Linnaeus and Shrubs

The new edition of the plant blog carnival Berry Go Round has sprouted at Watching the World Wake Up. Take a lot around that site while you're there, too - The Watcher (if that's his real name...) has a distinctive writing style that feels a bit like literary Jackson Pollock, but that I personally think is a lot of fun.

The next edition of Linnaeus' Legacy is coming soon, and is in fact being hosted by the founder of Berry Go Round, Laurent of Seeds Aside. So get your posts into him, me, or use the handy submission form.

The Mysterious Name of Queen Lestoros

The shrew-opossum Caenolestes fuliginosus. Photo from here.

Those of you who are familiar with the more encyclopaedically-arranged natural history books will almost certainly have encountered the phenomenon of the Mysterious Name. In the introductory section of the book, where the scope of the text is indicated, there'll be some sort of taxonomic listing - the phyla of animals, for instance, or the families of birds - with each of the taxa listing being described in a subsequent part of the book. But often, if you're the sort that will pore over such a listing closely enough, you'll notice that the listing includes at least one name, one taxon (often more) on which the remainder of the book is silent. It's there in the beginning, it has its place firmly indicated in the hierarchy - and then silence.

One taxon that throughout my youth remained to me a mysterious name was the Caenolestidae. Caenolestids are small South American marsupials, commonly known as shrew-opossums*. In most lists of marsupial families, they'll be near the beginning, after the true opossums of the Didelphidae. But all the books I read as a child would skip straight from Didelphidae to Dasyuridae, with nary a hint of anything in between.

*Another sign of their obscurity in the public eye - that they are only given the names of other animals, rather than being thought deserving of a name of their own.

Admittedly, the caenolestids are not a large family. Gardner (2005) lists just six species in three genera, Caenolestes, Lestoros and Rhyncholestes. Four of those species are in Caenolestes, the other two genera are regarded by Gardner as monotypic (though one effect of their understudied status is that no two authors will entirely agree on the caenolestid species list, and some authors may recognise two species in either or both of the smaller genera, while others will recognise only a single genus with as few as three species). Of course, that's still more species than other mammal families such as Rhinocerotidae or Hominidae that have no trouble claiming page space for themselves, and while caenolestids may be few in number now, they were more abundant in the past. Caenolestids were the most abundant small marsupials in South America during the early Miocene (Marshall, 1980).


Lestoros inca. Photo by Phil Myers.

Living caenolestids are widespread, and probably not particularly uncommon, but specimens are few and far between. This has mainly been blamed on their unobliging choice of habitat - they prefer very dense, humid forest, though they may be concentrated close to open meadows (Nowak, 1999). They are shrew-like in appearance (hence the common name), and females lack a pouch (presumably the young just hang directly onto the teats, but females with emerged young seem to have not yet been observed). The front of the lower jaw contains an elongate, procumbent pair of incisors, on which more in a moment.

The most detailed account of their behaviour comes from Kirsch & Waller (1979), who trapped and observed specimens of four caenolestid species. Though stomach contents indicate that the caenolestid diet is mostly invertebrates (Nowak, 1999), Kirsch and Waller found that specimens were most attracted to traps baited with meat, and when offered a choice between insects and meat, they would more readily take the latter. A male caenolestid offered newborn rats proved an efficient predator:

The animal would move toward a rat, sniffing vigorously, seize and lift the rat with its forepaws or pin it to the substrate, and bite it several times quickly with its incisors. The caenolestid would then commence eating the rat by biting off a section of the head with its cheek teeth and take successive bites posteriorly.

In fact, the large incisors were used rarely by caenolestids in feeding - almost all biting and chewing was done with the cheek teeth, and the incisors are primarily for dispatching prey. Caenolestids have a distinct flap on either side of the upper lip, and this probably protects the face and whiskers from getting clogged up with blood and dirt while the animal is busy stuffing prey towards the back of its mouth. When offered larger food items such as earthworms, the caenolestids would sit upright on their tails and use their front paws to manipulate their food, similar to the way a mouse does.


Skull of Caenolestes condorensis, so you can get a better look at those lower incisors which a such bad news if you're a baby mouse. Image from here.

Fossil caenolestids (or near-caenolestids, depending on your preferred classification) were ecologically more diverse than modern species, and a number appear to have been herbivorous. One such genus, the Miocene Abderites, had a large sharp and multi-grooved first molar like the teeth of the multituberculates. Marshall (1980), in the last major review of the fossil caenolestids, suggested that the arrival of the caviomorph rodents in South America was what triggered the demise of the caenolestid herbivores, while the more generalised insectivores/carnivores were able to keep sailing on.

Phylogenetically, caenolestids have been difficult. Perhaps the most honest representation of our current state of knowledge of marsupial phylogeny would be a trichotomy between the caenolestids, didelphids and australidelphians (Australian marsupials), with all possible relationships between these three having been suggested in the past. Some earlier authors suggested a relationship between caenolestids and the Australian diprotodont marsupials on the basis of the procumbent incisors, but this hypothesis was pretty firmly flattened when it was established that a different pair of incisors was involved in each of the two groups. Perhaps the most popular option at present is that caenolestids are the sister to australidelphians, to the exclusion of didelphids, as supported by some molecular data (Springer et al., 1998). However, a relationship between didelphids and caenolestids remains a distinct possibility due to the occurence in both of sperm pairing. After leaving the testes, sperm of members of these two families connect up to each other, forming a single moving pair (perhaps enabling them to swim faster through the uterus). However, the homology of this character is debatable, as the sperm connect in a different place in the different families.

REFERENCES

Gardner, A. L. 2005. Order Paucituberculata. In D. E. Wilson & D. M. Reeder (eds.) Mammal Species of the World: A taxonomic and geographic reference pp. 19-20. JHU Press.

Kirsch, J. A. W., & P. F. Waller. 1979. Notes on the trapping and behavior of the Caenolestidae (Marsupialia). Journal of Mammalogy 60 (2): 390-395.

Marshall, L. G. 1980. Systematics of the South American marsupial family Caenolestidae. Fieldiana: Geology, new series 5: 1-145.

Nowak, R. M. 1999. Walker's Mammals of the World, 6th ed. JHU Press.

Springer, M. S., M. Westerman, J. R. Kavanagh, A. Burk, M. O. Woodburne, D. J. Kao & C. Krajewski. 1998. The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole. Proceedings of the Royal Society of London Series B - Biological Sciences 265 (1413): 2381-2386.

Another Case of Mistaken Identity

Just the other day, Adam Yates showed us a couple of photos of a fossil that had been identified as dinosaurian, but actually belonged to a fish. Identifying isolated pieces of things can be a hazardous activity, and a mistaken identification can become something of a self-fulfilling prophecy - once the idea of a certain identity for your specimen has developed, you will tend to find "characters" that support your identification. Palaeontology, of course, presents researchers with no shortage of fragmentary remains, and it is not entirely surprising that a few snafus have occured. Adam referred to the case of Aachenosaurus multidens, a "hadrosaur" described in 1888 that was soon reidentified as a piece of petrified wood. A similar fate befell the "sauropod jaw" Succinodon putzeri (making the first four letters of the species name even more apropos). But while the most famous (and most dramatic) examples of such misidentifications involve fossils, studies of recent organisms have not been entirely free of impostors.



The figure above from Huys (2001) shows two views of the paratype of Megallecto thirioti, described by Gotto in 1986. The two specimens originally assigned to this species came from a plankton haul off the coast of Mauretania. Gotto identified them as parasitic copepods belonging to the family Splanchnotrophidae, and suggested that their hosts might be pteropods from the same haul.

Parasitic copepods can certainly be very strange creatures. While free-living males (and larvae of both sexes) may look like fairly ordinary copepods, the parasitic females may have highly derived morphologies that barely resemble crustaceans, let alone copepods. Consider the female of another splanchnotrophid, Arthurius elysiae (also from Huys, 2001):



When Huys (2001) revised the Splanchnotrophidae, however, he discovered that Gotto's Megallecto was (A) not a splanchnotrophid, and (B) not even a copepod. In fact:



'Megallecto' was nothing but a large chunk of the detached head of Phrosina semilunata, a pelagic amphipod. Phrosina belongs to a group of amphipods known as Hyperiidea. Most hyperiids feed on gelatinous plankton such as jellyfish or salps. They may or may not feed on pteropods.

REFERENCES

Huys, R. 2001. Splanchnotrophid systematics: A case of polyphyly and taxonomic myopia. Journal of Crustacean Biology 21 (1): 106-156.

Boobies

The northern gannet (Morus bassanus). Photo by Alan Wilson.

The Taxon of the Week post is a day late this week because, of course, yesterday was a public holiday here in Australia (as far as I can make it out, it seems a bunch of poms were so glad to see land after six months in a leaky boat [trying hard to keep afloat] that they've been celebrating ever since - the people already here may have had a different view of matters, but nobody ever asked them). Not only is it late, but it'll be short, too, because the Taxon of the Week is the Sulidae, which has been covered only recently by Darren Naish (here and here) with all the innuendo that is unavoidable when dealing with a group of birds going by the common name of "boobies" (though he did omit mentioning the close connection between boobies and shags).

The Sulidae are the boobies and gannets, a small but fairly cosmopolitan assortment of seabirds. Among the living sulids, the gannets form the genus Morus, and most boobies belong to the genus Sula. The exception is Abbott's booby (Papasula abbotti) which was originally included in Sula, and is still commonly referred to as such (at least in popular sources), but sits on the gannet rather than the booby side of the divergence between the two main genera (Friesen & Anderson, 1997). The distinctions between the three genera are not huge, and some authors in the past have referred to all living sulids as Sula. In the recent fauna there is a clear geographical division between gannets and boobies - Morus is found in the northern and southern temperate zones while Sula and Papasula are tropical or subtropical - but this does not appear to have always been so in the past. The Pliocene Pisco Formation of Peru has provided species assigned to both Sula and Morus (Stucchi & Urbina, 2004).


A sulid on the Galapagos Islands. This photo comes from here, where it is identified as a masked booby (Sula dactylatra). I don't think it is - the orange beak identifies it as a Nazca booby (Sula granti), a species that was only distinguished from S. dactylatra in 1998 (Pitman & Jehl, 1998). Don Roberson's site has a photo by Bob Pitman of the two species standing side by side to show the difference.

Eight fossil genera have been assigned to Sulidae (as well as fossil species of Sula and Morus*) - the Eocene Masillastega and Eostega, the Oligocene Empheresula, the Miocene Microsula (now a synonym of Morus), Miosula, Enkurosula and Sarmatosula, and the Pliocene Palaeosula and Ramphastosula. The Cretaceous Elopteryx did a stint as a close relative of the sulids, but is now regarded as a dinosaur of the Troodontidae and not even a bird (for most definitions of the word "bird"). Eostega lebedinskyi is known from a single mandible that was recently redescribed by Mlíkovský (2007), who reasserted its sulid nature (past authors have disagreed). Masillastega rectirostris is known from a skull from the famed Messel formation, and differs from living sulids in having a comparatively long beak (Mayr, 2002). It is also distinct in having seemingly inhabited a freshwater environment, while all modern species are exclusively marine. Mayr (2002) only tentatively regarded Masillastega as a sulid, and it may be a stem-member of the family (Mayr, 2005). Mlíkovský (2007) synonymised the two Eocene genera on the basis of a lack of significant differences between them.

*Apart from a single taxon described as a subspecies of the modern species (Papasula abbotti costelloi [ha ha]), there don't appear to be any fossil species assigned to Papasula. Considering the only recent distinction of Papasula from Sula, one wonders whether any fossils of the former are masquerading as the latter.

Empheresula arvernensis is represented by a pelvis from France (the original material also included a sternum, but Lambrecht later indicated that the sternum was not even sulid - Mlíkovský, 2002). The French Oligocene also provided Sula ronzoni, which, if correctly assigned (which seems to be debatable*), would suggest that the living sulid lineages had diverged by that point (Friesen & Anderson, 1997, used a molecular clock to estimate a divergence time for Sula vs. Morus/Papasula of 23 million years ago, which is also consistent with this, but the age calculation methods used by Friesen & Anderson can only be described as [ahem] dated). The European Miocene genera Enkurosula and Sarmatosula are both known from isolated humeri, and are both doubtfully distinct from Morus (Nelson, 2006; Olson, 1984, suggests that Microsula (=Enkurosula) pygmaea may be conspecific with the contemporaneous Microsula avita of Maryland in the United States, which has itself been since reassigned to Morus), as are the Californian genera Miosula and Palaeosula.

*I'm rather confused here. Nelson (2006) notes that Sula ronzoni has four notches on the sternum, and indicates that this would place it on the sulid stem. However, Mlíkovský (2002, 2007) states that the type material of S. ronzoni is an incomplete pelvis, so what is Nelson talking about?



The wierdest of all sulids, though, is the Pliocene Peruvian Pisco Formation's Ramphastosula ramirezi. The genus name means "toucan-booby" and is undeniably appropriate as Ramphastosula, instead of having a dagger-like straight beak like all other sulids, had a deep beak with a distinct arch as shown in the reconstruction above from Stucchi & Urbina (2004). The skull of Ramphastosula is also more robust than in other sulids, seemingly to support the enlarged beak. Ramphastosula was obviously pursuing a different lifestyle to other sulids, as it looks as if it would be ill-suited to catching fish by plunge-diving. Stucchi & Urbina (2004) suggest that its robust skull indicates greater diving ability than other sulids, so perhaps Ramphastosula was more inclined to pursue its prey underwater than its modern relatives. Unfortunately, no post-cranial material is known as yet for this species.

REFERENCES

Friesen, V. L., & D. J. Anderson. 1997. Phylogeny and evolution of the Sulidae (Aves: Pelecaniformes): a test of alternative modes of speciation. Molecular Phylogenetics and Evolution 7 (2): 252-260.

Mayr, G. 2002. A skull of a new pelecaniform bird from the Middle Eocene of Messel, Germany. Acta Palaeontologica Polonica 47 (3): 507-512.

Mayr, G. 2005. The Paleogene fossil record of birds in Europe. Biological Reviews 80: 515-542.

Mlíkovský, J. 2002. Cenozoic Birds of the World. Part 1: Europe. Ninox Press: Praha.

Mlíkovský, J. 2007. Taxonomic identity of Eostega lebedinskyi Lambrecht, 1929 (Aves) from the middle Eocene of Romania. Annalen des Naturhistorischen Museums in Wien 109A: 19-27.

Nelson, J. B. 2006. Pelicans, Cormorants, and Their Relatives: The Pelecaniformes. Oxford University Press.

Olson, S. L. 1984. A brief synopsis of the fossil birds from the Pamunkey River and other Tertiary marine deposits in Virginia. In Stratigraphy and Paleontology of the Outcropping Tertiary Beds in the Pamunkey River Region, Central Virginia Coastal Plain: Guidebook for the Atlantic Coastal Plain Geological Association 1984 field trip (L. W. Ward & K. Krafft, eds.) pp. 217-223. Atlantic Coast Plain Geological Association.

Pitman, R. L., & J. R. Jehl, Jr. 1998. Geographic variation and reassessment of species limits in the "masked" boobies of the eastern Pacific Ocean. Wilson Bulletin 110: 155-170.

Stucchi, M., & M. Urbina. 2004. Ramphastosula (Aves, Sulidae): a new genus from the early Pliocene of the Pisco. Journal of Vertebrate Paleontology 24 (4): 974–978.

Living Larvae and Fossil Fish

Marshall's macristium larva, from Rosen (1971).

Before anything else, a-few-days-belated birthday wishes to Tetrapod Zoology, which has now been going in one form or another for three years. Darren Naish, the author of Tetrapod Zoology, also notes that the number of palaeontology blogs being written that aren't afraid to be technical has increased significantly in recent times - "I don't know if it seems arrogant to think that Tet Zoo was a driving force behind this uber-nerd movement, but I like the idea that it was, so will stick with it". I don't know about other sites, but Darren Naish can pretty much take sole credit (or blame, whichever way you want to look at it) for inspiring yours truly to publish my own ramblings. Of course, I haven't Darren's ability, and I've never achieved his level of following (I'm still waiting for my invite to join ScienceBlogs ;-) ).

In my last post, I briefly alluded to the recent discovery that what have been thought to be three separate species of fish in three different families are, in fact, different life cycle stages (larva, adult male and adult female) of a single species. As remarkable as this discovery is, it can't be called completely incredible - it simply highlights just how little we know about many marine animals. In animals that undergo significant metamorphic changes over the course of development, it is not surprising that the connection between stages should not be initially recognised*. What really struck me about the affair were the low numbers of known specimens - of the three "families" involved, only 65 specimens of "Megalomycteridae" (the adult males) have ever been collected. "Mirapinnidae" (the larvae) are represented by only 120 specimens, while "Cetomimidae" (the adult females) tip the scales at about 600 specimens. To put that into a bit of perspective, the other day I was counting my way through a vial of harvestmen that included some 200 specimens from a single collection.

*Indeed, for those of you familiar with marine invertebrates, this is the reason behind the latin-derived terms for many invertebrate larvae - nauplius, cypris, cercaria. These forms were all initially described as distinct taxa, and after they were recognised as larvae of other taxa their past generic names persisted as terms for that stage in the life cycle.

Because Ed Yong at the link above has already done a bang-up job of explaining the cetomimid situation, I thought I'd dig into the vaults a little and bring up an earlier situation where a family of fish became written off as larvae - the Macristiidae.


Bathysaurus mollis. Photo from here.

"Macristium chavesi" was described by Regan in 1903 from a single specimen collected off the Azores in the North Atlantic (Rosen, 1971). It should be noted that "Macristium" was recognised from the start as a larval form, but supposedly of adults as yet unknown. Initially, Regan regarded Macristium as related to Bathysaurus, a genus of deep-water predatory fish currently in the Aulopiformes, but in 1911 he separated it as its own family that he suggested was related to the Alepocephalidae (other deep-water predators, but now in an entirely different order, the Osmeriformes). Regan's Macristium specimen was in dreadfully poor shape - the lower jaw was damaged, part of the upper jaw was lost entirely, and only one fin (a pectoral) had remained reasonably intact. A second macristiid specimen, in better condition, would not be recognised until 1961, when Marshall described a specimen collected by the ship 'Discovery' in the Bay of Biscay. Marshall's specimen was long and slender, with remarkably elongate fins. On the basis of the new specimen, Marshall reclassified Macristium once again, as a member of the Ctenothrissiformes.

Ctenothrissiformes is a small order of four genera known from England and Lebanon. The type genus, Ctenothrissa resembles Macristium in its elongate fins, but differs from it in being fairly deep-bodied. All three ctenothrissiform genera had one other significant difference from Macristium - they are known only from fossil deposits laid down in the Cretaceous (Patterson, 1964). If Macristium was indeed a member of the Ctenothrissiformes, it was a living survivor of a group long thought to be extinct. As it turned out, though, it was not to be. The relatively few features cited by Marshall as uniting Macristium and Ctenothrissiformes varied from the superficial (fin shape) to the non-existent (supposed similarities in jaw structure). When Berry and Robins described a third macristiid specimen from the Gulf of Mexico in 1967 as a new species, Macristiella lucens, they were sceptical of Marshall's interpretation.


Specimen of Bathytyphlops marionae. Photo from here.

The resolution of the macristiid mystery came in the early 1970s. A third specimen of Macristium was collected by the ship 'Chain' in the mid-Atlantic, allowing Rosen (1971) to convincingly relate it through various meristic characters such as vertebral count, anal position, etc. to members of what is now the order Aulopiformes, and specifically Bathysauridae. Specimens of "Macristiella" from the Pacific Ocean were identified by Okiyama (1972) as belonging to the genus Bathytyphlops in the Ipnopidae (also Aulopiformes). Finally, Johnson (1974) demonstrated using similar characters as in Regan (1971) that a specimen of Macristium from the Gulf of Mexico was assignable to the adult species Bathysaurus mollis. It is perhaps one of ichthyology's great ironies that Regan, as it turns out, had gotten it right in the first place.

As for the Ctenothrissiformes, it may not be a natural group even with the exclusion of Macristium. As indicated in Rosen (1971), while ctenothrissiforms are seemingly related to the modern acanthomorphs (spiny-finned fishes), the characters uniting them as a group are probably all primitive, and Patterson (1964) demonstrated that the genera show different mixtures of primitive and derived features for acanthomorphs. Rosen suggested a relationship to the Beryciformes, but certain features such as the absence of spines in the fins exclude Ctenothrissiformes from the Acanthomorpha (Patterson, 1964). Recent studies suggest that the "Beryciformes" may be a paraphyletic grade near the base of the acanthomorphs (Li et al., 1999), and perhaps the "Ctenothrissiformes" are themselves a paraphyletic outgroup to Acanthomorpha as a whole.


Part and counterpart fossils of Ctenothrissa from Lebanon. Photo from here.

Postscript: They sure don't write scientific articles like they used to. Hay (1903), writing in the American Naturalist, gave an introduction to the diversity of fossil fishes from the Cretaceous of Lebanon (including Ctenothrissa):

To the palæontologist the earth's crust, in its breadth and thickness, is a burial ground from which he may exhume the remains of the animals and plants that once lived on its surface or in its waters. The words of Bryant, spoken of the races of men, might truthfully be applied to other living things,

                     "All that tread
The globe are but a handful to the tribes
That slumber in its bosom."

But there are spots were the carcasses have been sown thicker and have been better preserved than elsewhere; and to such places the scientific birds of prey, who seek for, and must usually be satisfied with, fragmentary bones, and imprints of skeletons, and scattered scales and teeth, are gathered together; and, fed on such booty, they have visions of the swarms of animals, fat, sapid, and comely, that once populated the earth.

REFERENCES

Hay, O. P. 1903. Some remarks on the fossil fishes of Mount Lebanon, Syria. American Naturalist 37 (442): 685-695.

Johnson, R. K. 1974. A Macristium larva from the Gulf of Mexico with additional evidence for the synonymy of Macristium with Bathysaurus (Myctophiformes: Bathysauridae). Copeia 1974 (4): 973-977.

Okiyama, M. 1972. Morphology and identification of the young ipnopid, "Macristiella", from the tropical western Pacific. Japanese Journal of Ichthyology 19 (3): 145-153.

Patterson, C. 1964. A review of Mesozoic acanthopterygian fishes, with special reference to those of the English Chalk. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 247 (739): 213-482.

Rosen, D. E. 1971. The Macristiidae, a ctenothrissiform family based on juvenile and larval scopelomorph fishes. American Museum Novitates 2452: 1-22.

The Really Abominable Mystery

At the beginning of a post I wrote some time ago, I explained that it was written to feed a troll. I can't help feeling that if that one was feeding trolls, then this one will be kind of like spreading chum for them. Oh well. Before I start, though, I should note that Ed Yong has scooped some fascinating news involving whalefish. That has nothing to do with this post, but it is cool.


Saddleback caterpillar. Photo by Ross Hutchins.

One topic that both of my regular readers may have noticed I don't cover here that much is the creationist/intelligent design movement and supposed anti-evolution "arguments" (use of quotation marks entirely deliberate). One reason is that I have the good fortune to live in a country where the creationist movement is not currently (tap lignin) a serious issue. But the main reason is that these days, I find the whole thing to be so incredibly dull. Dull, dull, dull. The supposed arguments trotted out at every opportunity are just so hackneyed and unimaginative. The evolution of whales? The divide between man and monkey? Puh-lease! Since when have these trivialities ever been really worthwhile mysteries? I could probably give you four better enigmas before I even had time to pull my socks on. If you're going to insist on positing a God of the Gaps argument, then at least extend the poor block the consideration of giving him a decent-sized gap to run around in*.

*For some reason, as I wrote that I got the image of the aforementioned "gap" as something like a sort of cosmic rabbit hutch, with a bunch of onlookers exclaiming, "Oh look, a preternatural omnipotent deity! Isn't he just the cutest?"

So what are some of these great mysteries? Well, the origins of the nucleus, endoplasmic reticulum and Golgi apparatus in eukaryotes would have to be one. The development of the macronucleus and micronucleus in ciliates is probably another. But for my money, the biggest head-scratcher in evolutionary biology would have to be the origin of the holometabolous insect larva.


Nymph of the sandgroper (Cylindrachaeta), a hemimetabolous insect. Sandgropers are a type of burrowing Orthoptera. Photo from here.

Insect development can be characterised as ametabolous, hemimetabolous or holometabolous. Ametabolous development is the simplest. Among modern insects it is only found in a few basal wingless orders such as silverfish and bristletails, though one very early fossil group of winged insects, the Palaeodictyopteroidea (which I must describe in detail some day, because they're simply fantastic), seems to have had an ametabolous or near-ametabolous development. Ametabolous insects hatch out of the egg as pretty much miniature versions of the adults, and change little as they grow up. The next stage, hemimetabolous development, is found in insects such as dragonflies, grasshoppers and Hemiptera (true bugs). Hemimetabolous insects have distinct nymphal and adult stages, but they don't have a pupal stage between nymph and adult. Wings, in those species that have them, grow folded up in wing buds and are not extended until the final adult instar. It should be noted that there is not necessarily a clear dividing line between ametabolous and hemimetabolous development - in some hemimetabolous insects, such as grasshoppers, there may be relatively little morphological distinction between nymphs and adults except for some features such as wings. In others, such as some Hemiptera, the distinction between nymph and adult may be quite notable.

Holometabolous development, on the other hand, is an entirely distinct prospect. Holometabolous insects include moths and butterflies, flies, and beetles. In these taxa there is a distinct larval and adult phase. The larvae are soft-bodied and often vermiform (wormlike), and look completely different to the adults. While nymphs of hemimetabolous insects might develop wingbuds, holometabolous larvae possess not even a trace of visible wings. They may lack the appendages of the adult, and they may possess appendages of their own (such as the tendrils of some caterpillars) that are lost by the adult. Between the larval and adult stages is a non-feeding, usually immobile pupal stage, within which the insect undergoes a complete developmental overhaul before emerging as the adult.

Though holometabolous insects comprise the significant majority of modern taxa, they all fall within a single derived clade, the Holometabola, that probably appeared about the beginning of the Permian (Grimaldi & Engel, 2005). Phylogenetic bracketing indicates that they were derived from hemimetabolous ancestors, but how? How did such a significant change occur?


Larva of hoverflies (Syrphidae), commonly known as "rat-tailed maggots". The "tail" is a breathing tube, allowing the maggots to survive in anoxic environments by extending the tube to somewhere where oxygen is available. Photo from here.

One theory that was popular for some time was that the larval and pupal stages of holometabolans correspond to the nymphal stage of other insects. As I've already noted, many hemimetabolous insects also show significant differentiation between nymph and adult. There may be selective advantages to such differentiation, as the different stages may utilise different resources and not compete with each other. The holometabolous larva, it was suggested, was simply an exaggeration of this differentiation. However, the details of holometabolan metamorphosis refute this idea. In hemimetabolous nymphs, the cuticle is divided into sclerotised plates as in the adults. Holometabolan larvae in contrast, have a soft cuticle that is not divided into plates, and is ultrastructurally distinct from nymphal cuticle. During the pupal stage, collections of cells within the developing insect called imaginal discs proliferate and spread through the body, giving rise to adult organ systems such as eyes and wings, as well as the distinct adult cuticle divided into plates. Hemimetabolous nymphs have a fully developed nervous system much like that of their adults. In holometabolan larvae, the development of the nervous is halted at a rudimentary stage, and is not carried to completion until pupation. Even organ systems present in some form in the larva, such as the legs, may be partially or completely replaced by the products of imaginal discs during pupation, with little or nothing remaining of the larval tissue at maturity.

Recently, Truman & Riddiford (1999, 2002) have revitalised an earlier theory that holometabolan larvae actually correspond to the pronymph of hemimetabolous insects*. The pronymph is essentially the final stage of embryonic development. Pronymphs have an underdeveloped nervous system like holometabolan larvae, and an soft undivided cuticle with a similar ultrastructure to that of a larva. In some hemimetabolous insects, the pronymph molts through to the first nymphal instar prior to hatching from the egg. In others, the insect hatches while still in the pronymph stage. The pronymph does not feed in these taxa, but lives off its yolk reserves before moulting to a nymph within a few hours or few days. It may be motile - dragnoflies, for instance, are able to move from land to water as pronymphs. Pronymphs and holometabolan larvae also show high levels of JH, juvenile hormone. The role of JH in insects seems to be to retard development, so if an insect moults in the presence of high levels of JH the resulting instar will be much like the previous (Erezyilmaz, 2006). In hemimetabolous insects, levels of JH decline before the pronymph moults, allowing development of the nymph, but in holometabolous insects JH levels remain high until the final larval instar.

*The larva-as-pronymph theory is generally attributed to Berlese in 1913, but the idea that the larva was a sort of free-living embryo (a "crawling egg") was suggested by William Harvey in 1651, and its origins go all the way back to the writings of Aristotle in 322 BC (Erezyilmaz, 2006).



The figure above, from Truman & Riddiford (1999), shows suggested stages in the evolution of the holometabolan larva from the pronymph. Stages (a) and (b), as already noted, are both found in living hemimetabolous insects. The major step, which remains undocumented, would have been the evolution of the ability to feed in the pronymph, allowing maintenance of the pronymphal stage through more than one instar - stage (c) in the figure. Lengthening of the pronymphal stage seems to have been matched by a shortening of the nymphal stage, though again, the exact mechanics of this are as yet undocumented. It is possible that once the pronymphal stage became the main feeding and growing stage, then the multiple nymphal instars became fairly redundant, in which case there may have been a selective pressure for their rapid loss.



Eventually, we reach stage (d) - a single nymphal instar. This may be represented in the modern fauna by the Raphidioptera (snakeflies) and Megaloptera (dobsonflies). In these orders, the pupal stage remains mobile with well-developed legs (Grimaldi & Engel, 2005), as shown in the photo above of the pupa of Nigronia fasciatus (Megaloptera) (photo by Atilano Contreras-Ramos). The loss of mobility then leads to the fully-developed pupal stage. In some holometabolan insects, the imaginal discs don't develop until the end of the larval stage - (e) in the figure above - but in others - stage (f) - they develop early on and then remain quiescent until pupation. Examples are also known where development of adult tissues has been reactivated during the larval stage, such as the larviform reproductives of the beetle Micromalthus, perhaps by the development of localised resistance to the effects of JH.

If we were able to understand how the holometabolan larva evolved, it could have further interesting implications for our understanding of evolution. Morphological change in evolution is generally assumed to happen gradually, but researchers have suggested at least some situations where it could theoretically happen much more rapidly (I briefly described one such situation here. Such saltatory suggestions have been derided as "hopeful monster" scenarios, and are currently regarded with some skepticism. One of the main issues with the "hopeful monster" is that these deviant individuals would need to reproduce in order to successfully found a new lineage, and it might be difficult to find a willing mate if you look too unusual. However, when the holometabolous larva first evolved, it may have still developed into an adult that looked little different from its hemimetabolous ancestors. What would the implications of this be for the establishment of the new developmental pathway? Could the larval stage have spread through the population unhindered by questions of reproductive liabilities? Is this one situation where the hopeful monster might just have had a little more hope?

REFERENCES

Erezyilmaz, D. F. 2006. Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis. Integrative and Comparative Biology 46 (6): 795-807.

Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

Truman, J. W., & L. M. Riddiford. 1999. The origins of insect metamorphosis. Nature 401: 447-452.

Truman, J. W., & L. M. Riddiford. 2002. Endocrine insights into the evolution of metamorphosis in insects. Annual Review in Entomology 47: 467-500.

Forgotten Feather Stars

The Atlantic charitometrid Crinometra brevipinna. Photo by John E. Miller.

In earlier posts on this site, I've presented snippets of the diversity of fossil crinoids, so perhaps it was about time I finally worked up to the modern taxa. Today's Taxon of the Week is a family of feather stars, the Charitometridae.

Despite including the vast majority of modern species (and the best-studied of modern species), the feather stars (the order Comatulida) are in fact somewhat odd creatures within the main scope of crinoid historical diversity. The main point of oddness, of course, is their massively reduced stem (other strange features, which they share with other living crinoids, include the reduction of plating on the adoral side of the animal). When they first settle down from their free-swimming larval stage, feather stars are attached to the substrate by a stalk as in more typical crinoids, but before they reach maturity they once again break free. Technically, however, adult feather stars are not completely stemless - the proximalmost part of the stem is retained, and this becomes expanded and fused with the infrabasals (the lowermost ring of plates in the main body of the crinoid) to form the large basal plate known as the centrodorsal (Breimer, 1978a - it may seem odd to have something called the "centrodorsal" on the underside of the animal, but the thing is that, compared to other living echinoderms, crinoids are upside-down). The centrodorsal is the point of attachment for the cirri, tendril-like outgrowths of the underside. The cirri are used by the feather star for moving about, like something out of a Japanese cartoon.

Not that they necessarily do much moving about. Though feather stars are capable of a surprising amount of motility when the mood takes them (some even using their arms to become active swimmers), the mood does not often take them. Like their permanently attached ancestors, feather stars are still filter feeders, a lifestyle that is best achieved in a sedentary manner. Crinoids will only move if the local conditions become unfavourable, and then only as far as they must to find a more suitable location. Once there, they will fix themselves onto any available piece of substrate - Austin Clark provided a brief but disturbing description of the consequences of comatulids being denied a suitable attachment site (quoted in Breimer, 1978b):

If a dozen specimens of Antedon were thrown at night into a large basin of water and were left without any means of attachment they were all found dead in the morning, conglomerated at the bottom of the basin, clinging to each other with their cirri and having their arms intertwined in such a manner as to suggest the idea that they had died of the asphyxia produced by overcrowding after exhausting themselves in efforts to find suitable attachment...

Chondrometra robusta, a charitometrid from around the Philippines and Indonesia, with distinctly large cirri compared to other members of the family. Figure from Clark (1950).

The majority of studies on modern comatulids seem to relate to two families, the Antedonidae and Comasteridae - particularly the former. The Charitometridae, in contrast, have been much more neglected. As far as I can tell, they seem to have been pretty much untouched since being monographed in 1950 by Austin Clark, who recognised 32 species divided between eight genera, distributed pretty much world-wide but with the main centre of diversity in the Pacific (only a single genus, Crinometra, seems to have made it into the Atlantic*). Clark distinguished the Charitometridae from related families by the presence of distinct covering plates at the bases of the pinnules (the side-branches of the arms), by the lack of differentiation between pinnules at the bases and more distally on the arms, and by the relatively undifferentiated cirri. In general, Clark regarded the Charitometridae as a more generalised form than the closely related Thalassometridae, though of course in those pre-cladistic days its a little difficult to know exactly what he meant by this - whether or not he was actually saying that the charitometrids were ancestral to the thalassometrids, or whether he was just making a comparison.

*Clark recognised only a single species in this genus, Crinometra brevipinna, but a large number of varieties within that genus. Whether some of those varieties might be recognised as species were the genus to be revised, I couldn't say.

This lack of specialisation is perhaps part of the reason for the lack of study of charitometrids - Clark (1950) writes at length about the difficulties of distinguishing taxa within the family, and one gets the distinct impression that he was not particularly satisfied even with the system he himself ended up using. Even more of a factor, probably, is that charitometrids seem to be mostly inhabitants of deeper waters - Clark gives a depth range of 55 - 2194 metres. The ecology of the group, not surprisingly, seems to be completely untouched - we know that they're down there, but we don't really know what they're doing with their time.

REFERENCES

Breimer, A. 1978a. General morphology: recent crinoids. In Treatise on Invertebrate Paleontology pt. T. Echinodermata 2. Crinoidea (R. C. Moore & C. Teichert, eds.) vol. 1 pp. T9-T58. The Geological Society of America, Inc.: Boulder (Colorado), and The University of Kansas: Lawrence (Kansas).

Breimer, A. 1978b. Ecology of recent crinoids. In Treatise on Invertebrate Paleontology pt. T. Echinodermata 2. Crinoidea (R. C. Moore & C. Teichert, eds.) vol. 1 pp. T316-T330. The Geological Society of America, Inc.: Boulder (Colorado), and The University of Kansas: Lawrence (Kansas).

Clark, A. H. 1950. A monograph of the existing crinoids. Volume 1. The comatulids. Part 4c.-Superfamily Tropiometrida (the families Thalassometridae and Charitometridae). Bulletin of the United States National Museum 82 (4c): 1-383.

TAFKAMI Walks

Various individuals of the amoeboflagellate Breviata anathema. Note particularly the extended anterior and posterior pseudopodia on numbers 13, 14 and 18. Figure from Walker et al. (2006).

There's been a couple of really interesting things come through the pipeline lately. For this post, I'm not going to talk (yet) about yesterday's publication of an analysis of acanthodians that suggests that they are not a monophyletic grouping. If you want to know what that's all about, ask Adam Yates (and if you don't know what an acanthodian is, I've briefly discussed them previously). Today, I'm going to discuss another recent publication.

One of the first posts I wrote for this site (in fact, the sixth) was on an organism that I dubbed TAFKAMI, or The Amoeboid Formerly Known As Mastigamoeba invertens. This organism had been originally identified as 'Mastigamoeba invertens' when isolated in 1992, and was eventually properly described by Walker et al. (2006) as Breviata anathema* (the real Mastigamoeba invertens is known only from an undiagnostic description published in 1892, and, short of someone inventing a time machine so that they can look over its original describer's shoulder, will probably never be identifiable). Breviata is an amitochondriate, microaerobic amoeboid or amoeboflagellate (depending on life cycle stage). As explained in the previous post, Breviata has proven to be an obscenely difficult organism to place phylogenetically. Its position in phylogenetic analyses has been very unstable, and it jumps wildly about depending on the analysis parameters. The earliest division in eukaryotes appears to be between unikonts (animals, fungi and amoebozoans, which have a single flagellum with a single basal body) and bikonts (including plants, algae and excavates, with flagella in doublets or with double basal bodies), and it has not even been conclusively established whether Breviata is a unikont or a bikont. It has a single flagellum like a unikont, but two basal bodies attached to that flagellum like a bikont**, and sturdy branching filose pseudopodia like nothing else. Whatever its position, it seems likely that the divergence of Breviata from other eukaryotes happened not long after the the origin of crown eukaryotes in total.

*Tragically, Walker et al. (2006) gave no etymology for the new name. I have always wondered what exactly is so anathematic about Breviata anathema.

**Just to confuse matters, there are unikonts with double basal bodies, and bikonts with single flagella. However, bikonts with single flagella always retain two basal bodies. The anterior basal body in bikonts is always the younger of the two, and when the posterior basal body dies off the anterior body moves to the back and a new basal body grows in front of it. Those unikonts with two basal bodies still lack this distinctive growth pattern. Unfortunately, the flagellar growth pattern has not yet been studied for Breviata.

A new paper published by Minge et al. (2009) presents a new phylogenetic analysis incorporating Breviata anathema that draws on 17,283 nucleotide sites from no less than 78 genes (for contrast, the analysis of Breviata by Walker et al. used 1274 sites). The results of this analysis place Breviata with the amoebozoans, the clade including the majority of amoeboids with lobose pseudopodia. The support for this result is actually not too bad for this high a level of evolutionary divergence. Under certain analytical parameters, Breviata fell within other amoebozoans as sister to the other amitochondriate amoeboids Entamoeba and Mastigamoeba proper, but in the majority of cases it was the sister group to all other amoebozoans. This seems the more likely option as Breviata lacks certain sequence signatures (including a small insertion) characteristic of other Amoebozoa.

Sadly, as interesting as this result is, and as impressive as the amount of data used is, the analysis of Minge et al. (2009) suffers a fatal flaw. Though the analysis by Walker et al. did not give a conclusive result, the position they suggested to be most likely for Breviata was as sister to the Apusozoa. Apusozoans are a small group of flagellates with doubled flagella, and have been suggested to represent the basalmost divergence in the bikont lineage. As well as the double basal bodies, Apusozoa also produce filose pseudopodia like Breviata. Unfortunately, due to lack of data, the analysis by Minge et al. (2009) doesn't include a single apusozoan. While I'm personally sceptical of an apusozoan-Breviata relationship, I do think that without their inclusion the results of Minge et al. can't really be taken as conclusive.

Even if the phylogenetic results can't be entirely trusted, Minge et al. (2009) do have some interesting things to say. One of the interesting results from Walker et al. (2006) was the identification in Breviata of what appeared to be a hydrogenosome. Hydrogenosomes are hydrogen-processing organelles found in a number of anaerobic eukaryotes that have been shown to be altered mitochondria (Akhmanova et al., 1998). If Breviata did have a hydrogenosome, that would add to an increasing amount of evidence that all of the various 'amitochondriate' eukaryotes living today actually descend from ancestors that once had mitochondria (in contrast to previous opinions that they diverged from other eukaryotes prior to the origin of mitochondria). Among the genes possessed by Breviata, Minge et al. identify a number of genes derived from the pre-mitochondrial endosymbiont, confirming that Breviata's lack of mitochondria is a secondary feature.

Finally, there is the way Breviata moves. Amoeboids move, of course, by the extension of pseudopodia, but the exact method by which pseudopodia are produced can differ significantly between taxa. Indeed, in organisms with few permanent morphological features, the mode of pseudopodium formation has turned out to have a fair amount of phylogenetic significance (Smirnov et al., 2005). With its unique phylogenetic position, it seems only fitting that Breviata should have a unique mode of movement - it walks. A pseudopodium is protruded from the front of the cell and attached to the substrate. The rest of the cell body then rolls forward over the attached pseudopodium (like a tractor on treads, is Minge et al.'s analogy), until the pseudopodium is left trailing behind before being retracted and another pseudopod is extended from the front to repeat the process. No other organism has a mode of movement like Breviata - always twirling, twirling, twirling towards the future!

REFERENCES

Akhmanova, A., F. Voncken, T. van Alen, A. van Hoek, B. Boxma, G. Vogels, M. Veenhuis & J. H. P. Hackstein. 1998. A hydrogenosome with a genome. Nature 396: 527-528.

Minge, M. A., J. D. Silberman, R. J. S. Orr, T. Cavalier-Smith, K. Shalchian-Tabrizi, F. Burki, Å. Skjæveland & K. S. Jakobsen. 2009. Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proceedings of the Royal Society of London B 276: 597-604.

Smirnov, A., E. Nassonova, C. Berney, J. Fahrni, I. Bolivar & J. Pawlowski. 2005. Molecular phylogeny and classification of the lobose amoebae. Protist 156: 129-142.

Walker, G., J. B. Dacks & T. M. Embley. 2006. Ultrastructural description of Breviata anathema, n. gen., n. sp., the organism previously studied as "Mastigamoeba invertens". Journal of Eukaryotic Microbiology 53 (2): 65-78.

The Beautiful Angel of Death

If you're a tiny zooplanktic animal, that is.

This video was recently posted by Kevin Zelnio at Deep Sea News:



The animal shown in the video (swimming to music from Hayao Miyazaki's great ecofable Kaze no Tani no Naushikā [Nausicaa in the Valley of the Wind]) is the pelagic gastropod Clione limacina. Aquatic gastropods are usually members of the benthos, and relatively few groups have made the change to a pelagic lifestyle. Those that have are invariably freakishly bizarre:


Two species of the planktic nudibranch Glaucus (G. atlanticus on the left and G. marginatus on the right). Glaucus is a member of the Aeolidioidea, and like other aeolids it feeds on cnidarians (siphonophores and chondrophores in the case of Glaucus) and sequesters their stinging cells for its own defense. Photo by Gary Cobb.

Even the superficially more normal-looking (albeit attractively coloured) violet snails of the genus Janthina (also predators of planktic hydrozoans) make up for their unassuming appearance with their bohemian lifestyle, hanging upside down from a floating raft constructed from bubbles held together with mucus:


Janthina feeding on a Portuguese man-of-war, Physalia. Photo by Bill Rudman.

The sea angel Clione belongs to one of the larger groups of pelagic gastropods, the Gymnosomata. Together with another group, the Thecosomata, they have been classified into the Pteropoda, characterised by the adaptation of the foot into a pair of 'wings' for swimming. Recent authors have disagreed as to whether or not the pteropods form a monophyletic group (with probably the majority favouring "not"), or whether gymnosomates and thecosomates took to the seas independently, but pteropod monophyly was supported by Klussmann-Kolb & Dinapoli (2006). Pteropods have an interesting taxonomic history. When Cuvier first established the group in 1804, he regarded them not as gastropods but as a separate order in their own right. Pteropods seem to have been regarded as a link between gastropods and cephalopods, with some believing them closer to the latter than the former. Even after the modern pteropods were well-established to be gastropods, and 'Pteropoda' often abandoned as a formal category, the name maintained a strange shadow existence in palaeontology, with many Palaeozoic fossil problematica such as tentaculitoids, hyoliths or even conulariids (almost meaninglessly) regarded as or compared with "pteropods".

Within the pteropods, the most obvious difference between Gymnosomata and Thecosomata is that gymnosomates such as Clione completely lack a shell, while thecosomates retain one. And what incredible shells they are - the ultimate in lightweight, translucent construction, some thecosomates are ethereal constructions in blown glass:


Limacina helicina, photographed by Russ Hopcroft.

REFERENCES

Klussmann-Kolb, A., & A. Dinapoli. 2006. Systematic position of the pelagic Thecosomata and Gymnosomata within Opisthobranchia (Mollusca, Gastropoda) – revival of the Pteropoda. Journal of Zoological Systematics and Evolutionary Research 44 (2): 118-129.

In Which I am Defeated by Shells

The tiny Mediterranean marine snail Fossarus ambiguus. Photo by A. Piras.

I knew this day was coming. Every Monday I assign myself a random taxon to write a post on, and so far I've generally been pretty successful. But I always knew that some day I'd assign myself a target that would prove hopeless. That day has come.

The Fossarinae are a group of marine gastropods belonging to the superfamily Cerithioidea that also includes the famous gastropod radiation of Lake Tanganyika in Africa (which, now I think about it, would have probably been a much more promising post subject). As a rule, fossarines are pretty tiny - the best-known species, the Mediterranean Fossarus ambiguus, is only three to five millimetres in size - and they are usually short, squat shells with fairly prominent ribbing. Older references place the fossarines in their own family, Fossaridae, but they were placed in the Planaxidae as a subfamily by Kowalke (1998) (which I haven't read). Fossarines and other Planaxidae (Planaxinae) are fairly distinct in appearance (planaxines are longer and more turret-shaped) but they have similar protoconch morphologies and are both larval brooders. After fertilisation, the female does not lay eggs but incubates her embryos in a pouch behind the head, eventually releasing them as free veliger larvae. One individual of the possible (see later) fossarine Larinopsis turbinata held as many as 400 embryos in its brood pouch.

And that is pretty much it, as far as I've been able to find. And to be honest, most of that I lifted off one webpage. Research-wise, Fossarinae seem to have been almost criminally ignored. They don't seem to be particularly rare, and seem to be found pretty much worldwide, so I can only ascribe this to their small size and unassuming natures. Also, as a result of this lack of study, there seems to be an underlying implication that the subfamily is poorly defined and many of the taxa currently regarded as "fossarines" may not be so.


One of these doubtful fossarines is this rather neat little shell, Larinopsis ostensus (photo from here). The shell in the photo is the holotype of this species, collected off Jervis Bay in New South Wales, and still the only known specimen. Larinopsis is big for a fossarine (more than three times the size of Fossarus ambiguus) and lacks the prominent ribbing of most fossarines. It also has that very neat loosely coiled shell, so thin that you can see right through it.

Completely unrelated postscript: While looking stuff up for this, I made the mistake of looking into Finlay (1927). Why are old taxonomic works on molluscs always so horrendously painful to read? There seems to have been this great conspiracy among malacologist prior to, say, 1950 to only ever present the most turbid of prose, to never be explicit when they could possibly be obscure, and to never present explanatory details. For instance, they might state that "Species A is so obviously distinct from species B that I am creating a new genus C" without (a) giving any actual detailed description of these "obvious" differences, or even (b) stating whether it is species A or B that is to belong to this new genus. Take this all-too-typical example from Finlay (1927):

Phasianella huttoni Pilsbry, 1888

As already noted, Thiele includes Prisogaster in his subfamily Phasianellinae (which is better regarded as a family), with two other genera, Phasianella and Tricolia. For the latter, Humphrey's name Eutropia must be used, and the family name would become Eutropiidae, but the Neozelanic species does not belong to the genus Eutropia. Pilsbry has pointed out that the small Australian species have a radula of the Phasianellid style, not of the Tricolia (=Eutropia) form. Consequently one may propose for the Neozelanic species the new generic name, Pellax, associating with it the Australian rosea Angas, virgo, Angas, etc.

And that is all Finlay has to say about that particular genus. He continues in this manner for 159 pages (excluding references), establishing no less than 177 new taxa in the process. In some places, even a single page is enough to inspire thoughts of suicide in the suffering reader.

REFERENCES

Finlay, H. J. (1927). A further commentary on New Zealand molluscan systematics. Transactions and Proceedings of the New Zealand Institute 57: 320-485.

Kowalke, T. 1998. Bewertung protoconchmorphologischer Daten basaler Caenogastropoda (Cerithiimorpha und Littorinimorpha) hinsichtlich ihrer Systematik und Evolution von der Kreide bis rezent. Berliner geowiss. Abh. E, 27: 1–121, 11 Taf., 13 Abb.

Why Animals are not Plants

Orchids, from Ernst Haeckel's Kunstformen der Natur.

Before I start this post, I should note that this is simply a line of speculation I've had running through my head recently. I have no idea how accurate this is, or whether I'm just spouting a load of hooey. Either way, I think the question is an interesting one.

Why are there so many more species of animals than plants? More than 1.2 million species of animals have been described on this planet to date, as opposed to only about 300,000 species of plant. Even if one allows for differing species concepts, as yet undescribed species*, etc. there is no question of measuring error - animal species outnumber plant species more than four to one. Also, while most animal species tend to have clear distinctions from their closest relatives, plant species have a greater tendency to bleed into each other, with less clear boundaries (The same is also true of other non-animal eukaryotes and prokaryotes. Animals are the wierd ones in this regard). A comparison between animal and plant fossil records shows significant differences as well - even when they first arrived on land, plants never underwent an equivalent of the animals' Cambrian explosion. Plant evolution has been a far more sedate affair, with the divergences of the major modern taxa more spread out in time.

*Of which there are probably a higher proportion of animals than plants, anyway. Plants are generally easier to study in terms of biodiversity because they don't usually run away.

These points all suggest that speciation tends to happen differently for animals and plants. Why should this be? At least one major factor, I suspect, is that unlike most plants, most animals engage in active behaviour. Mobility is the key to the animals' evolutionary diversity. In most animals, reproduction happens through more or less direct copulation. As such, animals have a direct choice as regards whose gametes they fertilise or are fertilised by. Plants, in contrast, use more indirect means - wind pollination, or intermediary pollinators. As a result, their control over their fertilisation is more limited. Even in those species pollinated by insects and other animals, pollinator specialisation seems to play little part in speciation, and most pollinators are not hugely discriminating in their visits (Waser, 1998).


A diversity of cichlids at Dallas Aquarium. Photo by Tanya Dewey.

Speciation is the process of isolating gene pools. The differences between controlled fertilisation in animals versus more uncontrolled fertilisation in plants means that speciation in animals tends to be an active process, while that of plants tends to be a passive process. Changes in mate choice can lead to rapid speciation - for instance, they were probably a major factor in the evolution of the cichlid species flocks of the African Great Lakes*. For those organisms in which mate choice is not generally a factor, speciation is more likely to occur as a result of stochastic processes such as genetic drift. Isolating factors between species will develop with less frequency, and those barriers that do develop are likely to be less resilient.

*Lake Victoria is home to over three hundred endemic cichlid species, but sedimentary data indicate that the lake itself has only been there in its present incarnation for the last 12,000 years or so (Johnson et al., 1996). That implies the divergence of, on average, one new cichlid species every forty years.

As a test of this idea, one can look to those plants and animals that provide the exceptions proving the rules. In animals, many marine animals such as corals are broadcast spawners - they release gametes into the water and fertilisation occurs after the gametes leave the parent. Despite their worldwide distribution, corals are not a hugely speciose group of animals, with a little over two thousand known species. Or compare the diversity of the mostly broadcast-spawning bivalves (30,000 species) with the more often directly-fertilising gastropods (40,000 species).

Perhaps the most dramatic support comes from the orchids. While other flowering plants entice their fertilisers with food rewards such as nectar and pollen, orchids have developed more nefarious methods such as pseudocopulation or providing their pollinators with fragrant chemicals that the pollinators can use in their own mating displays. As a result, orchids are one group of plants for which direct mate choice is a significant factor, and speciation in orchids has boomed. Orchids include about 22,000 species, while their sister group, the remainder of the Asparagales, contains only about four thousand species all up.

REFERENCES

Johnson, T. C., C. A. Scholz, M. R. Talbot, K. Kelts, R. D. Ricketts, G. Ngobi, K. Beuning, I. Ssemmanda & J. W. McGill. 1996. Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273: 1091-1093.

Waser, N. M. 1998. Pollination, angiosperm speciation, and the nature of species boundaries. Oikos 82 (1): 198-201.

More Giant Larvae

Just a brief post - the air-conditioning in our office hasn't been working these past two days, I'm currently sitting in thirty degree-plus heat, and consequently I simply haven't the mental strength to compose anything more. Weather in Perth is evil.

I just thought that I'd show you something that I alluded to briefly nearly a year and a half ago in my post on Planctosphaera. This is the giant phoronid larva described by Temereva et al. (2006 - phoronids are small filter-feeding worms related to brachiopods), as illustrated in a figure from that paper:



For comparison, the animals to its right are more normal phoronid larvae (Actinotrocha is a form genus for such larvae, as it is not generally possible to identify a particular larva with its mature adult form). Phoronids are not the only marine animals for which such giant larvae have been found. If you've read the other post, you may recall that Planctosphaera was such an example. There's also the famed giant leptocephalus larvae, similar to the ten-centimetre (at most) leptocephalus larvae of eels or tarpons but reaching lengths of over six feet. Findings of giant larvae have lead to speculations about the existence of truly gigantic adults (particularly, it hardly needs saying, in the case of the leptocephali), but these adults remain as yet undiscovered. Many researchers suspect that giant larvae are not spawned from giant adults, but instead are pathological larvae of more normal-sized species that have failed to mature in the proper manner.

Even if the majority of giant larvae are merely abortive freaks, they are not without interesting implications for our understanding of evolution. Temereva et al.'s giant phoronid larva differed from other phoronid larvae in more than mere size. It also possessed a more fully developed circulatory system, as well as rudimentary gonads (which normally don't appear in phoronids until maturity). It takes little imagination to see the next step leading to a phoronid larva attaining full maturity while maintaining its larval form. It would not be the first known case - in 1928, Heath described Graffizoon lobatum, an animal very similar to the larva of a polyclad flatworm except for its possession of fully-developed gonads (as a reminder of our lack of familiarity with marine life, Graffizoon does not seem to have been recorded since).

For comparison, this is what adult phoronids look like (Phoronopsis viridis, from UCMP):



How difficult would it be to recognise the relationship between animals potentially only separated by a single generation?

REFERENCES

Heath, H. 1928. A sexually mature turbellarian resembling Müller's larva. Journal of Morphology and Physiology 45 (1): 187-207.

Temereva, E. N., V. V. Malakhov & A. N. Chernyshev. 2006. Giant actinotroch, a larva of Phoronida from the South China Sea: the giant larva phenomenon. Doklady Akademii Nauk 410 (5): 712-715 (transl. Doklady Biological Sciences 410: 410-413).

Linnaeus' Legacy # 15 - The Legacy Goes to the Congo and Gets Eaten

The latest edition of Linnaeus' Legacy is up at Greg Laden's Blog. This month's keywords: Not, a third of it is in Latin, now you get it for free, dahlias, something about the way, littlest sauropodomorph, martini, can of worms, Jocko, finches on mescaline, wench, tricks, oriole, parrots, bucket full of gasoline, extinction.

Next month's edition will be at Seeds Aside.

Kneel before the Shrimp Queen

A pair of commensal snapping shrimps Synalpheus on their host crinoid. Photo from here.

As a child, snapping shrimp were one of my favourite things to find under rocks at the beach. The characteristic bang made by their enlarged pincer snapping shut never fails to fascinate. This 'snap' can often be heard for some distance, and the explosive force generated by it can be strong enough to stun small animals that get too close. Snapping shrimp form the family Alpheidae, and Synalpheus, with well over a hundred described species and counting, is one of the larger genera in that family.

Synapheus has a pantropically-centred distribution. Though it seems to be more abundant in the east Pacific and Atlantic Oceans than in the Indian, I'd be a little suspicious of the role collection bias has played in this. The various species of Synalpheus are retiring animals by nature, and sequester themselves in cryptic habitats, all the better to defend themselves against would-be intruders with that impressive claw. The best-known species of Synalpheus live within the body cavity of other animals such as sponges or corals, and a few species live on the underside of crinoids (VandenSpiegel et al., 1998). It is debatable to what extent the relationship between Synalpheus and their host should be regarded as commensal (with the shrimp feeding on food particles brought in by the host) or parasitic (with the shrimp feeding directly on the host tissue), as evidence exists for Synalpheus individuals doing both. Dardeau (1984) suggested that Synalpheus species could be divided into three broad levels of host association, from group I (generally free-living or opportunistically commensal species with very low or no host specificity) to group III (invariably commensal species with high host specificity). Many commensal-living individuals will do so as male-female pairs, aggressively excluding any conspecific competitors that attempt to settle in their home. Other species may be more tolerant, with numerous individuals in a single host.


Colonial Synalpheus on a sponge. Photo from Biology-Blog - this would appear to be a laboratory colony, with dabs of identifying paint on the individuals.

The most remarkable association of all, though, is found in certain species of what is called the Gambarelloides species group (after the species Synalpheus gambarelloides). The Gambarelloides group is a morphologically distinct association of species (most notably, they have a dense brush of setae on the smaller pincer) that was separated by Ríos & Duffy (2007) from the remainder of Synalpheus as their new genus Zuzalpheus. This separation was debated by Anker & De Grave (2008), but the complaint does not seem to concern the integrity of 'Zuzalpheus' itself, but that of the remainder of Synalpheus if the Gambarelloides group species are not included. Some of the group III sponge-dwelling species in this group (using Dardeau's grouping) form large colonies with hundreds of individuals in a single sponge. It was only recognised as recently as 1996 (Duffy et al., 2000, 2002) that these Synalpheus colonies actually qualify as eusocial, in the manner of bees and ants, representing the only known occurrence of eusociality outside insects other than mole rats. Reproduction within the colony is conducted by a single queen, though it remains unknown how the queen of a colony is established, and how she prevents other members of the colony becoming reproductive. The sexual ratio of the remainder of the colony remains unknown, as males are indistinguishable from non-egg-bearing females (and gender may be environmentally-determined rather than genetic), but the colony does include a number of larger individuals (called "males" by Duffy et al., 2002) that seem to be primarily responsible for the colony's defense, moving about the sponge more than the smaller juveniles seemingly on the lookout for intruders. The queen plays little part in defending the colony, and in one eusocial species, Synalpheus filidigitus, she lacks the large snapping pincer of the other individuals (Duffy et al., 2002). It is not yet established how fertilisation of the queen occurs, but allozyme analysis suggests that there may be only a single reproductive male in the colony (Duffy et al., 2000).

Phylogenetic analysis of the Gambarelloides group by Duffy et al. (2000) found that eusociality has evolved at least three times within the group. They suggested that it may have evolved as a response to severe competition for habitat. Where eusocial shrimps are found, almost all suitable hosts are home to a colony, so unoccupied homes are few and far between (offhand, how new colonies do become established is yet another unknown factor - eusocial Synalpheus lack a planktonic larval stage, so hatching offspring remain in the parent colony). A colonial group may be more effective at defending their host against would-be usurpers than a solitary individual or pair would be. With the large "soldiers" defending her, the queen is able to spend more time feeding and reproducing, safely hidden within the sponge.

REFERENCES

Anker, A., & S. De Grave. 2008. Zuzalpheus Ríos and Duffy, 2007: a junior synonym of Synalpheus Bate, 1888 (Decapoda: Alpheidae). Journal of Crustacean Biology 28 (4): 735-740.

Dardeau, M. R. 1984. Synalpheus shrimps (Crustacea: Decapoda: Alpheidae). I. The Gambarelloides group, with a description of a new species. Memoirs of the Hourglass Cruises 7 (2): 1-125.

Duffy, J. E., C. L. Morrison & K. S. Macdonald. 2002. Colony defense and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behav. Ecol. Sociobiol. 51: 488-495.

Duffy, J. E., C. L. Morrison & R. Ríos. 2000. Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus). Evolution 54 (2): 503-516.

Ríos, R., & J. E. Duffy. 2007. A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuzalpheus, new genus, and six new species (Crustacea: Decapoda: Alpheidae). Zootaxa 1602: 1-89.

VandenSpiegel, D., I. Eeckhaut & M. Jangoux. 1998. Host selection by Synalpheus stimpsoni (De Man), an ectosymbiotic shrimp of comatulid crinoids, inferred by a field survey and laboratory experiments. Journal of Experimental Marine Biology and Ecology 225 (2): 185-196.