Arthropod Early Evolution: A Solution to the Arthropod Head Problem?

[lpetrich]

The arthropod head problem, about the origin of arthropod heads, has long been a contentious issue; but some time ago, I'd come across an interesting paper on that question:

A palaeontological solution to the arthropod head problem
Graham E. Budd, Nature, 417, 271 (2002)
Here in PubMed (http://www.ncbi.nlm.nih.gov:80/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=12015599)

It features an analysis of the heads of several of the more enigmatic Cambrian arthropods, comparing to those of arthropods represented later in geological time (euarthropods). A remarkable result emerged: those Cambrian arthropods form a rather bushy tree that the euarthropods branch from inside of. This means that euarthropods are rather derived by Cambrian-arthropod standards. Many of those Cambrian arthropods are noted for having a large pair of appendages on their first segments, with smaller or absent ones on later segments. Anomalocaris is well-known for having such "great appendages". However, euarthropods lack such great appendages, or at least so it seems. Dr. Budd proposes that the great appendages have become the euarthropod labrum, a small plate just forward of the mouth. Here are Dr. Budd's identifications:

Fortiforceps, one of those early-Cambrian stem arthropods.

#1: Frontal appendage
-- Mouth
#2: Antenniform appendage
#3: Walking limbs 1
#4: Walking limbs 2
#5: Walking limbs 3
...

Chelicerates (horseshoe crabs, arachnids, etc.)
#1: Labrum
#2: Chelicerae (fangs)
-- Mouth
#3: Pedipalps
#4: Walking limbs 1
#5: Walking limbs 2
#6: Walking limbs 3
#7: Walking limbs 4
...

Crustaceans (including insects)
#1: Labrum
#2: Antennae 1
#3: Antennae 2 (insects: absent)
-- Mouth
#4: Mandibles
#5: Maxillae 1
#6: Maxillae 2 (insects: labium)
#7: Walking limbs 1
#8: Walking limbs 2
#9: Walking limbs 3
...

So spiders walk with limbs that insects use for eating.

When it is present, the labrum moves backward to be just in front of the mouth. The segments have these shared features:

#1: Ocular, protocerebrum (~ vertebrate forebrain)
#2: deutocerebrum (~ vertebrate midbrain)
#3: tritocerebrum (~ vertebrate hindbrain)

In effect,
Cerebrum est omne divisum in partes tres
Every brain is divided into three parts
(apologies to Julius Caesar)

The arthropod-vertebrate homology here is described in papers like:

An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila.
Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H.
Development. 2003 Jun;130(11):2365-73.
Here in PubMed (http://www.ncbi.nlm.nih.gov:80/entrez/query.fcgi?cmd=Retrieve&db=pubmed&dopt=Abstract&list_uids=12702651)

If the idea of insect mouthparts as limbs seems strange, check out this picture of a grasshopper embryo from pharyngula.org (http://pharyngula.org) - PZ Myers's site:

http://pharyngula.org/galleries/hoppers/hopper.jpg
The 'hopper's head is at the top of the picture; from top to bottom, its limbs are:
Antennae (1 set)
Mouthparts (3 sets)
Walking limbs (3 sets)
Notice also that the hindlimbs are only slightly enlarged with respect to the other two pairs of walking limbs; they become much larger as the embryo grows.

And finally, on a lighter note:

Bug heads, bug heads, roly-poly bug heads.
Bug heads, bug heads, eat 'em up, yum!

[Steviepinhead]

Hey, lp!

Didn't want you to think this fascinating contribution was being ignored!

I've been following the discussion around similar issues on PZ Myers' "Pharyngula" blog and in other writings (The Evolution of the Insects) for several years now.

I appreciate your links -- I've managed to get through the wiikipedia article and will try to find time for Budd today.

[DMB]

I wonder what creationists make of this? I almost feel tempted to go elsewhere and ask Dave H. :evil:

[lpetrich]

The arthropod central nervous system has an interesting curiosity. It is ladder-shaped, with ganglia (little brains) where the rungs meet the sides. Nearly all of it is ventral (belly side), but in the head, the side nervous cords go from ventral to dorsal (back side) to arrive at the brain. And as they do so, the throat goes between them.

brain | gut
mouth | nerve cords

A clue as to the origin of this oddity comes from studying some of the arthropods' closest relatives, which are the onychophorans and tardigrades. Onychophorans resemble caterpillars, though they have antennae and their legs look alike. Fossils of them are rare, though there are some Cambrian fossils of some of them, like Aysheaia and Hallucigenia.

B. Joakim Ericsson and Graham E. Budd have done some groundbreaking work on onychophoran heads, which they have published in several places:
Evolution and Development of the Onychophoran Head and Nervous System (http://uu.diva-portal.org/smash/record.jsf?pid=diva2:162611)
Onychophoran cephalic nerves and their bearing on our understanding of head segmentation and stem-group evolution of Arthropoda (http://www.ncbi.nlm.nih.gov/pubmed/18088927)
Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system (http://www3.interscience.wiley.com/journal/99018561/abstract?CRETRY=1&SRETRY=0)

Though the onychophoran mouth, like the arthropod one, is on the ventral side, it is connected to three parts of the brain, with one of the connections being dorsal-side. From that and some other developmental features, Ericsson concluded that onychophorans had an ancestor whose mouth is at the front end of the body (terminal), rather than on one side, and that the mouth later moved to one side.

This may also explain the arthropod pass-through.

Looking a bit further, there are some relatives of these "panarthropods" that have front-end mouths and brains around their throats, the Cycloneuralia.

Scalidophora: (Markuelia, (Kinorhyncha, (Loricifera, Priapulida)))
Cycloneuralia: ((Nematoda, Nematomorpha), Scalidophora)
Panarthropoda: (Arthropoda, Onychophora, Tardigrada)
Ecdysozoa: (Cycloneuralia, Panarthropoda)

Panarthropoda may branch from inside of Cycloneuralia, however.

Markuelia (http://palaeo.gly.bris.ac.uk/donoghue/page2/page22/page22.html) is known from some Cambrian fossil embryos, but it is preserved with enough detail to enable its identification as a basal scalidophoran.

[lpetrich]

Also interesting about onychophoran heads: their antennae grow out of segment #1, instead of arthropods' segment #2 or #3. So they are a case of convergent evolution, and they may be homologous with early arthropods' great appendages.

They are also in front of onychophorans' eyes, which are on segment #1, like arthropod eyes. By comparison, arthropods' antennae are behind their eyes.


If you have trouble loading my previous post's Markuelia link, try PZ Myers's blog entry on that tiny Cambrian worm: Pharyngula: Beauty in a speck of dust (http://scienceblogs.com/pharyngula/2006/08/beauty_in_a_speck_of_dust.php) He has a lot of nice links on it, as well as some nice Cambrian-embryo pictures.

I've put together this table of how long members of various phyla in Ecdysozoa can grow:

Arthropoda: Jaekelopterus rhenaniae (Devonian eurypterid), est. 2.5 m
Onychophora: 20 cm
Tardigrada: 1.5 mm
Kinorhyncha: 1 mm
Loricifera: 1 mm
Priapulida: 15 - 30 cm
Nematoda: Placentonema gigantissima (found in a sperm whale's placenta), 8.5 m / free-living: around 1 mm
Nematomorpha: 1 m, dia. 1 - 3 mm

I could not find any estimates of the size of Markuelia adults, however.

Of these, Jaekelopterus likely had the largest body mass of any ecdysozoan, but I could not find estimates of that either. The most massive present-day arthropod is likely the American lobster, Homarus americanus, recorded at 22 kg and 1.18 m long. Scaling to the estimated size of Jaekelopterus suggests a body mass of 100 - 200 kg.

Some sources: Largest organisms and Largest prehistoric organisms

[Steviepinhead]

Maybe this is the appropriate place to say how much I love the word "tagmosis."

I look for excuses to drop it into casual conversation: "My dear, your tagmosis really matches your shoes, today!" "Excuse me, ma'am, but I think you just dropped your tagmosis!" "Did you guys catch today's tagmosis forecast?"

When someone looks startled (it's amazing how many people fail to react at all, if you maintain an even tone -- their miinds apparently "translate" the unfamiliar term to something that sounds similar and makes some sort of sense), you just repeat the phrase but insert something more commonplace, like "earrings," "handkerchief," or "weather"...

I've actually had people say, "Bless you!" as if I'd coughed or sneezed.

Ah, well. Moving right along...