People are always arguing about whether primitive apes could have evolved into men, but that one seems obvious to me: of course they did! The resemblances are simply too close, so that questioning it always seems silly. One interesting and more difficult question is how oysters could be related to squid; one’s a flat, sessile blob with a hard shell, and the other is a jet-propelled active predator with eyes and tentacles. Any family resemblance is almost completely lost in their long and divergent evolutionary history (although I do notice some unity of flavor among the various molluscs, which makes me wonder if gustatory sampling hasn’t received its proper due as a biochemical assay in evaluating phylogeny.)
One way to puzzle out anatomical relationships and make phylogenetic inferences is to study the embryology of the animals. Early development is often fairly well conserved, and the various parts and organization are simpler; I would argue that what’s important in the evolution of complex organisms anyway is the process of multicellular assembly, and it’s the rules of construction that we have to determine to identify pathways of change. Now a recent paper by Shigeno et al. traces the development of Nautilus and works out how the body plan is established, and the evolutionary pattern becomes apparent.
Working out the development of a cephalopod is very hard work. They aren’t trivial to raise, requiring large quantities of filtered sea water and constant tending — imitating an open ocean environment in a tank in a lab isn’t easy. The Shigeno group has managed to raise 3 generations of Nautilus in the lab, which is an accomplishment in itself; they collected 1035 eggs over the course of five years, of which 81 reached the hatching stage. I think you can understand why most of us work with model systems rather than these difficult species. In my small zebrafish colony, I can get that many eggs in a week, and have well over a 90% hatching rate. Furthermore, it takes 8 months for a Nautilus egg to reach the hatching stage; that takes 2 days in a zebrafish. Ouch. The investigators have my sympathy. This is slow, difficult work.
The animals they were raising were Nautilus pompilius. If you need to be reminded of the differences between a nautiloid and a squid, here’s a handy reference diagram to their gross anatomy.
The affinities are clear. Both can be roughly divided into two body parts, a posterior visceral mass (that bag-like “head” of an octopus isn’t actually a head, it’s where it keeps its guts, and similarly the mass in these animals is within the shell or mantle) and an anterior head, with eyes and tentacles/arms and a collar and funnel. Nautiloids have a shell, simpler eyes, and more tentacles that lack suckers. These regions are set up early in development, and the purpose of this particular paper is to sort out what’s going on in just that head region.
Let’s get one confusion straightened out quickly. We usually think of the tentacle side as the front side, but embryologically, it’s the ventral side, and the visceral mass is dorsal. Just that swiveling around of perspective helps clarify the developmental process. In the picture below, you can see just how cute and adorable a baby nautilus is, but you can also see that the external morphology of the head complex is also the most complicated part of the animal.
So now we roll back the clock and look at an earlier stage of development, at 3 months after fertilization. You have to imagine taking the animal above, putting one hand on top (dorsal), one hand on the bottom (ventral) and squishing it into a pancake-shaped disc. The picture in (a) below is looking down on the disc. The visceral mass, the mantle and shell field, is in the middle, and the more ventral head parts are now splayed out in concentric rings around the periphery.
Now you might be able to see some of the similarities to other molluscs. Another point of interest most easily seen in (b) is that there are little buds that will eventually form the tentacles — and there are nine on each side, for a total of 18. The primitive number of tentacles in cephalopods is thought to be 10, and what we can see here is that embryonically, each tentacle (except one pair in Nautilus) are formed from a pair of buds that are thought to fuse later in development.
One of the common hallmarks of papers describing the development of a species is the establishment of a staging series. Because the number of specimens is so small in this case, though, the staging is understandably a bit rough, and there aren’t a lot of detailed steps described. The process of tentacle bud fusion, for instance, wasn’t seen, and has to be inferred from widely spaced samples. The photos below show embryos at 3, 4, and 6 months, at least, and can give you a sense of the changes going on. And (h) in particular is very pretty — a kind of short, stumpy version of the later nautiloid to emerge.
Tentacle/arm development and evolution is confusing! The authors compared Nautilus with a coleoid cephalopod, Idiosepius paradoxus. Idiosepius is a little strange itself; it’s a highly specialized, tiny (less than a centimeter long) squid with reduced arms that at least is prolific and easily harvested, and does represent the coleoids in this study. Nautiloids add additional tentacles beyond the basal 10 that muddle up the issue enough, but we can still see a core similarity. Idiosepius is shown in (e-g), and they also have 9 buds on each side, grouped in pairs (except for one). The irregularities in the distribution suggest to me that when we someday get around to identifying the molecular/genetic patterning elements in the cephalopod, we aren’t going to find a simple pattern generator—I suspect we’re instead going to find hard-coded specific regulatory elements for each arm.
One other question people always ask — we’ve got mostly ten-armed squids, and eight-armed octopus. What happened? We don’t know. The paper briefly discusses the homologies between different species, but unfortunately the homologies in the octopods seem to be an open question, still, with different competing explanations. Obviously, what we need is more octopus embryology!
At least when comparing nautiloids and coleoids, we aren’t completely lost. The similarities in the organization at that early pancake-like stage are easy to see, and are color coded in this diagram.
Note also how the arm buds are initially located posteriorly and the mouth anteriorly, like a more typical descendent of a bilaterian worm. Later in development, the arms migrate to wrap around the mouth, to produce the familiar central mouth surrounded by arms.
Now to answer that question raised at the beginning of this article: what is the evolutionary relationship between the organization of a primitive gastropod and a cephalopod? The diagram below relates the parts of Patella, more familiarly known as a limpet, to Nautilus and Idiosepius, and also within the cephalopod group. What cephalopods did was modify the muscular gastropod foot into an array of tentacles, and then elaborate the set of organs above them (eyes, ganglia, funnel, etc.) into a head complex.
We can also sketch out the molluscan body plan and see the relationships in the phylotype of gastropods and cephalopods. The ironically amusing part is that what we’re calling the “head complex” of a squid is actually derived in part from the foot — it’s an amazing piece of of morphological juggling that actually makes a heck of a lot of sense from a developmental point of view.
This was an awesomely data-rich paper, and I haven’t even touched on some of the information on gene expression, so I’m just going to give you the very handy brief summary from the end of the paper.
The tentacles/arms were derived from the foot
region. Acquisition of a nektonic life from a
benthic ancestor accelerated the loss of a creeping pedal sole and the development of tentacles
from a freely mobile foot.
In an ancestral cephalopod, the number of ten-
tacles/arms was five pairs (or 10 pairs of bipartite
arms). This means that the large number of tentacles in Nautilus results from secondary multiplication. Alternatively, the 10-arm condition of
coleoids could be neotenous.
The mouth surrounded by foot-derived tentacles/arms is unique among molluscs. This
body plan was created by enwrapping the head
part by epidermal tissues of pedal origin. During embryogenesis the pedal region shifts for-
wards on the body surface, and eventually the
“foot” is displaced anterior to the head.
The rhinophores of Nautilus and olfactory
organs of coleoids are presumably homologous,
since they develop at similar posterior parts
of the cephalic compartment as discussed earlier. Therefore, ancestral olfactory organs might
have been present at an early stage of cephalopod evolution.
An unfused hyponome as a primitive funnel
might have arisen from the posterior part of the
hood-collar compartment, which is possibly
derived from an intermediate zone between the
head-foot and visceral mass in the monoplacophoran ancestor. Alternatively, there
is a possibility as suggested by Naef that
a region of epipodial (dorsal) tentacles may differentiate into the hood-collar compartments.
Then, with modifications for free-swimming
behavior, the collar became distinct at the lateral region of the mantle and well-developed,
including the funnel.
Cephalopod brain masses centralized from the
primitive tripartite neural-cord condition
as seen in the embryonic nervous system of
coleoids. Early cephalopods probably had a
cord-like brain (not ganglia) as is found in the
pedal cords of primitive gastropods.
The optic lobes innervating cerebral eyes were
derived from the cerebral cord, since this connection is found in the early embryos of Nautilus.
The hood seems to be a secondarily-derived
structure, convergent with the operculum of
gastropods, which was coopted from two dorsal
arm pairs together with ocular tissue and part
of the collar/funnel complex.
The ancestral function of transcription factor
engrailed was conserved during the shell formation process, given that similar expression patterns were seen in Nautilus, Idiosepius, and
other molluscan embryos. Further
analysis is required; however the expression
patterns may suggest a role for arms (pedal
components), funnel, collar, and eyes in the evolution and development of molluscs.
The whole system is beautifully complicated, but what we see in this work is the power of developmental biology to illuminate the underlying, fundamental rules that define the evolution of organismal form.
Shigeno S, Sasaki T, Moritaki T, Kasugai T, Vecchione M, Agata K. (2007) Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: Evidence from Nautilus embryonic development. J Morphol. [Epub ahead of print].