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.

Viruses upon viruses

Mimivirus. From Mimiviridae.

So, naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em;
And so proceed ad infinitum.

--Jonathan Swift, 1733, On Poetry, a Rhapsody

I've commented before on the hazards of making generalisations in biology, because no sooner do you think you've found a hard and fast rule than something comes along to break it. Seemingly basic questions have a way of becoming insanely difficult. Such as how do we decide whether or not something is alive? It may seem obvious at first glance - you may be fully confident that you yourself are alive, while the bloated gaseous corpse of a particularly unfortunate raccoon is most definitely not alive*. However, in making this argument you are glossing over the point that you are only considering extremes on the spectrum - as one gets closer and closer to the border between "alive" and "not alive", you may find it harder to confidently assign something to one or the other of your supposedly exclusive categories. Viruses have long been a classic example of such a difficult prospect. Viruses reproduce and disperse like more standard living organisms, but are generally regarded as not alive they do not do so independent of their host (but then, arguably neither do intracellular parasites such as Chlamydia and Microsporidia), and indeed they have to integrate themselves fully into their host's genome as part of doing so (which, admittedly, Chlamydia and Microsporidia do not). Is a virus alive or not alive? To what extent, if any, does it even make a difference?

*It's when I use phrases such as "bloated gaseous corpse" that it becomes obvious that I read way too much Mervyn Peake in my youth**.

**Not my misspent youth, I should point out. I tried to misspend it, but I don't think I ever really got the hang of misspending.

A few years ago, this still didn't seem like that much of an issue. Because viruses do not maintain a separate organismal identity throughout their reproductive cycle, it may be easier to imagine them as independently dispersing genetic fragments rather than discrete organisms in their own right. But then Mimivirus came along and, to use Scott Adams' phrase, demanded a "paradigm shift without a clutch". Mimivirus, a parasite of the amoebozoan Acanthamoeba, was the largest known virus to date when first described in 2003 (La Scola et al., 2003). So large is it that it is actually visible using an optical microscope and was apparently originally mistaken for a bacterium. When Mimivirus first infects its host, it releases its genetic material into the host cytoplasm. The viral DNA travels into the host nucleus (where it may or may not begin replicating) before travelling out again and inducing the formation of a separate "viral factory" that produces the progeny viruses (Suzan-Monti et al., 2007). However, with a genome of some 1.2 million base pairs, Mimivirus carries considerably more genetic material than many parasitic prokaryotes. It even carries genes to produce its own translation RNAs (Raoult et al., 2004). Phylogenetic analysis of the Mimivirus tRNA genes gave a position on the eukaryote stem outside the three standard domains of living organisms, leading to the implication that this might be some sort of surviving "progenote" (though I am personally skeptical - Mimivirus is different enough from prokaryotes and eukaryotes that even if the analysis is theoretically valid, long-branch effects are bound to be an issue). If Mimivirus is to be dismissed as not an organism in its own right, then it is as close to being one as one can possibly get, and trying to argue for either possibility carries a distressingly high risk of brain implosion.

A paper currently sitting in the advance online section of Nature (La Scola et al., in press 2008) carries the confusion even further. The authors of the paper were investigating a newly-discovered close but even larger relative of Mimivirus that they had dubbed Mamavirus in view of its size. In the process of doing so, they noticed a much smaller virus in association with Mamavirus that was eventually dubbed Sputnik. At first, Sputnik was assumed to be another Acanthamoeba pathogen, but further investigation established that Sputnik would only replicate in amoeboids that were also infected with mimivirids. In fact, Sputnik replicates in the mimivirid viral factories. Its presence is associated with the production of misformed mimivirids, and causes a 70% reduction in production of infectious Mimivirus. The conclusion of the researchers is unprecedented but almost inevitable - Sputnik is a virus that parasitises another virus.

Of course, it's not so simple and straightforward. Perhaps one could argue that Sputnik is not so much attacking the Mimivirus directly as hijacking the replicative framework produced by the amoebozoan host that the Mimivirus is inducing. But then, one could make similar (and perhaps similarly facetious) arguments about almost any case of hyperparasitism involving more unequivocal living organisms, or many other trophic relationships - if a lion kills a zebra then eats the zebra's stomach and intestines, is it eating the zebra or the grass ingested by the zebra? If there is one rule in biology, it is that life does not take kindly to clear-cut definitions.

More has been written on the Sputnik virus at Living the Scientific Life.

REFERENCES

La Scola, B., S. Audic, C. Robert, L. Jungang, X. de Lamballerie, M. Drancourt, R. Birtles, J.-M. Claverie & D. Raoult. 2003. A giant virus in amoebae. Science 299: 2033.

La Scola, B., C. Desnues, I. Pagnier, C. Robert, L. Barrassi, G. Fournous, M. Merchat, M. Suzan-Monti, P. Forterre, E. Koonin & D. Raoult (in press, 2008) The virophage as a unique parasite of the giant mimivirus. Nature.

Raoult, D., S. Audic, C. Robert, C. Abergel, P. Renesto, H. Ogata, B. La Scola, M. Suzan & J.-M. Claverie. 2004. The 1.2-megabase genome sequence of Mimivirus. Science 306: 1344-1350.

Suzan-Monti, M. B. La Scola, L. Barrassi, L. Espinosa & D. Raoult. 2007. Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS ONE 2(3): e328.

Linnaeus' Legacy #10: The Warbler Has Landed

Linnaeus' Legacy #10 is up at A DC Birding Blog. This month's keywords: a gull still looks like a gull, grammatical complexities, the first few billion years, gigantic ostracod, ticky land snail, specimens sitting in jars, friendly animals, larid not a Larus, ring species, enigmatic eclectus, eastern and western, not easy being green, wood warblers.

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?

Life Before it had Facial Features

Fossil cyanobacteria of the form taxon Myxococcoides minor from the Bitter Springs Formation of Australia. Photo from UCMP.

On a Monday morning when I am feeling every little nuance of the fact that it's a Monday morning, it seems appropriate to discuss a section of organismal diversity whose study seems pretty severely crippled before it has even begun. I speak of the study of fossil bacteria, and the subject of today's Taxon of the Week post is the Proterozoic fossil taxon Myxococcoides.

Myxococcoides is a small (1-35 µm) spherical to ellipsoidal fossil without distinctive ornamentation or other visible features found either singly or in loose colonies without an enclosing sheath or other distinct colony shape. It is an oft-repeated, but perhaps little appreciated, fact that bacteria were around and about long before a few of them considered getting together and making a eukaryote. I mean really long before. The earliest evidence of bacteria in the fossil record dates back nearly four billion years, while the earliest unequivocal evidence for eukaryotes is only about 850 million years old* (Cavalier-Smith, 2002). In other words, fully three-quarters of the history of life on this planet is represented only by prokaryotes. Only members of a species with severely anthropocentric delusions of grandeur would imagine that biodiversity did nothing in all that time except twiddle its thumbs and wait for the nucleus to develop, but there are some serious hurdles to understanding what was happening for the first three billion years of life.

*It will probably come as no surprise that the earliest date for eukaryotes is rather debatable - Cavalier-Smith (2002) gives a brief, if somewhat partisan, review. The 850 Mya date represents the earliest appearance of protist fossils of eukaryote cell size and complex cell morphology that implies the existence of a well-developed microfilament skeleton to hold it all in place. Certain fossils dating back as far as 1200 Mya or even 2100 Mya have been identified as eukaryotes, such as the putative "red alga" Bangiomorpha. However, these taxa have fairly simple cell morphologies and their identification as eukaryotes rather than prokaryotes rests on relatively few characters such as cell size. As argued by Hofmann (1976), supposed 'nuclei' in fossil cells may represent degradational artefacts where cytoplasm has become detached from the surrounding cell wall. While prokaryote cells are generally much smaller than eukaryote cells, bacteria can occassionally reach considerable sizes - the largest known bacterium, the sulphur-oxidizing Thiomargarita namibiensis, has cells almost a millimetre in diameter, a size that, as pointed out by Schütt (2003), is more than twice that of the smallest known spiders, which is a great piece of information to bring up at parties (technically, some actinobacteria such as Streptomyces are arguably even larger, but have a fungus-like filamentous hyphal morphology). It is therefore a perilous activity to label Proterozoic fossils as eukaryotes on the basis of size alone, especially as it is not unlikely that bacteria may have occupied a number of niches prior to the appearance of eukaryotes from which they were later excluded.

Lacking as they do the well-developed eukaryote cytoskeleton, the morphology of most prokaryotes is decidedly simple, with the majority of taxa conforming to the basic rod or sphere. For instance, Thermoproteus and Mycobacterium are both rod-shaped prokaryotes with colonies formed through snapping division that may be morphologically almost indistinguishable despite one being a archaebacterium and the other a Gram-positive eubacterium. Instead, bacterial taxa are generally distinguished by features of their genetics, biochemistry and physiology - all features that, of course, are generally completely unavailable when studying fossilised remains. As a result, taxa based on fossilised bacteria are doomed to be form taxa or morphotaxa - labels to indicate a particular morphology without necessarily indicating the actual relationships of the fossils involved. To complicate matters further, a single living morphology may potentially give rise to multiple fossil 'taxa' due to the level of degradation prior to preservation, as shown in the figure below from Hofmann (1976) of various stages of degradation from a Myxococcoides-like morphology.



Needless to say, the relationships of forms such as Myxococcoides to modern taxa is difficult if not impossible to establish. Most Precambrian fossil bacteria have been found in association with stromatolites and interpreted as cyanobacteria. They have then been assigned to modern orders on the basis of colony morphology, so forms without defined colony structures such as Myxococcoides have been assigned to the Chroococcales. However, phylogenetic analysis of recent taxa has shown that the Chroococcales (not surprisingly seeing as it was defined solely on negative characters) is a strongly paraphyletic assemblage from which filamentous forms have arisen polyphyletically (Litvaitis, 2002).

So why, some of you may be asking yourselves at this point, should we study fossil bacteria at all? Well, the simple fact is that, murky as it is, the bacterial fossil record remains our main window into three billion years of evolution. Some distinctive probable cyanobacterial groups, such as the family Aphralysiaceae (Vachard et al., 2001), have been identified solely from fossils, while others, such as the stromatolite-forming Entophysalidaceae, held far more ecological significance in the past than presently. If, as alluded to above, forms such as Grypania and Bangiomorpha represent prokaryotes convergent on eukaryotes that were later replaced by actual eukaryotes, then such diversity would have remained unknown except through the fossil record. Three billion years is a long time to miss out on.

REFERENCES

Cavalier-Smith, T. 2002. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. International Journal of Systematic and Evolutionary Microbiology 52: 7-76.

Hofmann, H. J. 1976. Precambrian microflora, Belcher Islands, Canada: significance and systematics. Journal of Paleontology 50 (6): 1040-1073.

Litvaitis, M. K. 2002. A molecular test of cyanobacterial phylogeny: Inferences from constraint analyses. Hydrobiologia 468: 135-145.

Schütt, K. 2003. Phylogeny of Symphytognathidae s.l. (Araneae, Araneoidea). Zoologica Scripta 32 (2): 129-151.

Vachard, D., M. Hauser, R. Martini, L. Zaninetti, A. Matter & T. Peters. 2001. New algae and problematica of algal affinity from the Permian of the Aseelah Unit of the Batain Plain (East Oman). Geobios 34 (4): 375-404.

Linnaeus' Birding

The next edition of Linnaeus' Legacy will be appearing at A DC Birding Blog in a few days' time. I've already received a number of submissions for the carnival, and if you want a piece of the action get submission in to me on gerarus at westnet.com.au, your host John (empidonax at gmail.com), or use the submission form at Blog Carnival. A reminder, too, that we're still looking for a host for September.

Inevitable Moles in a Lonely Universe

In 1989, the book Wonderful Life by Stephen Jay Gould made its triumphant appearance - of all the many writings by that prolific author, it was to become perhaps the most famous of all*. In this exploration of (then-)recent advances in our understanding of the animals making up the Cambrian explosion, the relatively rapid appearance of the distant ancestors of most living major animal groups, Gould argued extensively for the role of contingency and chance in evolution. If we were somehow able to turn time back to the Cambrian then let it run all over again, claimed Gould, then we would not see a repeat of the same evolutionary history. Major groups of organisms in our modern environment might fail to appear, while other groups that are currently minor and marginal might diversify to take their place. In particular, humans or intelligent life in general might never come to be.

*Something I find quite surprising - I personally find Wonderful Life rather drekky and overblown, and its arguments ultimately rather weak. To quote Moe Szyslak in the angel episode of The Simpsons (in which Gould actually made a guest appearance, "How about you stop telling us what it ain't, and start telling us what it am?"

Central to this argument of Gould's was his interpretation of the studies on animals from the Canadian Burgess Shale by Simon Conway Morris. Gould argued that very few of the animals present in the Burgess Shale could be definitely associated with taxa that survived the Cambrian, while most of the Burgess animals represented isolated lines that would eventually go extinct. Were one to look at the Burgess fauna in the absence of knowledge about future events, there would be no way of distinguishing which taxa were to survive and which would not. As it turned out, Gould's interpretation of Conway Morris' work was to rankle quite significantly with Conway Morris himself, who has since written two books that essentially counter Gould's book. In the 1998 The Crucible of Creation, Conway Morris attacked Gould's characterisation of the Burgess taxa as phylogenetically isolated oddballs, arguing instead that most were identifiable as stem-taxa showing connections to modern animals. While far more scientifically rigorous than Gould's Wonderful Life, The Crucible of Creation does suffer significantly from the constant shadow of Conway Morris' evident ire at Gould's 'misappropriation' of Conway Morris' work - Richard Fortey was later to comment in his 2000 book Trilobite! that he had "never encountered such spleen in a book by a professional".

I haven't yet read Conway Morris' second book of reply, the 2003 Life's Solution: Inevitable Humans in a Lonely Universe, but I would like to comment on its basic premise. In Life's Solution, Conway Morris addressed Gould's contention that the course of evolution was contingent on past history and essentially unpredictable. Instead, Conway Morris uses the prevalence of convergent evolution, the independent evolution of similar characters in unrelated organisms occupying similar habitats, to argue that selection pressures result in a relatively small number of potentially viable forms, and that even if Earth's history were rerun then a roughly similar assemblage of organisms would result. There might not be humans in exactly the form we now them, but intelligent, self-aware organisms of some kind would eventually appear.

Of course, both Gould's and Conway Morris' propositions are not directly empirically testable - there is no way of actually rerunning the course of evolution. However, convergent evolution is a widely prevalent phenomenon that we can examine and stimate its effect on the form of organisms. Convergent evolution seems to be the result of strong selective pressures - when a certain habitat or lifestyle strongly favours a certain morphology.

Moles, for instance, are definitely inevitable, at least among mammals. At least three different groups of living mammals have independently adopted a burrowing lifestyle - the Holarctic true moles, the African golden moles and the Australian marsupial moles. All three groups have developed a very similar morphology - reduced or lost eyes, dense fur, compact body with short limbs and spade-like forelimbs. Among fossil mammals, the marsupial (or at least metatherian) Necrolestes and the erinaceid Proterix have also been interpreted as burrowers with a very mole-like morphology. Even at least one group of burrowing insects, the mole crickets, went through a similar development of shortened limbs and spade-like forelimbs.

Cacti are fairly inevitable. A number of groups of plants inhabiting arid habitats - most notably various members of the Euphorbiaceae as well as the cacti proper - have evolved thickened water-storing stems with the loss or reduction of functional leaves to reduce water loss. Interestingly, the alteration of leaves to spines has occurred on numerous occassions, and it has been suggested that as well as the obvious benefit of protection, spines may help promote the condensation of moisture onto the plant as dew.

Lice, I'm sorry to say, seem to be inescapable. As well as the lice proper, a number of other insect groups have become ectoparasites living among the fur or feathers of other animals, such as a number of families of flies (including the sheep ked and bat flies) and the earwig Hemimerus. All such groups show a loss of wings, reduction of sensory organs such as eyes and antennae, and development of a flattened morphology that is probably less able to be squashed or scratched off by the host.

On the other hand, antelope are not inevitable. While the primary cursorial grazers of Eurasia and Africa are slender-legged quadrupeds, in Australia their niche is occupied by the bipedal kangaroos. I am not sure why kangaroos became jumping bipeds rather than running quadrupeds, but my suspicion is that their arboreal ancestry (phylogenetic analyses suggest that kangaroos descend from a possum-like ancestor) meant that the ancestral kangaroos started out with a difference in length between hind- and forelimbs. The point is that in this case two very different morphologies have developed to cope with very similar niches.

And humans? Well, it is my personal opinion that we have no reason to regard humans as inevitable. Invoking convergent evolution to claim the inevitability of humans runs up against the major stumbling block that we have no other examples of convergence on the human form. Questioning whether intelligence and self-awareness were destined to arrive as a result of selective pressure demands that we answer the insanely difficult yet crucial questions of how we define "intelligence" and "self-awareness", and how we would recognise them once defined. So difficult are these questions that yours truly is going to be a complete weasel and avoid them (I've spent enough time on this post already), but I will rather weakly point out that most behaviours cited as evidence for self-awareness in humans, such as figurative language and the production of art, are as yet unknown in other organisms when not encouraged by direct human intervention (but refer back to the recognition problem above). How is one to claim convergent evolution to support the existence of something for which no convergences are known?

A coda. In Kurt Vonnegut's 1985 novel Galapagos, a small boatload of people are shipwrecked on the Galapagos islands at about the same time as a plague wipes out humanity in the rest of the world. Over the course of the following million years, the descendants of this small group of shipwrecked survivors lose many of the features that have generally been regarded as the keys to what make us human but which are no longer selectively advantageous in their new environment, such as manual dexterity and large brains. Instead, humans become seal-like animals, covered in dense water-repellent fur with flippers for swimming and catching fish. It doesn't really matter what you're talking about - whether or not it's a good thing really depends on circumstance.