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

Down with the "Gene for X" nonsense already!

So how do I properly respond to a question like "Wouldn't putting fish genes in a tomato make it fish-like"?

I could go on explaining how genes don't actually carry any mysterious 'quality' of the organism they're found in, and generally just code for some protein that merely catalyses a specific chemical reaction. For example, jellyfish green fluorescent protein is just a fluorescent protein that gets most 'turned on' by blue light and changes it to green. It has nothing to do with jellyfish stings or tentacles or an aptitude for drifting behaviour. It was simply isolated from a jellyfish, and there's nothing fishy about it. Basically, GENETICS - UR DOIN IT WRONG. But in a more verbose and less condescending manner...

But then they respond that they don't believe you. That it just doesn't seem right. Ok, what do I do now? Not only have they got so much wrong I don't know where to begin fixing, they also have their faith, and information from someone who works with transgenic stuff on a daily basis is not going to be enough to change their minds.

First off, what the hell is the point of asking if you then don't 'believe' their response? If they had an argument of some sort against my story, or if they didn't understand some part, then by all means, ask away! But simply stating you don't 'believe' is a bit of a conversational cul-de-sac. Besides, it doesn't seem that genetics itself cares very much about what you believe.

Next, this leaves me wondering: where has public education gone wrong? How did the 'fish gene' concept emerge in the first place?

Perhaps this is an extrapolation of the "height gene" that permeates introductory genetics classes. Intro genetics is full of problems like "You cross a homozygous recessive short (tt) plant with a heterozygous tall plant (Tt)..." It seems that while convenient pedagogic tools for the study of heritability, problems like this distort the perception of how genes actually work. Genes do not code for qualities or traits - they are just A,T,C,G,N* strings that eventually make their way to being translated into amino acid language to become [hopefully] functional proteins. Playing around with this string of A,T,C,G can result in different phenotypes or physical appearances, starting from the shape and functionality of the protein and sometimes reaching all the way to physical appearance, such as height.

Seeing the gene as coding for a certain phenotype is messy and...well, wrong. Often one locus (gene) has several alleles (variants) which were found in screens for different things by different labs. For example, Arabidopsis rsw2 (radially swollen) was found along with rsw1 when screening for root swelling defects. This same locus was found by a lab studying the plant vascular system, and named irx2 (irregular xylem); dec (deffective cytokinesis) and acw (abnormal cell wall) by some other groups.

Does this gene code for forming a proper xylem, mediating proper cytokinesis or to prevent root swelling? Is this a 'Xylem Gene' or a 'Root Swelling Supressor'? What if I tell you defects in this gene result in substantial dwarfism? Is this yet another 'Gene for Height'? If you cross a short plant (homozygous rsw2) with a tall plant, your F1 progeny are all tall. Selfing the F1 results in 1:3 segregation of short:tall, respectively. Determine the genotypes...yadda yadda. See how useless and confusing this way of seeing genes can be?

The gene in question results in a protein chemically known as an 'endo-1,4-beta-D-glucanase' called KORRIGAN1 by biologists. It's believed to hang out near the cellulose synthase complex and cut the crystalising cellulose strands to relieve tension. (Reiter 2002 Curr Opin Plant Biol; pdf) All those mutants are results of point mutations and insertions in various parts of the same locus - many of the phenotypes actually overlap quite a bit, but the labs were focusing on different areas of plant biology, thus naming the allele as it was relevant to them. Yes, it can get quite messy!

Interestingly, different point mutations in this gene can have different phenotypes - implying there are several protein domains with different functions. Perhaps this thing acts in some sort of complex - the story is rather sophisticated at this point. But let's say it results in weakened cellulose fibrils due to crystalisation defects. Celluse is important in plant cell morphogenesis; essentially a plant cell expands like a balloon in a cage, with the cell wall acting like the cage in directing the expansion. Break the cage, and the balloon will tend to swell spherically. Thus the affected plant would end up with cell swelling. This disrupts growth in many tissues, eventually leading to problems with the vascular system and a severely dwarfed sick-looking plant. This gene doesn't 'code for' any of that, but defects thereof have far reaching consequences in the massive tangle of pathways that is life.


Of course, when you first find a gene, you don't know what it is yet, and thus name it after the mutant phenotype. This can lead to comical results - we have a 'Retinoblastoma-Related' gene in plants! No, plants haven't 'mutated/evolved eyes' (like 'evolve', 'mutate' should NEVER ever be used as a transitive verb...it is a strictly passive, non-volitional, non-directed event!) ... this gene is named after a homologous Retinoblastoma (RB) gene in the human system, where it may have been first isolated when studying the retinal cancer. While this gene does act in human eyes, this is not its 'purpose' or funtion it all. It carries no 'eye' qualities - its actual function is to supress DNA replication genes to prevent extra rounds of DNA copying out of turn. When it's broken, cell cycle problems follow, among them retinoblastoma in the human eye. Plants experience increased ploidy levels (number of copies of the genome) and hyperplasia in proliferating tissue. (reviewed in Inze & DeVeylder 2006 Annu Rev Genet; Gutierrez 2009 in The Arabidopsis Book) I hope it's clear by now that RB and RBR don't code for supressing retinoblastoma, but rather code for closely related proteins with very strictly defined chemical activities and precise functions affecting a multitude of pathways downstream.

Actually, the whole idea of genes having any function at all is an artefact of human reasoning (namely the intentional stance) - Dennett (1995 Darwin's Dangerous Idea) argues that while artefactual, the intentional is a powerful tool in inquiry as long as we acknowledge it doesn't actually imply a real 'purpose' encoded anywhere.

Population biologists (grrr) and evolutionary ecology folks ain't helping either. They intend to use the 'gene for blah' concept metaphorically, but that can easily mislead both the public and even some research in the field itself!


So if genes don't code for qualities or characters, how do you get from genes and proteins to organisms? We're working on that. The complexity of this problem will be enough to sustain many a developmental biologist with a lifetime of work (funding is whole other question altogether =( ) I intend to eventually share some snippets of the stories in that field... some of the mechanisms are truly elegant, others truly outrageous!

But hey, it works... otherwise you wouldn't be able to read any of this!


I do need to think up a simpler way of explaining 'how genes work'...

*Ah, the N, the phylogeneticist's worst nightmare and greatest blessing =P Freedom and ambiguity in one nice letter. (N stands for 'any' in FASTA format - ie A, C, T or G)
It's a bit creepy to watch phylogeneticists change 'edit' their sequences "Oh, that T shouldn't be there... *delete*" ...