Amaurobioidea: Rummaging through a Wastebasket

A representative of the strikingly-coloured Nicodamidae from Australia. Photo by Nick Monaghan. While such spiders were previously identified as Nicodamus bicolor, there are no less than 23 species in seven genera that have previously been included under that name.

One term that you may come across in discussions of phylogeny is the concept of a "wastebasket" taxon. As the name suggests, a wastebasket taxon is one into which authors tend to throw everything that they can't really deal with. Often, a wastebasket will include the members of a group that are relatively unspecialised, often primitive, and united less by their shared characters than their lack of distinct features to connect them to one or another of the specialised subgroups that the author may recognise within the parent group. Phalangodidae among short-legged harvestmen, Sylviidae among passerine birds and Perciformes among spiny-finned fishes are all examples of taxa that have become wastebaskets in the past. Some wastebasket taxa are explicitly established as such, like the 'Deuteromycota' that included asexual fungi before techniques were developed that made it significantly easier to relate asexual and sexual fungal taxa. More often, though, a taxon originally based on a certain combination of features will develop into a wastebasket over time as phylogenetic studies show that the original basis characters for that taxon represent plesiomorphies (ancestral characters). This week's highlight taxon, the spider superfamily Amaurobioidea, perhaps belongs to the latter group.


Tegenaria gigantea (Agelenidae). Photo from Wikipedia. Agelenids build funnel-shaped webs and are apparently often called some variant of "funnel spiders" in North America, but such names are likely to cause confusion here in Australia with a certain notorious mygalomorphs. Some species of Tegenaria such as the hobo spider are also known for being toxic, but nowhere near as toxic as the Australian funnel-web.

In an earlier post, I included a quick overview of basal spider phylogeny, going as far down as the clade Araneoclada that unites those spiders that have only a single pair of book lungs (ancestrally, at least - many families of Araneoclada have lost the book lungs entirely, or evolved tracheae in their place). Members of the Araneoclada are further divided between the Haplogynae and the Entelegynae, originally based on the presence (Entelegynae) or absence (Haplogynae) in females of paired copulatory ducts opening on a sclerotised plate called the epigyne. While the absence of such ducts in the Haplogynae is obviously a primitive character and no longer regarded as uniting them, the group has funnily enough been supported as monophyletic based on a number of other characters (except for a small number of 'haplogyne' taxa that are phylogenetically entelegynes) (Coddington & Levi, 1991). However, the Amaurobioidea belong to the Entelegynae, which is by far the larger of the two clades. Within the Entelegynae, the primary division was long based on whether or not a species possessed a cribellum, a plate-like structure among the spinnerets that bears hundreds of tiny silk-producing spigots. As these spigots exude silk simultaneously, the spider uses a specialised arrangement of bristles on the fourth pair of legs to weave them together to form a woolly thread (see here for a more detailed description). Because this woolly thread is composed of multiple tangled strands, it can effectively entangle prey such as small insects that get caught among the strands. Unfortunately, as knowledge of entelegyne spiders improved it became clear that possession of a cribellum did not define a phylogenetically coherent group. A number of cases were identified of pairs of taxa clearly related by other characters in which one taxon possessed a cribellum and the other did not. The eventual conclusion was that the cribellum was an ancestral character for the Entelegynae (as also supported by its presence in one haplogyne family, the Filistatidae) that had been lost on numerous occassions.


Ctenus floweri (Ctenidae), from Singapore. Photo by David Court. Ctenids are active hunters.

In general, the Amaurobioidea included cribellate spiders with unbranched abdominal median tracheae, as opposed to Dictynoidea with branched abdominal median tracheae (Coddington & Levi, 1991). Families that have been assigned to Amaurobioidea include (among others) Amaurobiidae, Agelenidae, Ctenidae, Amphinectidae and Nicodamidae, but relatively little unites these families. Most of them are generally ground-dwellers (which may explain the common name of one of the best-known members, the hobo spider Tegenaria agrestis). Many members build small sheet-webs, but others are active hunters. Both the characters referred to above have since been shown to represent plesiomorphies of larger clades, with the alternative conditions arising multiple times. The phylogenetic analysis of entelegyne spiders by Griswold et al. (1999) found the 'Amaurobioidea' to fall within a clade that was sister to the clade including the orb-weavers, but the same clade included the Dictynoidea and Lycosoidea (wolf spiders and such) nested within 'amaurobioids'. Indeed, not even the type family of Amaurobiidae was monophyletic, with some members closer to the lycosoids while others were closer to the agelenoids. The Amaurobioidea, it seems, was a bust.

Coming up - science and art, whether taxonomy is science, why family names are so awful, micro-spiders, and Parapseudoleptomesochrella almoravidensis.

REFERENCES

Coddington, J. A., & H. W. Levi. 1991. Systematics and evolution of spiders (Araneae). Annual Review of Ecology and Systematics 22: 565-592.

Griswold, C. E., J. A. Coddington, N. I. Platnick & R. R. Forster. 1999. Towards a phylogeny of entelegyne spiders (Araneae, Araneomorphae, Entelegynae). Journal of Arachnology 27: 53-63.

E Pluribus Unum

For many people, the name "Ernst Haeckel" is most associated with slightly dodgy illustrations of vertebrate embryos that have doomed his memmory to be quote-mined by people with an agenda to push for all eternity. For others, though, the epitome of Haeckel's work lies in the many spectacular illustrations of invertebrates and protozoa he produced in such works as his reports on the biological material collected by the HMS Challenger expedition, and his 1899-1904 Kunstformen der Natur ("Artforms in Nature"). With their awe-inspiring detail and spectacular presentation, the plates he produced are more than just technical illustrations, they are true works of art. Perhaps among the greatest of his productions were the plates of siphonophores, an example of which is shown above. Baroque tentacled horrors, they loom out of the page threatening to engulf Dunwich. I wouldn't be able to tell you whether Lovecraft had ever seen one of Haeckel's illustrations to inspire him in his descriptions of the twisted hybrid offspring of Yog-Sothoth, but the resemblance is uncanny.

Siphonophores are planktonic cnidarians (the group that includes corals and jellyfish), distantly related to hydras (a good online reference on siphonophores has been put together by Casey Dunn). The most familiar member of the group is Physalia, the Portuguese man of war (so-called because of a supposed resemblance to that form of ship), but on the whole Physalia is not very typical of the order. All siphonophores are colonial, in their way - incomplete budding leads to the production of a colony of generally large numbers of metabolically interconnected zooids that are developmentally homologous to the more independent polyps of other cnidarians. However, the individual zooids of siphonophores are each highly specialised for separate divided functions such as feeding, reproduction or motility, meaning that siphonophore zooids are incapable of living independently of the colony. Perhaps more than any other group of organisms, the siphonophores challenge the question of what defines an individual or a colony, which has led to their description as "superorganisms".

Siphonophores have been divided into three main groups, the Cystonectae, Physonectae and Calycophorae, but the phylogenetic analysis of Dunn et al. (2005) found calycophores to be nested within physonects, the two together forming a clade they named the Codonophora. Cystonects (which include Physalia) form the sister-group to the codonophores, and share a colony morphology characterised by a division between a terminal pneumatophore (float) and the siphosome, the region of the colony containing feeding and reproductive zooids coming off a central stalk (in Physalia the central stalk is relatively short, but other siphonophores will have exceedingly long colonies). In the "physonects", the pneumatophore and siphosome are separated by the nectosome, a region of generally bell-shaped zooids called nectophores specialised for motility. In the calycophores, the pneumatophore has been lost and the colony is composed of the nectosome and siphosome. The illustration at the top of the post represents the physonect Physophora hydrostatica - the pneumatophore is the bulb-shaped structure at the top, with the zooids of the nectosome between the pneumatophore and the tentacle-like structures representing the top of the siphosome. These latter structures are not actually tentacles (the tentacles are the filaments radiating from the siphosome) but palpons, zooids whose function remains unknown but has been suggested to be related to excretion or defense. Underneath the palpons are the gonophores, the reproductive zooids, with separate male and female forms (males and females may both be present in a single colony, or there may be colonies of separate sexes). The large funnels like the horn of an old gramophone are gastrozooids, the feeding individuals. The clubbed side-branches on the trailing tentacles are tentilla, and contain concentrations of nematocysts for capturing prey. Most codonophores (but not cystonects) also have shield-like gelatinous bracts protecting the siphosome. Cystonects also have structures called gonodendra, which are concentrations of gonophores, palpons and also specialised nectophores that can propel a detached gonodendron through the water. Many codonophores are bioluminescent - the bracts may contain luminescent cells, and at least one member of the genus Erenna has flashing red tentilla that probably function as lures. The Physonecta illustrated above has only one iteration of the siphosome, but in other forms (such as the one illustrated below in another Haeckel plate) the clusters of palpons, gastrozooids and gonophores may form iterative elements that repeat continuously down the growing stem.



Despite what can only be described as their inherent coolness, siphonophores as a group are poorly known. Like other planktonic cnidarians, their gelatinous structure makes them quite frail and difficult to collect. The entire colony may be only loosely connected by the slender stem, such as in the example just above. Some siphonophores reach spectacularly large sizes - species of Apolemia may be more than 30 m in length, yet only a few centimetres in diameter. Attempts to net such specimens using conventional means would be lucky to retrieve anything more than disassociated mush.

REFERENCES

Dunn, C. W., P. R. Pugh & S. H. D. Haddock. 2005. Molecular phylogenetics of the Siphonophora (Cnidaria), with implications for the evolution of functional specialization. Systematic Biology 54: 916-935.

Haeckel, E. 1899-1904. Kunstformen der Natur. Bibliographisches Institut: Leipzig & Wien.

Sacred Monkeys

Hanuman langurs - photo by Kamal Kumar Dua. Though identified on the source site as Semnopithecus entellus, this taxon has been divided between up to seven species in recent publications.

Todays' Taxon of the Week is the primate genus Semnopithecus. Once again, that's a sentence that's a bit easier to glibly write than it is to define. Semnopithecus includes the langurs, and together with the surelis (Presbytis) and leaf monkeys (Trachypithecus) forms a generally-accepted clade within the Colobinae, a group that also includes the colobus and odd-nosed monkeys and is characterised by a number of adaptations to a higher proportion of leaves in their diet than most other primate groups - most notably, a division of the enlarged stomach into an upper neutral region and a lower acid region, with leaves being broken down by fermenting bacteria in the upper region. Within the langur clade, however, there has been disagreement on the best way to treat the three subgroups taxonomically. Some authors have included all three groups in Presbytis, others have restricted Presbytis to the surelis and combined the langurs and leaf monkeys as Semnopithecus, while others have recognised three separate genera. Because this is purely a question of ranking and there doesn't seem to be any disagreement that langurs and leaf monkeys are more closely related to each other than either are to surelis, there is no "correct" answer here. For the purposes of this post, I'm going to treat langurs and leaf monkeys as two subgenera of Semnopithecus, for no reason whatsoever other than it allows me to cover both groups, though it is worth noting that the phylogenetic analysis of Osterholz et al. (2008) did not confirm the monophyly of Trachypithecus relative to Semnopithecus sensu stricto.

No consensus seems to exist on the number of species within Semnopithecus. The langurs may represent as little as one or as many as seven species, depending on how the various populations around the Indian subcontinent are divided up. The leaf monkeys are even worse - Trachypithecus is the largest generic grouping in the Colobinae, and includes more than ten species scattered through south-east Asia. Many leaf monkey populations are poorly studied and species boundaries within the group are often unclear. Osterholz et al. divided Trachypithecus into fifteen species in five species groups as apparently recognised by Groves (2001) (which I haven't read), one of which (the Semnopithecus vetulus group with two species found in Sri Lanka and southernmost India) they found to cluster polyphyletically within Semnopithecus sensu stricto and transferred into the latter genus as a result. The Trachypithecus pileatus group, found on the boundary between the Indian subcontinent and south-east Asia, clustered with Semnopithecus in analysis of mitochondrial DNA but with Trachypithecus in analysis of Y chromosome data, leading Osterholz et al. to suggest the possibility of ancient hybridisation in the origin of the group.


The golden langur (Trachypithecus geei). Photo from bhutanonline.net.

Most leaf monkeys live in small groups of about six to eighteen individuals (Brandon-Jones, 1984). Compared to some other primates, colobines apparently show relatively little social interaction among members of a troop (though still being fairly social compared to many other mammals, of course), which Brandon-Jones (1984) suggested may be an indirect consequence of their diet. Almost all colobines include a certain proportion of young leaves in their diet, but few can eat a significant amount of mature leaves. As this is fairly low-nutrition fare, colobines must spend a higher proportion of their time feeding than other primates, while the scattered distribution of young shoots requires individuals to spread themselves fairly thinly through a foraging site. Most colobines do eat fruit and other plant parts in addition to leaves, and langurs have a fairly varied diet that also includes such things as insects, roots, gum and sap. Indeed, langurs are noted for being able to readily stomach toxin-bearing foods such as Strychnos fruit that other herbivorous mammals would find inedible or even fatal. Langurs may be found in larger groups than leaf monkeys, with up to seventy individuals recorded in a troop (the largest size referred to by Brandon-Jones is a group of 120 individuals, though this may have been a temporary cluster of troops seeking water rather than a single troop). This may reflect their more varied diet, and/or it may reflect the fact that langurs are looked on favourably in most parts of India due to their supposed connection with the monkey god Hanuman (indeed, the name Semnopithecus means "sacred monkey") and are tolerated by humans or even actively encouraged and fed. Langur social structure varies significantly between different areas, possibly also as a result of food availability and population density. Like lions in Africa, langur troops are based on related females, with male offspring being evicted as they reach maturity, often forming nomadic all-male clusters. In some areas, breeding troops may include a number of mature males co-existing relatively peacefully, but in many areas most troops generally include only a single mature male. Also like lions, eviction of the incumbent male by another male in single-male areas is also often followed by the entering male killing any young already present in the troop in order to favour the raising of his own young. Interestingly, females who are pregnant at the time of takeover will engage in "pseudo-oestrus" behaviour - to completely anthropomorphise things, they fake sexual interest in order to induce the invading male to accept their offspring as his own. Production of young in all colobines often involves their being "shared around" between members of a troop, and females will often "borrow" and nurse the young of other females.

REFERENCES

Brandon-Jones, D. 1984. Colobus and leaf monkeys. In All the World’s Animals: Primates (D. Macdonald, ed.) pp. 102-113. Torstar Books: New York.

Groves, C. P. 2001. Primate Taxonomy. Smithsonian Institution Press: Washington.

Osterholz, M., L. Walter & C. Roos. 2008. Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups. BMC Evolutionary Biology 8: 58.

In Which I Reveal Just How Much of a Freak I Am

It's all there in the subtitle to this site. In the last few days I've decided to set myself a task that will probably be ridiculously time-confusing, gut-wrenchingly futile and will doubtless cause me to become even older before my time than I already am. But it's something that hasn't been done since 1923, and I think the time is ripe for it to be done again. I'm thinking of compiling an index for all described taxa of long-legged harvestmen. With a few thousand species involved, this is no small task.

But the thing is, and this is the freakish part, I actually really like nomenclature. Nomenclature is the specific part of the taxonomic process where the researcher sifts through the assortment of available names and works out which is the correct name to use for the organism sitting before them. It is important to distinguish the identification of the correct nomenclature from the identification of the organism itself - the nature of the specimen won't somehow magically change if the name attached to it does. Nomenclature is simply the system of labels that researchers have agreed to use in order to allow communication. As such, many people seem to regard the identification of the appropriate label as a somewhat arduous and uninspiring task, but personally I find it can be quite a lot of fun. As frustrating as past confusions can be, there is also something appealing in the challenge of sorting them out.

As a group, harvestmen have their share of nomenclatural challenges. I've just linked to my post on the mess that is Gagrella in which I just scratched the surface. There are no less than five taxa laying claim to the name Gagrella bispinosa as a result of its repeated use as a subspecific name. The oldest harvestman genus, Phalangium, was originally used by Linnaeus for pretty much any arachnid that wasn't a spider or a scorpion, leading to a fair number of homonyms spread between a number of orders. These are the sort of things I'd like to delve into for the next few years. Sure it's a big call, but if you can't be a little hubristic as a grad student, when can you be?

I's Been Ejucated, now I Can Haz Snails Pleez? Kthnx

The National Postgraduate Taxonomy Workshop has been and gone, and I arrived back late on Friday evening from a fun and very full week that definitely constituted time well spent. A full range of students was represented, working on taxa from algae to arthropods, myxosporeans to mosses, podocarps to Platypterygius, frogs to fungi. The presentations were exceedingly helpful, though by about midway through the week my head was feeling so crammed full of information that I feared that moving my head to quickly would cause my brain to slosh out from my ears. Highlights for me included getting a better understanding of what a Bayesian analysis actually does (something that, to be quite honest, I'd heretofore been a little fuzzy about), a very helpful presentation from the editor of one of the high-level Australian systematics journals on effective methods for presenting and processing article manuscripts and revisions, and discussion on the future of taxonomic research and how best to secure that future. As expected, the workshop was a fantastic resource in a time when formal taxonomic training has become something of a rarity, and I believe all the students involved were unanimous in urging that such workshops become a regular occurrence.

Cepaea nemoralis, a highly variable terrestrial snail that has long been a model organism in heredity studies. Image via Palaeos.

But now things must return to normality, and it being Monday it's time for a Taxon of the Week post. The last such post two weeks ago was on the fossil gastropod family Scoliostomatidae, and this week's highlight post continues with that gooey molluscan goodness with another group of gastropods, the Stylommatophora. While you may not be familiar with the name, Stylommatophora are actually the most instantly recognisable of all gastropod groups, for this is the group that includes the significant majority of land snails. Aydin Örstan has recently presented a series of posts discussing the difficulties of classing many gastropods (or other moisture-associated organisms for that matter) as "terrestrial" or "aquatic", so I should probably qualify that last statement by stressing that "land snails" here refers to fully terrestrialised taxa that do not have an aquatic component to their life cycle. The name "Stylommatophora" refers to what must be the second thing that any child learns about snails (after learning that they carry their house on their back), that their eyes are on the end of stalks. More than one group of stylommatophorans has reduced or lost the shell - these, of course, are the slugs and semi-slugs (yes, "semi-slug" is a valid term, though unfortunately, to the best of my knowledge "slugi" is not). Such shell loss has occured multiple times. The most influential classification of stylommatophorans was the 1900 classification by Pilsbry that divided them into three groups based on the anatomy of the excretory system, the Orthurethra, Sigmurethra and Heterurethra. Pilsbry regarded the orthurethran straight ureter as ancestral to the sigmurethran sigmoid ureter, but more recent molecular phylogenies have supported the reverse - orthurethrans are a monophyletic group within the paraphyletic "sigmurethrans", with the earliest division within the stylommatophorans being between the "achatinoid" and "non-achatinoid" clades (Wade et al., 2001, 2006). The Elasmognatha (≈Heterurethra) are a small group of two families, the shelled Succineidae and shell-less Athoracophoridae, whose status as a monophyletic group is well-supported but whose position relative to other stylommatophorans is not.


The giant African snail Achatina fulica, one of the largest terrestrial gastropods. Photo by Roberta Zimmerman. Introduced populations of Achatina snails (often imported for food) have become a serious problem in some parts of the world. Interestingly, snails are generally attracted to calcium, and chalk-based baits have often been used in their control. I once lived in a rather damp and disgusting house that had a problem with slugs crawling into the pantry through openings in the base. Once there they would invariably make a beeline direct for the flour. I still don't really know why.

This newer division into achatinoids and non-achatinoids does not appear to be well-supported morphologically, though non-achatinoids tend to have better developed copulatory organs than achatinoids. For instance, those families with members that inject each other with calcareous "love darts" are all non-achatinoids. However, it is debatable whether and to what to degree this represents phylogenetic versus functional considerations. All stylommatophorans are functional hermaphrodites, but mating behaviour differs between taxa that mate face-to-face and inseminate each other simultaneously or those in which one individual mounts the other and insemination may be simultaneous, sequential or unilateral. As well as only occurring in achatinoids, love-darting only occurs in face-to-face copulators - and all face-to-face copulators are non-achatinoids. The function of the love darts is poorly known, but studies in Helix aspersa have shown that they induce faster uptake of received sperm by the darted individual, and one of the leading suggestions is that they discourage reproductive "cheats" that attempt to donate sperm while not taking up their partner's. Such behaviour is really only a consideration in species that inseminate simultaneously, and while many achatinoids do have simultaneous insemination their shell-mounting behaviour may be less conducive to forcing reciprocity in sperm uptake (Davison et al., 2005).


Triboniophora graeffei, an athoracophorid slug. The large hole visible behind the head is the opening to the lung. Photo by Bill Rudman.

Their fully terrestrial habits (not to mention the absence of a shell in many species) mean that stylommatophorans have a much poorer fossil record than other gastropods, and their time of origin is a little doubtful. While Solem & Yochelson assigned some Carboniferous and Permian fossil snails to extant stylommatophoran families, this assignation is not well-supported and the next record of land snails is not until over 100 million years later in the Cretaceous (Wade et al., 2006). As discussed in the scoliostomatid post, the elucidation of relationships between Palaeozoic and later gastropods and distinguishing true relationships from convergences is generally a process fraught with difficulty.

REFERENCES

Davison, A., C. M. Wade, P. B. Mordan & S. Chiba. 2005. Sex and darts in slugs and snails (Mollusca: Gastropoda: Stylommatophora). Journal of Zoology 267 (4): 329-338.

Wade, C. M., P. B. Mordan & B. Clarke. 2001. A phylogeny of the land snails (Gastropoda: Pulmonata). Proceedings of the Royal Society of London Series B - Biological Sciences 268 (1465): 413-422.

Wade, C. M., P. B. Mordan & F. Naggs. 2006. Evolutionary relationships among the pulmonate land snails and slugs (Pulmonata, Stylommatophora). Biological Journal of the Linnean Society 87 (4): 593-610.

Snails Letting It All Hang Out

This week's highlight taxon is the Scoliostomatidae, a distinctive small family of six genera of Devonian gastropods. For those unfamiliar with geological stratigraphy, the Devonian was Very Long Ago. It was during the Devonian that plants started making a real go of it in the terrestrial environment (they had arrived there earlier, but had so far been very half-hearted about the whole thing), while it wasn't until towards the end of the Devonian that some fishy thing gave thought to the possibility of investing in some piggly-wiggly toes. Of course, as marine organisms, Scoliostomatidae lived in an environment that had been long stocked with everything it needed and could have quite happily ignored the development of terrestrialised upstarts. The family is only known from what is called the "Old World Realm", the section of Devonian geography that incorporated what is now Australia, Asia, Europe, western North America, and the Morocco-India fringe of Gondwana (eastern North America was then part of the separate Appalachian realm). These were tropical seas at the time, and the Scoliostomatidae would have been warm-water taxa.

The Scoliostomatidae weren't recognised as a family until 2002, even though Scoliostoma itself had first been described as far back as 1838 (Frýda et al., 2002). Members of the family share a unique morphology - while most of the shell grows as a standard conical shape, the very last whorl of the shell undergoes a drastic change in direction, growing outwards and backwards (and in the case of four genera forming the subfamily Scoliostomatinae, upwards as well) from the rest of the shell. The image at the top of this post (from Frýda et al., 2002) shows Pseudomitchellia macqueeni, an inch-long member of the Mitchelliinae, the other two genera of Scoliostomatidae distinguished from the Scoliostomatinae in that the last coil did not have an upwards curve. In the left-hand photo in particular you can see how the aperture is facing in the wrong direction. This has the minor side-effect of making scoliostomatids buck the trend for the usual means of distinguishing dextral and sinistral gastropod shells - even though the aperture appears at first glance to be on the left-hand side, examining the rest of the shell demonstrates that it is actually on the right.

Though their distinctive morphology clearly unites the Scoliostomatidae as a group, the relationships of the family to other gastropods are completely unknown. This is sadly not unusual among Palaeozoic gastropods, especially such early forms as this. There was a time when gastropods were classified according to large-scale features of the shell, but study of Recent taxa has shown that such features are prone to significant homoplasy and are usually indicative of ecology rather than phylogeny. Instead, gastropod classification is more reliably based on such things as internal anatomy and the morphology of the protoconch, the larval shell which is visible as a small morphologically distinct region at the very tip of the adult shell. Internal anatomy is of course not preserved in fossils beyond possibly such basic points as muscle attachment scars. The protoconch is much more useful in studying fossil shells, but its small size and delicate nature means that it often fails to be preserved, and the chance of preservation becomes significantly reduced the older the fossil is (just to make things even more difficult, some gastropods shed the protoconch when they reach maturity). Many (if not most) Palaeozoic-only families are simply too old for more than a minuscule chance of protoconch preservation.

What was the ecological significance of the uncoiled scoliostomatid shell? In Recent gastropod families showing a loss of standard coiling, such as the worm-like Vermetidae and Siliquariidae, the uncoiled shell is related to a sessile filter-feeding lifestyle. Similarly uncoiled gastropods were even more widespread in the Palaeozoic than they were afterwards, or at least included representatives of a more diverse array of families. Indeed, a greater diversity of filter-feeders compared to today was a characteristic of Palaeozoic marine faunas in general, their disappearance generally attributed to an increase in predation pressure with the appearance of faster and more active predators. For Scoliostomatidae, the displaced aperture means that the bulk of the animal would have no longer been in line with the centre of gravity for the shell, meaning that they would have also had reduced motility and would have probably been fairly sedentary. However, in most filter-feeding uncoiled gastropods the uncoiled whorls became irregular in their growth. Scoliostomatidae retained a well-defined growth form with the aperture close to the remainder of the shell. The lifestyle of scoliostomatids remains unknown. I am going to speculate here that scoliostomatids may have been semi-sessile soft-sediment-feeders (if only because I like the sound of the phrase). If the aperture is directed downwards, then the remainder of the shell lies more or less flat on the substrate. The edge of the aperture would have also been more or less flush with the substrate, offering quite effective protection.

REFERENCES

Frýda, J., R. B. Blodgett & A. C. Lenz. 2002. New Early Devonian gastropods from the families Crassimarginatidae (new family) and Scoliostomatidae (new family), Royal Creek area, Yukon Territory, Canada. Journal of Paleontology 76 (2): 246-255.

The Ugly Stick in Action

Psettodes erumei, as depicted by Sir Francis Day.

I had two things I could have written about this morning, both of them very cool. There's the identification of possible chloroplast-derived genes in ciliates, for one. This is very neat, because ciliates belong to a group of protozoans called alveolates that also includes dinoflagellates. Dinoflagellates have red-alga-derived chloroplasts that contain chlorophyll c, a form of chlorophyll otherwise only found in chromists, the group of algae that includes brown algae and their unicellular relatives. On this basis, it has been suggested that chromists and alveolates together form a superclade called chromalveolates (as opposed, I suppose, to alveomists). See the post I wrote earlier about the discovery of the rather significant little alga Chromera velia for more details. Ciliates have been something of a fly in the ointment for this theory, as they contain nary a trace of a chloroplast, which might support the alternative idea that dinoflagellate and chromist chloroplasts are independently derived. Monophyly of chromalveolates would require that ciliates are derived from chloroplast-carrying ancestors that lost their ability to photosynthesise, something that chloroplast-derived genes in ciliates would make more credible.

The other option to write on was the identification of stem-flatfish. I was leaning towards ciliates, because the stem-flatfish story has already been covered by Ed Yong, GrrlScientist and Carl Zimmer, but I can't access the ciliate paper. So I guess that flatfish it is.

Flatfish are the group that includes such creatures as flounders, sole and halibut. Fish are, of course, the animals that invented ugly. With contenders such as gulper eels, sculpins and dories in action, the title of World's Ugliest Fish is hotly contended. While flatfish are far from being the winners at ugly (that position is quite firmly held by the anglers), they definitely deserve an Honourable Mention.


Flatfish larval development, from Pharyngula.

At some point in their history, both eyes of the ancestral flatfish moved onto the one side of their head. The eyeless side of the body is used by the fish to lie flat on the substrate (hence the name), so left and right have effectively become upper and lower (in most species, right is upper and left is lower, but there are some exceptions). The really odd thing is that flatfish actually hatch out as fairly normal-looking larvae, with the eyes in their usual places on either side of the body, and over the course of maturation one of the eyes migrates over the top of the animal to the other side. How this state of affairs came into being has been a difficult question, and Goldschmidt actually gave flatfish a significant role in his arguments for saltatory evolution (evolution happening by a series of rapid jumps), a theory that has been parodied as the "hopeful monster" position. A paper in today's Nature (Friedman, 2008) adds some crucial data to the debate, as well as confirming that the change took place gradually.

Friedman (2008) establishes that the fossil fish genera Amphistium and Heteronectes show distinctly asymmetrical eye positions on the skull. While the eyes are still on separate sides of the head, one eye is positioned distinctly higher than the other. That these were fully developed adult fish rather than larvae with eyes in the process of moving is indicated by the complete ossification of the skull. Phylogenetic analysis supports the position of the two genera as fossil outgroups to living flatfishes, lying along the stem. This position is supported by characters other than those related to the asymmetry of the skull, so is unlikely to represent convergence. Because the specimens lack distortion in other elements of the skull, Friedman was also able to conclude that the asymmetry was not the effect of post-mortem distortion.

The idea of a gradual development of flatfish asymmetry actually already had support from the living genus Psettodes, generally agreed to the sister taxon to other living flatfish. In Psettodes, the migrating eye moves to the other side, but only as far as just below the dorsal edge. It is also notable that Psettodes apparently spends more time swimming upright than other flatfish. While most flatfish species show a distinct developmental preference for which side the eye migrates to, with opposite-sided individuals as relatively rare mutations, Psettodes individuals may experience eye movement to either side during development. Interestingly, a study by Schreiber, 2006, on larval development in southern flounder (Paralichthys lethostigma) found that while all wild-caught specimens were left-sided, 16% of larvae in the lab developed right-handedly, while 4% of larvae actually developed bilaterally symmetrically, with either the eyes remaining where they were or both moving dorsally. It seems likely that the failure to find such variants in the wild indicates that for some reason or other they do not generally live to adulthood.


From Friedman (2008).

Of course, the identification of these asymmetrical ancestral forms still leaves a lot of questions open. What we still don't know, of course, is why the ancestors of flatfish started lying on their sides, and why they became asymmetrical. The asymmetrical-but-not-one-sided forms Amphistium and Heteronectes are known from two stages of the Eocene, and were contemporary with more derived crown flatfishes, so they were not a short-lived maladaptive form that shuffled off as soon as their better-adapted descendants arrived. It has been suggested that the flattened habitus of flatfishes allows them to better conceal themselves while waiting for other fish as prey, which they are then able to ambush from below, and Amphistium, like living flatfish, does appear to be piscivorous. Side-resting fish may have been subject to selective pressure for eye asymmetry that allowed them to keep an eye out for prey while remaining concealed, and Friedman suggests (in comparison with modern flatfish behaviour) that Amphistium and Heteronectes may have been able to prop themselves up on their pectoral fins, raising the lower eye above the substrate and allowing them to 'squint' for prey. At the moment, of course, this is all speculative. From the aforementioned developmental studies (Schreiber, 2006), though, we can add some details. As well as having the eyes move sides, the larvae also change from swimming vertically to swimming laterally, but the two are independent events. Change in swimming orientation occurs before eye migration, and that small percentage of larvae that did not experience eye migration still changed swimming orientation. In a very small fraction of larvae, swimming orientation actually developed in the opposite direction to eye migration, so they ended up swimming with the eyes on the underside (needless to say, these unfortunate individuals did not live long). Further investigation of how asymmetry develops in living flatfishes - particularly the basal Psettodes - may shed further light on how this remarkable condition arose in the first place.

REFERENCES

Friedman, M. 2008. The evolutionary origin of flatfish asymmetry. Nature 454: 209-212.

Schreiber, A. M. 2006. Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish. Journal of Experimental Biology 209: 610-621.

Of Lions and Lace

The "non-green, green lacewing" (Catanach, 2007) Abachrysa eureka. Photo by M. C. Thomas.

There is a term that bird-spotters use to describe the ability to recognise what species a bird belongs to even if one cannot see the details of its features - they refer to the "jizz" of a bird, derived from the acronym GIS for "general impression and shape". The jizz of a bird species is not something that can be described easily, if at all - it is something that can really only be appreciated with experience. It should hardly come as a surprise that the same concept applies with identifying other organisms just as much as birds. Lacewings (Neuroptera) are a smallish order of insects (only about 5000 species) that include a diversity of forms, but many look at first glance not unlike small dragonflies. Still, a closer look will reveal significant differences to a dragonfly. For a start, lacewings have longer antennae and are able to fold their wings back over their abdomen in a way that no dragonfly can. There is also the feature that gives them their name - the wings of lacewings are particularly densely covered with veins, the little criss-crossing fluid-carrying lines that you can see on any insect wing. While you might need to look very closely indeed to see the individual veins, the cumulative effect of the dense veins is to give lacewing wings a distinctive shimmer, like light off satin, or the glimmer of colour across oil. This week's highlight taxon is a specific group of lacewings - the tribe Belonopterygini.

Lacewings have a complete metamorphosis, meaning they have a distinct larval stage separated by a dormant pupal stage from a very different-looking adult. Most lacewings start out life as formidable predators, and are quite recognisable by their large, protruding jaws. The most famous are the antlions of the family Myrmeleontidae, which dig themselves conical pits at the bottom of which they lie dug into the soil, waiting for any small insects unlucky enough to fall into the pit. While the large jaws are used for capturing and macerating prey, lacewing larvae are actually liquid feeders, injecting digestive saliva into their prey then sucking out the dissolved juices (Canard, 2007). One intriguing (yet kind of disgusting) feature of the order is that the midgut is not actually connected to the hindgut until pupation, meaning that the larva is not capable of defecation. Any indigestible waste products are stored in the gut until the lacewing reaches adulthood and passed after emerging from the pupa. Can you imagine the relief?


The belonopterygin Italochrysa insignis. This photo illustrates very well the distinctive shimmer that neuropteran wings possess in the right light and which I've found is actually one of the quickest ways to recognise an adult lacewing. Photo by Sheila.

Belonopterygini are a cosmopolitan tribe of a different family, the Chrysopidae (green lacewings), whose larvae are active hunters, many of them of economic significance as predators of plant pests such as aphids and thrips. Belonopterygin larvae are specialist associates of ant nests (Freitas & Penny, 2001), feeding on the ants therein. Unfortunately, such specialist habits make Belonopterygini one of the less-studied chrysopid groups, and I have been unable to find how the larvae evade detection by the ants. Like other chrysopids, belonopterygin larvae use small bits of soil and debris to disguise themselves, starting with the shell of the egg they hatched from (Catanach, 2007). Larvae of other chrysopids have been observed to incorporate the husks of drained prey into their trashy disguises so I would be interested to know if belonopterygins do the same, as has been described recently for assassin bugs.

Adult chrysopids may be predacious like the larvae, or they may feed on non-live food such as honeydew. Honeydew-feeding species possess diverticula in the gut that house symbiotic yeasts aiding the lacewing in digestion. Sounds produced by tapping the abdomen on the substrate are used by chrysopids in courtship, and the pattern of sounds produced may differ significantly between closely related species (New, 1991). Eggs are laid perched on the end of long silk threads.

REFERENCES

Canard, M. 2007. Natural food and feeding habits of lacewings. In Lacewings in the Crop Environment (P. McEwen, T. R. New & A. Whittington, eds.) pp. 116-129. Cambridge University Press.

Catanach, T. A. 2007. Abachrysa eureka (Banks) (Neuroptera: Chrysopidae): egg, first instar larva and biological notes. Unpublished thesis, Texas A & M University.

Freitas, S. de, & N. D. Penny. 2001. The green lacewings (Neuroptera: Chrysopidae) of Brazilian agro-ecosystems. Proceedings of the California Academy of Sciences 52: 245-395.

New, T. R. 1991. Neuroptera. In The Insects of Australia (CSIRO, ed.) pp. 525-542. Melbourne University Press.

Araneidae - With Web and With Scent

The St. Andrew's Cross (Argiope keyserlingi). Photo by Louise Docker.

The orb-weavers are undoubtedly the best-known of all spiders. Ask anyone to imagine a spider and they will probably picture an orb-weaver (they may also have transcribed the words "some pig" in the web). This is something of an unfair characterisation - of the more than 100 recognised families of spiders, less than ten are orb-weavers. Still, it is one of the orb-weaving genera that holds the name of "spider", Araneus, which, as the only generic name used in Clerck's (1757) Aranei Svecici, the only taxonomic work recognised by the ICZN that predates the 1758 tenth edition of Linnaeus' Systema Naturae, is officially the oldest generic name in zoological nomenclature*. That's right - spiders came before humans. Nyeh nyeh nyeh.

*Admittedly Clerck did use the name Araneus for all spiders, not just species included in the modern Araneus.

The Araneidae are the largest family of orb-weaving spiders, with a little less than 3000 described species. They are actually a lot more numerous than you might realise - many species build their webs only at night, taking them down in the morning before hiding during the day and rebuilding the web every evening. The family is decidedly diverse in appearance - from the gaudy colours and spines of the Christmas spiders to the idiosyncratic figures of the tailed spiders to one group whose common name describes their appearance perfectly - the bird-dropping spiders.



The classic orb-web is made by first floating a line of sticky silk horizontally across a space between two anhoring points (such as a pair of branches), then running a second looser non-sticky strand along the initial strand. The spider then drops herself* from the centre-point of the second strand, trailing a third strand behind her, so that the second and third strands form a Y-shape. The vertex of the Y will be the centre of the web. The spider next constructs an outer frame, as shown above in a diagram by Ed Nieuwenhuys (the page linked to has diagrams of each of the stages in orb-web construction), then runs a series of spokes from the centre of the web to the outside. She then runs a broad spiral of non-sticky thread from the centre of the web until she reaches the outer edge. After that, it travels back to the centre laying a much tighter spiral of sticky thread, removing the non-sticky scaffold as she goes. As the sticky thread is stretched, the sticky coating breaks into a series of globules of coiled thread, which is how the web is able to be so elastic and stand up to the thrashings of captured prey. The spider herself is able to move about without being trapped by means of secretions produced by glands near the mouth with which she coats her legs. Forster & Forster (1999) refer to an experiment where the tips of a spider's legs were dipped in solvent before the spider was returned to its web. The spider initially showed great difficulty in moving due to the removal of its protective coating, though it was able to renew the covering and regain mobility. After the web has been completed, the spider will take up residence at the central hub, legs resting on the radiating spokes in order to feel for any vibrations. Araneid eyesight is almost non-existent, and orb-weavers are incapable of hunting without a web. They are perhaps the closest thing to a terrestrial filter-feeder, filtering the air for small animals.

*All spiders are referred to as female unless proven otherwise, like ships and birds of prey. It's another one of those things that make the English language so damn confusing.


An unidentified member of the genus Gasteracantha. These spiders come in a dazzling array of colours and ornamentations, and unlike many other araneids are often visible during the day, earning them such names as "jewel spider" or "Christmas spider". Colour patterns can vary significantly even between members of the same species. Photo from here.

Many araneids may vary the basic orb-web design further. Ladder-web spiders, for instance, have a long narrow web instead of the usual circle. The function of these is not really understood, though it has been suggested as a specialisation for catching moths - moths have a covering of loose scales on their wings which would normally allow them to shake off a web and escape, but it is suggested that the elongate shape of a ladder-web means that as the moth shakes off its scales, it falls onto a lower part of the web until eventually it is no longer able to escape. Many orb-weavers construct a stabilimentum, a zig-zag ladder-shaped structure that extends upwards from the central hub. Again, despite being such a distinctive structure, the function of the stabilimentum remains largely unknown, though subject to intense debate - suggested roles include strengthening the web (the original source of the name), disguising the position of the spider from predators or making the spider look bigger, attracting prey or even making the web more visible for larger animals and so reducing the risk of them walking or flying through it. One large and striking araneid found here in Australia, the St. Andrew's cross (Argiope keyserlingi), shown at the top of this post, gets its name because it builds four stabilimenta radiating from the central hub, while the spider itself sits with the front two and rear two pairs of legs held alongside each other, so the spider itself forms the eponymous cross shape.

Perhaps the most remarkable thing about araneids, however, is that despite the total dependence of most species on their webs for survival, some species no longer make them. The aforementioned bird-dropping spider (Celaenia) is so-called because its lumpy brown-and-white-splotched abdomen really does look like a lump of bird poo, offering excellent camouflage from discerning predators. Instead of constructing a full web, Celaenia simply hang from a leaf or a thread with their legs outstreched. There they catch and feed on moths (excellent pictures of hunting Celaenia can be seen at Esperance Blog). It used to be a mystery how this seemingly limited and haphazard means of capture could possibly feed the spider (after all, how many moths could reasonably be expected to pass by one point over the course of a night) until it was observed that a surprising proportion of the moths being caught (that is, all of them) were males, and that, far from passing by the spider accidentally, male moths will actually approach the spider and remain close by it until caught. It seems that the spider actually emits pheromones that mimic those of a female moth, luring their prey in with the false promise of sexual gratification (like a Trojan virus attached to a spam e-mail). The bolas spiders of the tribe Mastophoreae have refined this process further - as well as producing attractive pheromones, they also dangle a single sticky thread below themselves. When a moth approaches close enough, the spider spins the sticky thread around in the air until it sticks to the moth and they are able to draw it in. How bird-dropping and bolas spiders make their living until they become large enough to handle moths seems a little confused - Brunet (1996) claims that Celaenia construct standard orb-webs until they reach maturity, while bolas spiders produce different pheromones for attracting different-sized moths when at different ages. Forster & Forster (1999) and Yeargan (1994), in contrast, both claim that Celaenia spiderlings produce pheromones to attract psychodid midges. Interestingly, while bird-dropping and bolas spiders are both members of the subfamily Araneinae, it is debatable whether they are each other's closest relatives within the subfamily (Yeargan, 1994), so it is possible that their amazing pheromone-capture techniques could have arisen separately of each other!

REFERENCES

Brunet, B. 1996. Spiderwatch: A Guide to Australian Spiders. Reed New Holland: Sydney.

Forster, R. R., L. M. Forster. 1999. Spiders of New Zealand and their Worldwide Kin. University of Otago Press: Dunedin (New Zealand), and Otago Museum: Dunedin.

Yeargan, K. V. 1994. Biology of bolas spiders. Annual Review of Entomology 39: 81-99.

Back to the Scleritome - Tommotiids Revealed!

Disarticulated mitral sclerites of Micrina xiaotanensis. Image from GeoScience World.

Back in January, I brought you Scleritome Week where I looked at a range of fossil organisms that were originally described from bits of disassociated external skeleton. Some of these were still of unknown live appearance, some had turned out once soft-body fossils were discovered to look very different from what anyone had imagined. One such group that I didn't cover (though I did refer to them in passing) was tommotiids. Tommotiids are part of the Cambrian assemblage of scleritome animals that may or may not be related to each other, and may or may not include basal lophotrochozoans (the clade that includes brachiopods, annelids and molluscs). Tommotiids in particular have been suggested to be related to brachiopods, with which they share a similar shell ultrastructure (Holmer et al., 2002). Until recently, no articulated tommotiid specimens had been found, but comparisons of tommotiid sclerites with those of Halkieria and Wiwaxia had led to suggested reconstructions of tommotiids as bilateral armoured slug-like animals. A new paper by Holmer et al. (in press, 2008) suggests a quite different image.

An articulated tommotiid scleritome was recently described by Skovsted et al. (2008), though frustratingly I don't have access to the paper. Far from the imagined bilateral slug, sclerites of the tommotiid Eccentrotheca were joined into an expanding tube-shaped structure. Skovsted et al. inferred that Eccentrotheca was a sessile, vermiform (worm-shaped) filter-feeder. Such an interpretation, they argued, fit well with the potential brachiozoan (brachiopod + phoronid) affinities of tommotiids, though Eccentrotheca may have been more similar in appearance to the worm-like phoronids rather than the brachiopods.

The reconstruction of Holmer et al. (2008) focuses on another tommotiid, Micrina, which is the most brachiopod-like of the tommotiids. Micrina possessed two types of sclerite, the smaller and flatter sellate and the larger, cap-shaped mitral. By comparison with Halkieria, Williams & Holmer (2002) suggested that the two sclerites could have been situated at either end of a slug-shaped animal. However, the revelation from Eccentrotheca that at least some tommotiids might be sessile suggested that this reconstruction should be re-examined.



The new reconstruction of Micrina from Holmer et al. (2008) is shown above in a figure from that paper. Rather than being a slug-like animal, Micrina is reconstructed as a sessile filter-feeder like Eccentrotheca. However, Micrina differs from Eccentrotheca in being cup-shaped rather than vermiform. What it does bear a distinct resemblance to is a basal brachiopod similar to the diagram I used in an earlier post, which are also sessile filter feeders attached to a substrate by a short pedicle. In contrast to brachiopods, the two valves of Micrina would not have been able to form a sealed chamber, but the shell ultrastructure of Micrina does suggest the presence of a fringe of setae that Holmer et al. suggest could have served a protective function. One potential issue with the reconstruction is that mitral valves are generally preserved in much greater numbers than sellate valves when the reconstruction suggests they should be equally abundant, but this may be a preservation artefact resulting from the smaller and lighter construction of the sellate valve.

A sessile reconstruction for tommotiids has interesting implications for the interpretation of other Cambrian scleritome animals. Halkieria was suggested as a stem-brachiopod by Conway Morris & Peel (1995), but this was debated by Vinther & Nielsen (2005) who interpreted Halkieria as closer to molluscs. While the sessile reconstruction of tommotiids does not entirely rule out a halkieriid ancestry for brachiozoans (one could still potentially argue that halkieriids were ancestral to a tommotiid + brachiozoan clade), it does make it significantly less likely. Conway Morris & Peel (1995) suggested that the two large subterminal sclerites at each end of Halkieria could have been brought into apposition to form the two valves of the brachiopod shell, but the sessile tommotiids suggest that the equal-sized valves of brachiopods could have been derived from an unequally-valved ancestor.

They are also interesting by way of analogy with the chancelloriids, those incredibly confusing Cambrian animals whose sclerite structure demands they be lophotrochozoans, but whose sessile habit and radial organisation screams non-bilaterian. While there is no reason to suggest an actual phylogenetic connection between tommotiids and chancelloriids, the presence of a sessile habit in the former, which are almost undeniably lophotrochozoans, suggests that the radial nature of the latter may not be so difficult to resolve with a lophotrochozoan ancestry after all.

REFERENCES

Conway Morris, S., & J. S. Peel. 1995. Articulated halkieriids from the lower Cambrian of North Greenland and their role in early protostome evolution. Philosophical Transactions of the Royal Society of London Series B – Biological Sciences 447: 305-358.

Holmer, L. E., C. B. Skovsted, G. A. Brock, J. L. Valentine & J. R. Paterson (in press, 2008) The Early Cambrian tommotiid Micrina, a sessile bivalved stem group brachiopod. Biology Letters.

Holmer, L. E., C. B. Skovsted & A. Williams. 2002. A stem group brachiopod from the Lower Cambrian: Support for a Micrina (halkieriid) ancestry. Palaeontology 45 (5): 875-882.

Skovsted, C. B., G. A. Brock, J. R. Paterson, L. E. Holmer & G. E. Budd. 2008. The scleritome of Eccentrotheca from the Lower Cambrian of South Australia: lophophorate affinities and implications for tommotiid phylogeny. Geology 36 (2): 171-174.

Vinther, J., & C. Nielsen. 2005. The Early Cambrian Halkieria is a mollusc. Zoologica Scripta 34: 81-89.

Williams, A., & L. E. Holmer. 2002. Shell structure and inferred growth, functions and affinities of the sclerites of the problematic Micrina. Palaeontology 45 (5): 845-873.

Bird Evolution - Problems with Science

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.

I'm afraid I'm going to be descending into cattiness for a moment later. I apologise in advance for any unwarranted snarkiness.

A paper (citation above) has appeared in today's edition of Science that adds to the ongoing debate on bird phylogeny. It is a fairly significant paper, giving the results of the largest molecular phylogenetic analysis to date for birds. As such, it largely supersedes the previous front-runner, the analysis of Ericson et al. (2006). However, most of the results of Hackett et al. (2008) are largely congruent with those from Ericson et al. (2006). So I'm a little bemused to read Chuck Hagner commenting that "What wasn’t expected was an apparent sister relationship between Passeriformes and Psittaciformes" and expressing surprise that Falconidae should cluster with that clade instead of with Accipitridae, when both these results had been reported in the 2006 paper. What is significant is that both these studies, conducted independently (no shared authors), found such similar results. Both studies (and the earlier Fain & Houde, 2004) found the same six major clades - Palaeognathae (ratites and tinamous), Galloanserae (gamebirds and waterfowl), Metaves (I'll explain in a minute), the "higher water-birds and allies" clade (including 'Ciconiiformes' and 'Pelecaniformes' intermixed), Charadriiformes and the "higher land-birds" (Passeriformes, Piciformes, Coraciiformes and allies).

Bird phylogeny as recovered by Hackett et al. (2008).

Metaves is one of the most controversial groupings of birds to have been proposed in recent years. It first made an appearance in a 2004 paper by Fain and Houde published in the journal Evolution. These authors coined the name Metaves for a clade containing nightjars, swifts and hummingbirds, pigeons and doves, sunbitterns, the kagu, mesites, tropicbirds and the hoatzin that was well-supported in an analysis of the β-fibrinogen gene. This clade was then completely unexpected - perviously, its members had been scattered among an assortment of other bird orders, and the only thing a number of them had previously had in common was that they had always looked a little out of place. In a message forwarded to the DML shortly after the publication of the 2004 paper, Peter Houde commented that the results had been so heterodox that it had been very difficult to get them published. The Charadriiformes, higher land-birds and higher water-birds together formed a clade that Fain and Houde dubbed "Coronaves". The Fain and Houde analysis did resolve the Charadriiformes and higher water-birds, but support was not great.

Ericson et al. (2006) increased the number of genes analysed to five, and again found the Metaves-Coronaves division of Fain & Houde (2004). They were also better able to resolve relationships within the major clades. However, the support for Metaves was completely reliant on the inclusion of the β-fibrinogen gene. If this gene was left out of the analysis, the clade collapsed.

Not too long after Ericson et al. (2006), a counter-sally from the morphological fort appeared in the form of the long-awaited Livezey & Zusi (2007) analysis. Using an awe-inspiring 2954 characters over 150 taxa, this morphological über-analysis bravely fought off the molecular novelties and called stridently for a return to more traditional relationships.

It is into this clash between the molecular data of Ericson et al. (2006) and the morphological data of Livezey & Zusi (2007) that Hackett et al. (2008) make their entrance. Hackett et al. increase the number of analysed genes to 19, and once again recover the much-maligned Metaves. Once again, though, the presence of this clade is dependent solely on the β-fibrinogen gene. The hoatzin abandons the Metaves and attaches itself to the base of the higher water-bird clade. I'm inclined to describe this as unsurprisingly surprising - once again, Opisthocomus is just being a prick. There seems to be a visible trail of respectability here - four years ago, Metaves had to fight its way for recognition in a respectable journal. With the publication of a paper supporting it in Science, it seems to have become a respectable hypothesis.

And that, really, is the source of my irritation. Nature and Science are widely regarded as the ultimate science journals, but it's difficult to escape the observation that many papers that appear in the two are, well, kind of crap. This is not the fault of the contributing authors, but results from the severe space restrictions on articles in these journals. At five very densely-written pages, Hackett et al. is a fairly long paper for Science, but the reader is left frustrated by the need to know about stuff that the authors were evidently forced to leave out. What happens when the analysis parameters change? If a given clade is collapsed, how does this affect the rest of the tree? Some of this is alluded to in the article, but there simply isn't the time for it to be explored properly. And was it lack of space that caused the authors to write clangers such as "flighted tinamous arose within the flightless Struthioniformes", which sounds to be suggesting that tinamous evolved or regained flight independently of other birds, rather than the far more likely scenario that flight was lost multiple times within the ratites? Nature and Science papers have been referred to as "extended abstracts" Sometimes, no matter how extended, an abstract just doesn't substitute for a paper.

Don't get me wrong, this is a very significant paper, and one that will provide a base-line for many future studies. It doesn't completely overthrow previous studies, but in the end that is exactly what is so fantastic about it - not that the results are completely unexpected, but that as more and more data is added, we can say more and more about the picture that has been developing over the past few years.

REFERENCES

Ericson, P. G. P., C. L. Anderson, T. Britton, A. Elzanowski, U. S. Johansson, M. Källersjö, J. I. Ohlson, T. J. Parsons, D. Zuccon & G. Mayr. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. Biology Letters 2 (4): 543-547.

Fain, M. G., & P. Houde. 2004. Parallel radiations in the primary clades of birds. Evolution 58 (11): 2558-2573.

Livezey, B. C., & R. L. Zusi. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zoological Journal of the Linnean Society 149 (1): 1-95.

Ceratopsids: A Cretaceous Flash in the Pan

Leptoceratops, one of the latest-surviving ceratopsians. Reconstruction from here.

After the previous post on ceratopsians, Zach Miller asked if I could follow up my basal-ceratopsian-focused post with one on the more famous ceratopsids, which for various reasons, most significantly time, I had rather neglected.

Sorry, Zach - this is not that post.

But what I thought I would elaborate on was something I referred to offhand in that post about the significance of the basal ceratopsians compared to the ceratopsids proper. I mentioned that the small bipedal ceratopsians, despite their relative obscurity, actually persisted in North America for just as long as the giant ceratopsids, and were with them 'til the end. I would like to add to this that as surprising as it may sound to any readers who are only familiar with popular presentations of evolution and their tragic tendency to fall into the "March of Evolution" trap, this actually wasn't much of an achievement. For even though ceratopsids are one of the iconic dinosaur groups, instantly recognisable by 95% of the developed world's population, they weren't actually around for very long.

Most of you will have probably heard of the Triassic, Jurassic and Cretaceous periods that together make up the Mesozoic era of earth's history. While these periods are quite sufficient for broad generalisations about the history of life, palaeontologists generally find that they need finer-scale divisions to refer to more specific time periods. I recommend going to Palaeos.com if you want to see the subdivisions for the Jurassic and Cretaceous, because I'm going to have to refer to a few of them in the course of this post. I know I'll be checking back there regularly as I write this post, because personally I can never keep track of them all.


Yinlong downsi, the earliest known ceratopsian. Reconstruction by Andrey Atuchin.

I mentioned in the previous post that the earliest ceratopsians are known from the Late Jurassic. Specifically, Yinlong downsi comes from the Oxfordian, which started about 161 mya (million years ago). (Taxon ages for this post have been taken from Justin Tweet's Thescelosaurus! website.) In the rough grade system I used in the previous post, Yinlong would be a psittacosaur-grade ceratopsian*, but phylogenetically speaking it is the sister taxon to later ceratopsians. The earliest and most basal known protoceratopoid-grade ceratopsian, Liaoceratops yanzigouensis, comes from early in the Cretaceous, some time between the Valanginian (starting about 140 mya) and the early Barremian (130 mya). The earliest known Ceratopsidae, in contrast, didn't crash the party until the mid-Campanian (perhaps about 78 mya). Ceratopsians had been around for about 80 million years already by the time the ceratopsids appeared. Or to put it another way, less time separates us from the latest ceratopsids than separates the ceratopsids from the earliest ceratopsians! With their extinction at the end of the Cretaceous, about 65 million years ago, the Ceratopsidae are only known to have been around for about 15 million years - an impressively long time by human standards, but really not so very impressive when compared to the nearly 100 million years of ceratopsian history, or the more than 180 million years the Mesozoic lasted for in total.

*You may be wondering how the psittacosaur-grade ceratopsians fared in terms of longevity. Psittacosaurus is the latest well-established psittacosaur, and seems to have survived until about the end of the Early Cretaceous, about 100 mya. However, the analysis of Butler et al.