Social onychophorans!

As much as I'm obsessed with protists, I'm a rather promiscuous type when it comes to academic relationships, and thus can find the occasional non-protist cute and interesting. Forgive me if that is 'immoral', but I'm not Christian and thus am not obligated to be intellectually monogamous. So there.

Onychophorans (velvet worms) are fucking adorable. Now, whether they are more or less adorable than, say, hypotrich ciliates or Apusomonas proboscidea, is open to debate (I remain loyal to my tribal academic affiliations in that regard), but there's no way you can look at this wonderful creature and not think it's damn cute:

Something about onychophoran morphology resonates quite nicely with our innate aesthetic senses...or maybe it's just me. Some of them have really pretty patterns too, or come in absolutely bizarre colours. (Mayer & Herzsch 2007 BMC Evol Biol)

A while back someone was waxing poetic about social spiders in class, which led me on quite an adventure. Since I had something very important to do that night, like an exam the following day or something, I got a lot of procrastination done: read about various social spiders (who also have an interesting story of evolutionary dead ends and conflicting levels of selection; oh, and a species with observed cooperative transport of large prey -- apparently fairly rare in arthropods), made my way to social pseudoscorpions (some of them apparently disperse by riding large insects like bugs or beetles), and then I hit upon this paper:

Social behaviour in an Australian velvet worm, Euperipatoides rowelli (Onychophora: Peripatopsidae) (Reinhard & Rowell 2005 J Zool)

Social behaviour in onychophorans? Seriously!? On a second thought, why the hell not? And then came a complete overload of cute that could've only been enhanced by better images...velvet worms who cuddle!

Awww =D Reinhard & Rowell 2005 J Zool

As cuddly as they may seem, these guys also have a strict social hierarchy involving an alpha female. Reinhard and Rowell (2005) describe a feeding process where a cricket was thrown into the petri dish and attacked by the adult onychophorans (who trap their prey with sticky salivary secretions). After subduing the cricket, the first female fed on the prey for nearly an hour, biting and chasing off any other individual that would approach. After that hour, other females were allowed to feed, and then eventually males and juveniles. Most of the males were feeding after the females left. A feminist's paradise.

The interactions between individuals were observed and classified into dominant vs. subordinate: biting and chasing were done by the dominant individual (with the subordinate fleeing) whereas climbing was done by the subordinate and up to the decision of the dominant whether or not to be tolerated:

Juveniles were generally left alone and tolerated. Meanwhile, the adults were involved in a constant display of aggression and submission. Females were dominant to the males. When groups of onychophorans from different logs (thus, different social groups) were pairs, individuals of both groups acted aggressively to each other, and despite the males insisting on climbing, no aggregations were formed as they were ruthlessly rejected. Thus, the social groups are stable and at least these onychophorans seem to be capable of kin recognition.

The dominance hierarchy seemed largely size-dependent, with smaller females almost always being subservient to the larger individuals. It is believed that as in many other instances of sociality, social behaviour here aids in the cooperative capture of large prey. Curiously, the strict hierarchy when it comes to feeding, with the alpha female hoarding the entire prey, is not known in any other invertebrate.

Onychophoran behaviour doesn't receive much attention, perhaps at least partly due to the onychophoran's idea of a perfect habitat not coinciding all too well with that of an ethologist: velvet worms love cold, damp places. So it wouldn't be too surprising if an entire group of social species were eventually discovered, perhaps even with separate origins. In fact, Reinhard and Rowell (2005) state that it is not even known whether sociality may be common for onychophorans in general. On the topic of behaviour, despite their cute and almost fluffy appearance, onychophorans can also be quite vicious. This one devoured a spider bigger than itself:

Sticky spit vs. sticky silk. Quite surprisingly, the spit won this battle. (while checking whether this spider actually produces silk, found out that apprently tarantulas secrete adhesive silk from their feet...)

It is thought that in order to partake in such complex social behaviours, the onychophoran must have a fairly well-developed region for higher level sensory processing. (considering the complexity of the visual and olfactory cues likely involved in this case, it seems quite plausible. That said, there may well be fairly intricate social interactions out there that do not rely on complex neurology, by executing much simpler rules...) Curiously, they seem to have structures similar to 'mushroom bodies' in arthropods responsible for visual and olfactory processing and regulating complex behaviours. Actually, that was just an excuse to show this stunning image:

Onychophoran nervous system. Pseudocoloured to reflect the nerve depth in the confocal projection. Parts of the nervous system arise in a segmented fashion (eg. leg innervation), parts are repeated but not in a segmented way, and they also lack segmental ganglia as those in arthropods. Thus, onychophorans are slightly segmented in some respects, if you will, but still quite different from annelids and arthropods. This image really needs to be submitted to Nikon Small World... (Mayer & Whitington 2009 Dev Biol)

Now I don't want to divert attention away from onychophora by mentioning their significance in understanding arthropod (and other Ecdysozoan) evolution -- one almost feels sorry for onychophorans as they're usually introduced as "that group that is interesting because it tells us stuff about those other lineages", and that really bugs me. But still, onychophorans are particularly important for evolutionary biology, especially since invert phylogeny seems to be in a bigger mess than that of protists**. It was typically thought that annelids and arthropods shared a common origin of segmentation, but some recent data conflict with that.

Onychophorans, conveniently branching between annelids and arthropods, seem to have little going on in the way of nervous segmentation. It has been first interpreted as having a reduced segmental nervous system with the ventral nerve cord bearing relics of reduced ganglia. The ring nerve bundles are absent in the leg regions (and present between them) in a segmentally-appearing fashion; however, Mayer & Whitington (2009) have shown that the number of bundles between each leg pair varies and that unlike in arthropods, ventral organs do not coordinate neural development, as they develop fairly late relative to the nervous system. Curiously, the function of ventral organs in onychophoran development seems to be poorly understood.

Thus, segmental ganglia seem to have evolved in annelids and arthropods separately, adding further support to the Ecdysozoa idea (a debate I know next to nothing about...). The story of protist phylogeny has shown that convergence is much more rampant than we'd like to think, so it would be quite interesting if the nervous system of annelids and arthropods is also a case of convergent evolution, further showing how outright dangerous it is to rely on morphology for phylogenetic reconstruction. Metazoan phylogeny is a mess. While trying to get a grip on invert phylogeny for a class, I found it rather daunting how much I'd have to learn in order to make any sort of personal judgement on the matter. While protists are enough to keep one busy and fascinated (and overwhelmed) for many lifetimes, it is still fun to occasionally wander outside one's field and check out the daunting questions others have to deal with.

Besides, prior to taking a course in developmental biology, I actually had quite an interest in it, before it was quelled mercilessly by having to memorise structures of the 72h chick embryo. Without any evolutionary context. I think studying unicellular development would be useful for those studying multicellular development, as there must surely be ultimate convergence between many processes and structures. After all, there's only so many ways one can establish polarity, regulate morphology, grow, reproduce, etc. Comparative study of the developmental biology of the various eukaryotic (and prokaryotic!) supergroups and phyla therein would surely be a fun field once enough is known about organisms that are NOT mice, mustard weed, baker's yeast and fruit flies.

Ummm, how did I go from protists to onychophoran developmental neurology again? Oh right, procrastinating with physchem final can do wonders to one's intellectual promiscuity (aka procrastination-induced curiosity...) But onychophorans are damn cute, aren't they?

Oh, and by the way, onychophorans are so totally like caterpillars. Especially the live birth part (in some species).

*OMG there are also eusocial thrips. With soldiers.
** I wonder if the traditional zoologists' repulsion towards anything molecular may be part of it...

References
Dias, S., & Lo-Man-Hung, N. (2009). First record of an onychophoran (Onychophora, Peripatidae) feeding on a theraphosid spider (Araneae, Theraphosidae) Journal of Arachnology, 37 (1), 116-117 DOI: 10.1636/ST08-20.1

Mayer, G., & Harzsch, S. (2007). Immunolocalization of serotonin in Onychophora argues against segmental ganglia being an ancestral feature of arthropods BMC Evolutionary Biology, 7 (1) DOI: 10.1186/1471-2148-7-118

Mayer, G., & Whitington, P. (2009). Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda Developmental Biology, 335 (1), 263-275 DOI: 10.1016/j.ydbio.2009.08.011

Reinhard, J., & Rowell, D. (2005). Social behaviour in an Australian velvet worm, Euperipatoides rowelli (Onychophora: Peripatopsidae) Journal of Zoology, 267 (01) DOI: 10.1017/S0952836905007090