, individuals of at least some species may form small groups, usually a male and a number of vixens. Members of a group will still forage for food separately (Macdonald, 1984). All foxes use a characteristic high pounce in capturing prey, springing upwards and landing on their quarry from directly above it.



Of course, foxes are also famed for being one of the few animals able to transform their appearance at will. They share this ability with the tanuki (Nyctereutes procyonoides), a canid whose phylogenetic position relative to the Vulpes-Canini split remains uncertain. Nevertheless, the foxes would doubtless like to point out that they are not as prone to buffoonery as tanuki. Because of the uncertain position of the tanuki and a shocking shortage of studies of shape-changing abilities in fox species other than V. vulpes, we cannot presently comment whether the shape-changing ability is a plesiomorphy of crown canids that has been lost in the Canini, or has been acquired independently in foxes and tanuki.

REFERENCES

Bardeleben, C., R. L. Moore & R. K. Wayne. 2005. A molecular phylogeny of the Canidae based on six nuclear loci. Molecular Phylogenetics and Evolution 37 (3): 815-831.

Lyras, G. E., & A. A. E. van der Geer. 2003. External brain anatomy in relation to the phylogeny of Caninae (Carnivora: Canidae). Zoological Journal of the Linnean Society 138 (4): 505-522.

Macdonald, D. W. 1984. Foxes. In All the World’s Animals: Carnivores (D. Macdonald, ed.) pp. 60-67. Torstar Books Inc.: New York.

Tedford, R. H., B. E. Taylor & X. Wang. 1995. Phylogeny of the Caninae (Carnivora: Canidae): the living taxa. American Museum Novitates 3146: 1-37.

Zrzavý, J., & V. Řičánková. 2004. Phylogeny of Recent Canidae (Mammalia, Carnivora): relative reliability and utility of morphological and molecular datasets. Zoologica Scripta 33 (4): 311-333.

Getting the Hang of Compromisation


The Colombian bromeliad Puya santosii. Photo by Andreas of Bogotá.


Imagine if a prominent mathematician published the results of his investigation of the value of the number "3", and demonstrated that our understanding of that number's value was actually wrong. Or if physicists proved that the length of time referred to as a "second" had to be increased by 4%. No matter how strong by the basis for these changes, they would raise a great deal of concern because of the effect they would have on everything else. Nothing may have changed about the actual state of things, but the way people describe that reality and their attitude towards it may need to be changed significantly. At some point the question is bound to be raised - should people change to using the new more accurate values, or should the old values be retained for the sake of stability?

This is the dilemma faced by taxonomy on a regular basis. On the one hand, taxonomy is a process of scientific investigation like any other, and our descriptions of things will inevitably change as our understanding of them improves. On the other hand, taxonomy does not exist as an end in itself, but provides as its results the basic units of communication for all other branches of biology. Recognising that what was thought to be two populations of a single species actually represent two completely separate species requires more than simply another entry in the checklist - it affects the way we deal with those populations. Do we need to revise their conservation priorities? When previous studies referred to the old collective species concept, which of the two species currently recognised was intended? Leme (2003) discussed the effects of changes in taxonomy on the conservation of Brazilian bromeliads, and highlighted the case of a 'rare' species of bromeliad that was suggested to be a synonym of another more widespread species. Should the rare taxon be maintained as a separate species because it would no longer be regarded as a conservation target if synonymised?

While change in concepts is almost always good when dealing with a scientific process, it does not automatically follow that it is advantageous when dealing with communication. Usually, it is - if the short-term disadvantages of losing old modes of communication are outweighed by the long-term advantages of adopting the new, then change remains the best option. The replacement of the telegraph by the telephone would have required a large investment of time and money, but the eventual outcome would have made it worth it. The dilemma is deciding when to make the investment.



A good example for taxonomy is the higher classification of birds. The most widely used system for classifying birds at present is the Wetmore system, established by Alexander Wetmore (the bloke in the photo above) in a series of publications between 1930 and 1960 (Wetmore, 1960). In the years since, continuing investigations into bird phylogeny have identified a number of inaccuracies in the Wetmore system (Hackett et al., 2008). Several of the taxa recognised by Wetmore, such as his 'Falconiformes' and 'Ciconiiformes', probably represent polyphyletic assemblages whose members have acquired similar adaptations to similar ecological niches rather than sharing an actual close evolutionary history. Despite the widespread recognition of these inaccuracies, many publications on birds such as field guides continue to use the Wetmore system. Why would they do so? Mainly because, as inaccurate as the Wetmore system may be, no strong competitor has yet taken its place. Even if the only reason for maintaining the status quo is simply that it is the status quo, most users are arguably better served by having a single widely-recognised system than a number of competing systems. Once a more accurate classification becomes more firmly established, a single wholesale change may be preferable to a series of cumulative changes. There may be other non-scientific factors involved too - even if storks and herons or grebes and divers are not actually each other's closest relatives, a certain appeal probably exists for field-guide authors in keeping these groups close together if they are the taxa most likely to be confused by bird-watchers.

In a recent post, I commented on the arguments for and against adoption of phylogenetic nomenclature, and ended up effectively arguing for a double standard. While adoption of phylogenetic nomenclature might be preferable from a theoretical basis, it may cause practical problems if researchers attempted to apply it to taxa whose phylogeny was not sufficiently well known. Similarly, in the bromeliad example referred to above, Leme (2003) recommended that even if doubts existed about the validity of an 'endangered' taxon, researchers should err on the side of maintaining its validity because otherwise they risked threatening its conservation status. From a theoretical perspective, Leme is completely wrong. Surely researchers should accept the result that their data indicates, whatever the practical consequences of that result might be? But from a more pragmatic point of view, is it responsible for researchers to ignore such consequences?

Ultimately, both these issues call for some sort of compromise. Change is a necessary consequence of improving knowledge, but change should arguably be instituted responsibly. Of course, no-one is going to ever agree about what counts as "responsible". That's the problem with compromise.

REFERENCES

Hackett, S. J., R. T. Kimball, S. Reddy, R. C. K. Bowie, E. L. Braun, M. J. Braun, J. L. Chojnowski, W. A. Cox, K.-L. Han, J. Harshman, C. J. Huddleston, B. D. Marks, K. J. Miglia, W. S. Moore, F. H. Sheldon, D. W. Steadman, C. C. Witt & T. Yuri. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763-1768.

Leme, E. M. C. 2003. Nominal extinction and the taxonomist's responsibility: the example of Bromeliaceae in Brazil. Taxon 52 (2): 299-302.

Wetmore, A. 1960. A classification for the birds of the world. Smithsonian Misc. Coll. 139 (11): 1-37.

Today's Best Article Title

Spotted in a Table of Contents alert:

Gounga, M. E., S.-Y. Xu & Z. Wang. 2008. Nutritional and microbiological evaluations of chocolate-coated Chinese chestnut (Castanea mollissima) fruit for commercial use. Journal of Zhejiang University - Science B 9 (9): 675-683.

Best lines from the abstract: "Chocolate coating significantly improved the nutritional value of chestnut....The combination of freeze-drying and chocolate-coating generally results in greater reductions on microbiological loads, extending shelf life of harvested chestnut for commercial application." I'm taking it for my health. Honest!

The Diversity of Slime Moulds



How could you not love an organism that manages to combine both slime and mould? Slime moulds are saprobic organisms (i.e. they gain their nutrients by breaking down dead organic matter) that spend most of their life cycle feeding as separate amoeboid cells or disaggregated plasmodium. However, when conditions become right all the cells or plasmodium near each other will stream together to form a fungus-like fruiting body that releases spores, as shown in the diagram above borrowed from here. Because slime moulds thus resemble protozoa for part of their life cycle but fungi at other times, they were an early protagonist in the destruction of the idea that all organisms could be divided between plants and animals. Slime moulds, it turns out, are mostly not related to plants or animals. As our understanding of organismal phylogeny has progressed, it has become clear that not all slime moulds are even related to other slime moulds. Instead, the term has been used to cover a number of phylogenetically disparate organisms with little in common other than similar life cycles. However, the majority of references to slime moulds out there fail to mention this, focusing on only a small part of "slime mould" diversity, so I thought I'd give a brief overview of the full diversity of organisms with a slime mould-type life cycle.



1 - Myxogastrea: The plasmodial or acellular slime moulds, also known as Myxomycetes. This is the largest group of "slime moulds" - both in terms of number of species and the size reached by some species. While most other groups of slime moulds are fairly microscopic, myxogastreans reach sizes where they can easily be seen with the naked eye, at which point they are usually mistaken for fungi. During the feeding stage of their life cycle, myxogastreans form a plasmodium - a spreading mass that is not divided into individual cells, like threads of jelly or mucus (photo above from here). Recent phylogenetic analyses agree that myxogastreans belong to the Amoebozoa, the clade that includes more familiar amoeboids such as, well Amoeba (Cavalier-Smith et al., 2004). Indeed, the amoeboflagellate genus Hyperamoeba has been shown to represent a polyphyletic assortment of myxogastreans that have dropped the plasmodial habit.



2 - Dictyostelia: While myxogastreans may be the largest group of slime moulds, dictyostelians may be the most famous, because they take the standard coolness of the slime mould life cycle and turn the dial up to eleven. The photo above from here shows the various stages of the life cycle of the most famous dictyostelian, Dictyostelium discoideum. Dictyostelians are cellular slime moulds - while myxogastreans form a plasmodium, dictyostelians spend their nutritive phase as separate individual amoeboids. When the time comes for reproduction, the separate amoeboids swarm together to form a slug-shaped mass that actually moves as one, like something out of a Japanese cartoon. The dictyostelian slug crawls around until it finds a suitable location, at which point it extends outwards to form a sporangium on the end of a long thin stalk. The complexities of Dictyostelium's life cycle have made it a favoured study organism for such topics as kin selection, as researchers attempt to identify what cues incite slug formation, and why some individual amoeboids forming the sporangium stalk are seemingly willing to sacrifice their own reproductive potential in order to promote the reproduction of those cells forming the sporangium.

Phylogenetically, dictyostelians are also amoebozoans, closely related to myxogastreans. However, analyses are currently unable to resolve whether amoebozoan slime moulds share a single origin (forming a clade called Mycetozoa) or whether dictyostelians and myxogastreans independently originated from closely related but separate amoeboid ancestors.



3 - Protostelia: Three small families of slime moulds, the Protosteliidae, Cavosteliidae and Ceratiomyxidae, form a spreading nutritive phase similar to that of the Myxogastrea, and have often been regarded as closely related to the ultrastructurally similar myxogastreans. However, while myxogastreans form a truly acellular plasmodium, different protostelians form a pseudoplasmodium, with cells retaining their individual identity (Protosteliidae and Cavosteliidae), or a plasmodium that breaks up into individual cells before sporangium formation (Ceratiomyxidae). Ceratiomyxidae form small coral-like fruiting bodies - the photo above by Keisotyo shows a Ceratiomyxa species - while Protosteliidae form minute sporangia on slender stalks like dictyostelians. If mycetozoans form a single group, protostelians may represent a morphological connection between the cellular dictyostelians and the acellular myxogastreans. A relationship between protostelians and other mycetozoans was supported by Baldauf (1999), but the group remains little studied. The protostelians themselves are of doubtful monophyly, and some families may be closer to myxogastreans than others.

4 - Buddenbrockia: One parasitic animal was only recently identified as having a slime mould-like life cycle, with disassociated cells in its host aggregating together to give rise to a worm-like reproductive stage. The sordid details were covered in an earlier post.



5 - Acrasea: Acrasids are cellular slime moulds like dictyostelians, and indeed were once united with dictyostelians under the name of Acrasiomycetes. Like dictyostelians, acrasids live as individual amoeboids that aggregate together to form raised sporangia. The photo above from here shows the fruiting bodies of the best-known acrasid, Acrasis. However, acrasids are ultrastructurally distinct from dictyostelians, and are not even amoebozoans - rather, they belong to a protozoan group called Heterolobosea that also includes Naegleria, the organism that causes amoeboid meningitis, and belongs to the Excavata eukaryote superclade. Whether or not it was due to the mistaken assumption that acrasids were closely related to the intensely studied Dictyostelium, or whether it was due to the fact that acrasids seem to be most often found growing on animal poo, studies of acrasids are laughably rare, and only Acrasis rosea appears to have received any recent attention.

6 - Labyrinthulea: The slime nets are members of the Heterokonta, the clade also including brown and golden algae (among others), and have been covered before at this site - twice, in fact.

One protist group, the Phytomyxa or Plasmodiophoromycota, has often been included with the slime moulds due to its formation of a plasmodium for part of its life-cycle. However, phytomyxans, which are parasites of plant roots belonging to the Rhizaria (the eukaryote superclade including foraminiferans and radiolarians), do not seem to have an aggregative phase of the life-cycle comparable to other slime moulds. The best known phytomyxan is Plasmodiophora brassicae, the cause of club root in cabbages and other brassicas.



7 - Myxococcales: Finally comes a group that has never been regarded as slime moulds, but which has a very similar life cycle. The reason why Myxococcales have never been lumped with slime moulds is because they are not eukaryotes of any kind, but bacteria. Myxococcales are saprobic bacteria generally found in soil. They are capable of gliding motility, a form of movement by means other than flagella, though the exact mechanism remains little known. When nutrient supplies run low, some species of Myxococcales are capable of swarming together in a similar manner to cellular slime moulds and releasing dispersive spores. Myxococcales are therefore one of the few groups of bacteria to have developed multicellularity.

REFERENCES

Baldauf, S. L. 1999. A search for the origins of animals and fungi: comparing and combining molecular data. American Naturalist 154 (S4): 178-188.

Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40: 21-48.

Musical Interlude - International Paranoia Edition

I was listening to this track recently, and decided that it rather aptly summed up my current attitude to world politics:

Linnaeus' Legacy # 11 - Giant Head-sized Isopod Edition

A bumper-sized edition of Linnaeus' Legacy has splashed down at The Other 95%, and has certainly aggregated 95% of the links. This month's keywords: extremely risque, wild shores, Zoobank, biglebowski, two personalities, House of Lords, playful and irreverent, Bond, beetle family tree, algebraic geometry, common data network, sex = death, superorganisms, diversity of forms, giant clam, bivalves don't all look the same, hermits, conservation of whale lice, olive-backed forest robin, Honor an Invert, self-recognition, Wolfquest, that will rock, singing, biodiversity and limits. Also, a tribute to echinoderm researcher Cynthia Ahearn.

Hyphae without Nuclei: Filamentous Bacteria


Sporangia of Streptosporangium nondiastaticum. Image from Atlas of Actinomycetes.


Large size can have its advantages. Pound for pound, a large organism is often more energy-efficient than a small one. A larger organism may have an edge in competing for resources. Larger organisms may be less at risk from predation by other organisms. Therefore, it follows that even when life was a single-cell only affair, things would eventually get bigger. However, large size can also have its disadvantages. If we imagine (for the sake of argument) that the original single cells were roughly spherical, then increase in overall volume occurs much faster than overall surface area - exponentially faster, in fact. As the ratio of surface area to volume decreases, the efficiency of movement of nutrients and other other respiratory requirements into the cell and waste products out of the cell also decreases, until eventually a point is reached where it is no longer possible to move stuff in and out of the cell enough to meet the cell's requirements for survival. At this point, the organism essentially has only one of two options if it wishes (speaking metaphorically, of course) to keep growing. One is the option that our far-distant ancestors took - going multicellular, so that instead of being one large, inefficient sphere the organism can be many, more efficient spheres. The other option is arguably simpler - why stick to a sphere? Why not go filamentous? This week's highlight taxon belongs to one group of organisms that did just that - the bacterial family Streptosporangiaceae.

The filamentous option has actually been taken up by more clades of organisms than has true multicellularity. In an evolutionary sense, it's much easier - multicellular organisms require a host of measures to hold cells together and transport materials between them. Filamentous organisms, at the most basic level, simply need to grow along one geometrical axis faster than they grow along the others. Indeed, filamentous organisms rather blur the line between "multicellular" and "unicellular". Many of the larger filamentous organisms such as have cross-membranes dividing sections of hyphae, but they don't necessarily have to. Fungi and xenophyophores are both groups of organisms made up of masses of filaments, and is there any real reason other than comparative tradition for one to be regarded as multicellular and one as unicellular? (Does the concept of a "cell" even really apply when discussing hyphal organisms?) Bacteria are usually imagined as being unicellular, but many members of two bacterial groups, the cyanobacteria (blue-green algae) and the somewhat slime-mould-like Myxococcales, are multicellular for at least part of their life cycles. In contrast, the group of bacteria that made a go of the filamentous life-style was the Actinobacteria, the group to which the Streptosporangiaceae belong. Actinobacteria (or actinomycetes) include a diverse range of bacteria, both filamentous and not so (another subgroup of the Actinobacteria, the Corynebacterineae, has previously been covered here and here). Because of our shaky understanding of bacterial phylogenetics, it's difficult to say anything truly meaningful about the evolution of the filamentous habit in Actinobacteria, but it has most likely been lost and regained a number of times in the group. Some of the Actinobacteria have developed the hyphal habit to the extent that they are superficially ver similar to fungi, and indeed have been classified as such in the past.


Sporangia of Planomonospora alba. Image from Atlas of Actinomycetes.


The Streptosporangiaceae include some of the more mould-like actinobacteria. Like fungi, Streptosporangiaceae form branching, non-fragmenting hyphae. Most (but not all) members produce aerial mycelia, on the ends of which are produced the spores. Rather unusually among bacteria, the various genera can mostly be distinguished by morphological features related to the production of sporangia and arrangement of spores (Tamura et al., 2000), leading to many of them being give such names as Planomonospora or Microtetraspora. Planotetraspora, for instance, bears long, cylindrical sporangia containing four spores in a single row (Tamura & Sakane, 2004), while Acrocarpospora produces spherical or club-shaped sporangia containing coiled spore chains (Tamura et al., 2000). The distinctive appearance of Streptosporangiaceae also means that they are one of the few non-cyanobacterial prokaryote groups with an established fossil record, thanks to the description of Streptosporangiopsis from Cretaceous amber (Waggoner, 1994).

While widespread in soils around the world, the Streptosporangiaceae have often been regarded as rare compared to other groups. As methods of culturing them have improved, however, it has been suggested that Streptosporangiaceae are not so much rare as slow-growing. When soil samples are cultured in the laboratory, they are unable to compete with faster-growing taxa (Lazzarini et al., 2000), and their isolation requires the application of stressors that they can handle better than their competitors, such as heat-drying or chlorinating compounds. Despite the difficulty of culturing them, it has been suggested that doing so would be worthwhile - Streptosporangiaceae have proven a promising target in research into isolating new antibiotic compounds.

REFERENCES

Lazzarini, A., L. Cavaletti, G. Toppo & F. Marinelli. 2000. Rare genera of actinomycetes as potential producers of new antibiotics. Antonie van Leeuwenhoek 78 (3-4): 399-405.

Tamura, T., & S. Sakane. 2004. Planotetraspora silvatica sp. nov. and emended description of the genus Planotetraspora. International Journal of Systematic and Evolutionary Microbiology 54 (6): 2053-2056.

Tamura, T., S. Suzuki & K. Hatano. 2000. Acrocarpospora gen. nov., a new genus of the order Actinomycetales. International Journal of Systematic and Evolutionary Microbiology 50 (3): 1163-1171.

Waggoner, B. M. 1994. Fossil microorganisms from Upper Cretaceous amber of Mississippi. Review of Palaeobotany and Palynology 80 (1-2): 75-84.

Phylogenetic Nomenclature - Oui ou Non?

We may or may not be passing through a revolution in taxonomy. That's the problem with revolutions - it's often unclear whether one is happening or not until it is over, by which point (because humans have an incredible tendency to assume that the status has always been quo) it generally doesn't seem revolutionary any more. The subject in taxonomy that in recent years has caused a great deal of ink to be spilled and keyboards thumped is the question of phylogenetic nomenclature. I'd like to express a few of my thoughts on this subject today. I'm not going to try and actually solve the debate - I'm a pretty determined fence-sitter in this case, and in practice I tend to mix and match systems as circumstances require. Still, there are a number of misconceptions running about that keep rearing their heads, begging to beaten back down in an endless game of philosophical Whack-A-Mole. There are, I think, perfectly valid reasons why the concept of phylogenetic nomenclature is one that should be instituted with caution. It's just that, wierdly, these are not the "reasons" most commonly brought up.

First, some textbook cardboard. Our current taxonomic systems date their academic heritage back to Carl Linnaeus, who in his Systema Naturae adopted the concept of dividing organisms (and minerals) between hierarchically-nested categories, the "ranks" of class, order, genus and species, with the last two ranks together representing the individual name of a given species. As a result, the nomenclatural system most widely used today is generally referred to as the "Linnaean" or "rank-based" system. Through various circumlocutions, this system has given rise to our current codes of nomenclature, which all share two main priciples relevant to this post - taxa are divided between nested hierarchical ranks, and each ranked taxon has a type (genus or species) at a lower rank whose inclusion is a pre-requisite in defining the concept of that taxon. The Zoological Code only covers taxa up to the ranks of family and superfamily and does not regulate higher ranks, while the Botanical and Bacterial Codes cover taxa up to class (Bacterial) or phylum (Botanical) level. Beyond these basic pre-requisites, the Codes are actually quite free and easy. The Codes demand that a "family" must be a subset of an "order", and not the other way around, but there is absolutely no official guideline as to what degree of divergence constitutes an "order" or a "family". For instance, humans have been included by many systematists in a family Hominidae separate from the great apes in the family Pongidae. However, it is now widely accepted that some of the apes are actually more closely related to humans than to other apes - specifically, that chimpanzees and humans form a clade that excludes gorillas, while all three form a clade that excludes orangutans. Some authors have represented this change of concept by including great apes and humans in a single family Hominidae, with a subfamily Ponginae for the orangutan and Homininae for humans and African apes. Others would retain the family Pongidae for the orangutans only, while placing the remainder in the family Hominidae divided between the Gorillinae (gorillas) and Homininae (humans and chimpanzees). Still others might divide the chimpanzees in a separate subfamily from humans. The thing is that the current systems of nomenclature make absolutely no distinction between these various set-ups. All the available options satisfy the basic requirements - subfamily Homininae (if used) is a subset of family Hominidae, and Hominidae always includes the genus Homo. Beyond that, the only thing determining which option an author uses is their own personal judgement on how different a human is from a chimpanzee. Consider, also, the following figure from Baum et al. (1998) (click on it to see a larger figure):



This figure shows phylogenetic relationships within the "core Malvales", a clade of flowering plants previously divided between the families Malvaceae, Bombacaceae, Tiliaceae and Sterculiaceae, but for which all families except Malvaceae had turned out to be para- or polyphyletic. The figure shows four alternative methods of re-classifying the core Malvales in light of improved phylogenetic understanding. The point is that despite the siginificant differences in appearance between the alternative systems (recognising from one to nine families, two to nine subfamilies, etc.), there is actually no difference in the underlying phylogeny. Nevertheless, all four classifications are equally valid because all four meet the requirements of the rank-based system of nomenclature. Because there is no philosophical underpinning to what each "rank" means, the only guideline is a sense of tradition about what has been referred to a certain rank in the past - and because workers on different groups of organisms have different traditions, this is meaningless. As pointed out by David Marjanović in the comments at Tet Zoo, ranks can be (and, all too often, actually are) actively misleading because the temptation to assume that a "genus" of insects is somehow directly comparable to a "genus" of rodents has proven irresistible far too often in the past. Take another look at the Baum et al. figure above. Is "subfamily Malvoideae" in option C a less significant taxon than "family Tiliaceae" in option A?

Problems have also arisen in rank-based nomenclature because of the sheer number of ranks sometimes required. Kingdom, phylum, class, order, family, genus and species is easy enough to keep track of, but nowhere near enough to deal with the ten million or so species that infest this planet. Take something as boring and well-known as the common house sparrow, Passer domesticus. Passer domesticus belongs to the genus Passer, which is part of the family Passeridae, which belongs to the Passeroidea, part of the Eupasseri, part of the Passerida, part of the Euoscines, part of the Oscines, Eupasseres, Passeriformes, Anomalogonatae, Coronaves, Neoaves, Neognathae, Aves, Ornithurae, Ornithothoraces, Avialae, Eumaniraptora, Metornithes, Maniraptora, Maniraptoriformes, Coelurosauria, Neotetanurae, Tetanurae, Neotheropoda, Theropoda, Saurischia, Dinosauria, Ornithotarsi, Dinosauriformes, Ornithodira, Archosauria, Archosauriformes, Archosauromorpha, Sauria, Neodiapsida, Eosuchia, Diapsida, Eureptilia, Reptilia, Sauropsida, Amniota, Cotylosauria, Batrachosauria, Anthracosauria, Neostegalia, Tetrapoda, Tetrapodomorpha, Sarcopterygii, Osteichthyes, Teleostomi, Gnathostomata, Vertebrata, Craniata, Olfactores, Chordata, Deuterostomia, Eutriploblastica, Bilateria, Eumetazoa, Animalia, Holozoa, Opisthokonta, Unikonta, Eukaryota, Neomura. Try thinking up ranks for every one of that lot! Some pretty horrendous terms such as "supersubphylum" have been perpetrated in such attempts.

It is response to such issues that the concepts of phylogenetic nomenclature and rankless taxonomy arose. In phylogenetic nomenclature, a taxonomic name is defined in relation to an underlying phylogeny (Queiroz & Gaulthier, 1990). For instance, in my first example above, "Hominidae" may have been defined as the largest possible clade that includes humans (Homo) but not orangutans (Pongo). In that case, under the phylogeny given above, chimpanzees and gorillas must belong to Hominidae, while orangutans cannot. Ever. Concordant with the development of phylogenetic nomenclature has been the concept of a rankless taxonomic system. The two are generally assumed to be equivalent by many critics of phylogenetic nomenclature, but in fact they are not. Theoretically, it would be still be possible to erect a system of phylogenetic nomenclature that assigned ranks to the taxa it recognised. It would also be possible to devise a rankless taxonomic system that was not based on phylogeny but on, for instance, overall morphological similarity only. These options have not been considered because, quite simply, they would offer no advantage over the current rank-based system. A ranked phylogenetic system would have the same "too many ranks" problem of the current system, as well as problems all of its own devising if, e.g., conflicting definitions required that one "family" refer to a subset of another "family".

As an aside, I think it is also important to distinguish between the Codes of Nomenclature and the principles underlying their construction. While the rank-based system has its current codes, the (in)famous PhyloCode is in the process of being drafted to regulate phylogenetic nomenclature. The rank-based codes may have the same underlying principles, but they differ in their regulations as a result of different opinions on the most effective means of serving those principles. Similarly, whether or not the PhyloCode is adequate as a regulatory code is a separate issue from whether phylogenetic nomenclature is worthwhile as a concept.

It goes without saying that the concept of phylogenetic nomenclature has had its share of detractors, both on the front of phylogenetic nomenclature in the strict sense, and on the front of rank-free taxonomy. Of the two fronts, it is actually the first that is (in my opinion) the easiest to deal with. One of the main complaints about phylogenetic nomenclature is that it effectively eliminates the possibility of paraphyletic taxa. Take the classic example of Reptilia (reptiles), a paraphyletic "class" that actually includes the ancestors of another "class", Aves (birds). Under phylogenetic nomenclature, Reptilia must either include birds, or be abandoned as a taxon. Supporters of the rank-based systems may point at modern representatives of the two "classes" - lizards, crocodiles, birds - and argue that because crocodiles are more similar to lizards, despite being closer phylogenetically to birds, lizards and crocodiles represent a paraphyletic grade that merits official recognition. However, this ultimately comes down to a judgement call that the similarities between lizards and crocodiles are more "significant" than the similarities between crocodiles and birds. It is also largely an artifact of the extinction of taxa intermediate between the latter two. Would the division be regarded as being as "obvious" if ceratopsians had survived to the present? What about allosaurs? With any paraphyletic taxon, a point is reached where an arbitrary line has to be drawn that exagerrates the differences between taxa on either side of that line. What is so significant about the difference between Archaeopteryx and Microraptor that one should be placed in a separate "class" from the other?

Despite what might be expected, the idea of a rank-free classification is actually more problematic than paraphyly-free classification. This may make no sense at first glance, because the ranked system seems philosophically almost indefensible. The thing is that, ultimately, the appeal of the ranked system doesn't lie in its philosophical defensibility at all. Rather, the rank-based system has such a strong appeal because of its usefulness as an initial didactic and organising tool. Students find it much easier to gain and remember a quick understanding of the hierarchical relationships of taxa if they have a set of pegs to pin them on. Also, people find it helpful to have an "agreed" list of significant taxa. It is often claimed that the rank-based system is somehow more stable than the phylogenetic system, because change in phylogenetic understanding can supposedly lead to sweeping changes in the contents of phylogenetically-defined taxa. The problem is that this stability is nothing more than an illusion. Not only does it feed into the comparability error I referred to earlier, but the "agreed" list is all too often nowhere near as "agreed" as people think it is. Take Aydin Örstan's comment on the seemingly straightforward aim of seeing at least one member of every animal phylum:

But, first, I need to figure out how many animal phyla there are. However, that is not an as easy task as it seems. Wikipedia lists 36, the Animal Diversity Web lists 32 and the University of California Museum of Paleontology gives 25 extant animal phyla.


The phylogenetic system is indeed prone to change with changing phylogenies, but so is the rank-based system. What is more, as shown in the Hominidae and core Malvales examples above, there doesn't even need to be a change in phylogeny, only a change in an individual author's perception of the "significance" of differences.

Overall, I have (initially somewhat reluctantly) come to the conclusion that from a philosophical position, phylogenetic nomenclature knocks down the rank-based system without even breaking a sweat. This does not mean that we should all be rushing headlong to embrace PN - I said at the very beginning of this post that there is cause for caution. The primary handicap of phylogenetic nomenclature is simply that it requires a pretty good understanding of phylogeny (well, duh). For some groups of organisms, such as apes, we have extremely good understandings of their phylogeny. Yes, it is still possible that our views may change with increasing study, but it is extremely unlikely that, say, humans aren't closely related to apes at all but instead convergently evolved from a giant Mediterranean dormouse. For other groups of organisms, our phylogenetic understanding is more minimal. My own stomping ground, harvestmen of the superfamily Phalangioidea, represents a few thousand species of arthropod for which the classification remains almost entirely untested phylogenetically. Phalangioids are divided between a number of families, subfamilies and genera, yes, but all too often the boundaries between taxa frankly couldn't be vaguer if they had been drawn up in the back of a van by Cheech and Chong. Nevertheless, three thousand or so species is far too many to be assimilated in one hit, and the current rank-based system does allow us to break them up into a set of more manageable bits. Attempting to impose a phylogenetic classification onto phalangioids in our current state of knowledge would be a decidedly rash and hasty move, because there is no confidence that the sort of sweeping content changes that the phylogenetic nomenclature critics claim to fear wouldn't happen. A phylogenetic system for some groups of organisms remains more of a target than a current possibility.

REFERENCES

Baum, D. A., W. S. Anderson & R. Nyffeler. 1998. A durian by any other name: taxonomy and nomenclature of the core Malvales. Harvard Papers in Botany 3: 315-330.

Queiroz, K. de, & J. Gauthier. 1990. Phylogeny as a central principle in taxonomy: phylogenetic definitions of taxon names. Systematic Zoology 39 (4): 307-322.

Fleshy Farewells

Three recent arrivals on the carnival rounds:

For things wet and squashy, see Carnival of the Blue at The Saipan Blog.

For things green and hayfevery, see Berry Go Round at Not Exactly Rocket Science.

For things hard and sedimentary, see The Boneyard at When Pigs Fly Returns.

And a reminder that Linnaeus' Legacy posts need to be in by the day after tomorrow!

When Ferns Don't Look Like Ferns

I suspect that I would hardly need to explain to anyone what a fern looks like - their cool, green, graceful appearance makes them a favourite of holders of foliage fetishes everywhere. What you possibly may not be aware with is that the classic fern is actually only part of the story. Odds are that the parent of the fern you next see growing in a pot or in a damp grove looked nothing like that fern, and if you took the spores of that fern and grew them, you may not recognise the product. Welcome to the world of alternating generations.



Alternation of generations is actually something that all land plants indulge in. A diploid sporophyte asexually produces haploid spores that grow into haploid gametophytes whose haploid gametes fuse to form the zygotes that grows into new sporophytes, as shown in the diagram above by Jeffrey Finkelstein. In seed plants, the gametophyte has been severely reduced and does not grow outside its parent - the female gametophyte remains contained within the parent flower or cone as the ovule, while the male gametophyte is only a few cells in size and forms the pollen grain. In ferns, the gametophyte grows as a separate (albeit really small - perhaps only about a centimetre across) individual with an undifferentiated thallus. Each gametophyte produces both male and female gametes at different places on the thallus, and male gametes require a layer of moisture across the surface to swim across to the female gametes and fertilise them. Cross-fertilisation occurs when multiple gametophytes grow in close proximity and joined by a common covering of moisture. The sporophyte then grows directly out of the parent gametophyte.

In the majority of fern species, the gametophyte is a small heart-shaped structure like in the diagram above. The meristem, the growing part of the plant, is restricted to the recessed point of the heart. In three fern families, though, the gametophyte is ribbon-like or filamentous with multiple marginal meristems and grows indeterminately. While gametophytes of other fern families tend to be short-lived affairs, the gametophytes of Hymenophyllaceae, Vittariaceae and Grammitidaceae can be much longer-lived. Dassler and Farrar (1997) recorded an individual gametophyte of the Hymenophyllaceae species Callistopteris baueriana still growing seven years after germination. What is more, some inderminately-growing gametophytes are able to reproduce asexually as well as sexually through the production of gemmae, side-buds that can detach and grow into new individuals (anyone who has owned a hen-and-chickens fern or a mother-of-millions plants may have seen gemmae growing along the edge of their leaves). For a very few species, this capacity for sexual reproduction has allowed them to bypass the sporophyte phase of the life-cycle entirely.


The gametophyte-only fern species Vittaria appalachiana. Photo by Bob Klips.


Currently, independent gametophytes (i.e. those that are able to establish populations without forming sporophytes) are known from a single species of Grammitidaceae, two Vittariaceae and nine Hymenophyllaceae (Lindsay, 2003). Most of these species also produce sporophytes over part of the distribution, but the gametophytes are able to survive in areas that are seemingly not conducive to sporophyte production. Vittaria graminifolia, for instance, is known in Louisiana only as gametophytes, with the nearest sporophytes of the species over a thousand kilometres away in Mexico (Lindsay, 2003). As yet, only three species are known that seemingly never produce sporophytes - Vittaria appalachiana, Hymenophyllum tayloriae and Trichomanes intricatum (Raine et al., 1991; Farrar, 1992). Nevertheless, there are good reasons to suspect that the diversity of unrecognised independent gametophytes out there might be much higher. Fern gametophytes have been studied much less than sporophytes - not only are they small and difficult to find, but they have generally been regarded as decidedly low on taxonomically useful characters. Vittaria appalachiana, the first-known gametophyte-only species, was actually discovered sixty years before it was confirmed to be identifiably distinct from sporophyte-producing species of Vittaria. It does not escape notice that all three known gametophyte-only species come from the eastern United States, even though the families involved are found in tropical and subtropical habitats throughout the world. Things become particularly suspicious when you realise that a single person, Donald Farrar of Iowa State University, has been privy to the description of all three. More than likely, the apparent absence of gametophyte-only species from other parts of the world does not suggest that there is something unusual about the eastern United States, but simply that no-one has really looked anywhere else.

Like the relationship between asexually- and sexually-reproducing fungi, the taxonomic and ecological implications of the independent gametophyte may be significant. Rumsey et al. (1999) demonstrated that the Killarney fern (Trichomanes speciosum), previously regarded as extremely rare in the British Isles based on the distribution of the sporophyte, was actually fairly widespread and common as the gametophyte. The wide distribution of the eastern North American Trichomanes intricatum, including areas previously subject to glaciation and despite the apparent low dispersal potential of gametophytes reproducing by gemmae only, led Farrar (1992) to suggest that the "extinction" of the sporophyte form may have happened only recently. Has this species really forever lost the ability to produce sporophytes, or might a change of climate lead to the unfurling of a long-forgotten frond deep within the forests of New England?

REFERENCES

Dassler, C. L., & D. R. Farrar. 1997. Significance of form in fern gametophytes: Clonal, gemmiferous gametophytes of Callistopteris baueriana (Hymenophyllaceae). International Journal of Plant Sciences 158 (5): 622-639.

Farrar, D. R. 1992. Trichomanes intricatum: the independent Trichomanes gametophyte in the eastern United States. American Fern Journal 82 (2): 68-74.

Lindsay, S. 2003. Considerations for a revision of the fern family Vittariaceae for Flora Malesiana. Telopea 10 (1): 99-112.

Raine, C. A., D. R. Farrar & E. Sheffield. 1991. A new Hymenophyllum species in the Appalachians represented by independent gametophyte colonies. American Fern Journal 81 (4): 109-118.

Rumsey, F. J., J. C. Vogel, S. J. Russell, J. A. Barrett & M. Gibby. 1999. Population structure and conservation biology of the endangered fern Trichomanes speciosum Willd. (Hymenophyllaceae) at its northern distributional limit. Biological Journal of the Linnean Society 66 (3): 333-344.