All in the Bauplan

This year is my last year teaching the Animal Form and Function dissection lab at the University of Ottawa.  I’ve done a lot for this lab over the years, and I want to do one more thing.

The course is a survey through the animal kingdom with a particular emphasis on body plans.  A creature’s “Bauplan” (in the original German) is the basic structure of its body, rid of peculiarities that disguise the similarity between the animal and its relatives.  The more deeply these plans are explored, the more the ancient relationships and divergences that link animals to the entire kingdom’s common ancestor can be illuminated.  Animal phyla, if the term still has any value, are often best understood as groups united by sharing a bauplan that distinguishes them from other groups, and these structures are important for an aspiring student of animal anatomy to recognize.

The most basic animal body plan is a mouth leading to a gastrointestinal cavity, similar to those novelty plastic cups with fluid inside the walls and floor that always look like they are full.  The interior, inaccessible fluid can have any of various names and compositions, and forms the basis of the body cavity or coelom that characterizes most animals.  The original gastrointestinal cavity, where one puts their drinks, had a single opening, which changed function as needed between ingestion and defecation.  Very primitive animals, such as cnidarians and ctenophores, tend to still resemble this shape.  A few, even more primitive animals lack even this much, and have much more alien patterns.

A novelty beer mug with beer-colored liquid inside the plastic of the mug so that it looks full even when empty.
The body cavity is the part with the fake beer that doesn’t pour out. The single-opening gastrointestinal tract is the part where the real beer goes. The sphincter is implied.

Most animals have innovated on this base by adding a second digestive orifice.  This enables a functionally and anatomically distinct anus and mouth, and with that, a much larger array of possible body shapes.  The inner core of almost every animal’s bauplan is a tubular digestive tract with a mouth at one end and an anus at the other.  The cup is now a straw, usually sealed at both ends with contractile sphincters.

Image of post-gastrulation animal embryos, showing the formation of the blastopore, archenteron, and secondary opening, which together become the mouth, digestive tract, and anus.
Image of post-gastrulation animal embryos, showing the formation of the blastopore, archenteron, and secondary opening, which together become the mouth, digestive tract, and anus.

What happens to the mouth becomes a big deal for understanding many bauplans.  (Mollusks take a bit more.)

Most animal groups retain the mouth as a contractile (but not necessarily muscular) sphincter.  Mollusks affix a rasping structure called a radula inside the mouth, protruding it as needed for scraping food off of its environment.  A handful of animal groups, such as nematodes, most marine annelids, and sea urchins, add hard parts to the mouth.  Pieces of shell or cuticle near the mouth gain muscle attachments and are used to snag or break food particles during ingestion.  What’s important to recognize here is that these invertebrate jaws are almost always outside of, and therefore anterior or posterior to, the ancestral mouth.  The muscular sphincter is still there, and additional feeding organs have formed to service it, often reaching ahead of it from behind.

Underside of Strongylocentrotus purpuratus sea urchin showing the five pieces of shell material serving as its jaws. By Wilson44691 (Own work) [CC0], via Wikimedia Commons
Underside of Strongylocentrotus purpuratus sea urchin showing the five pieces of shell material serving as its jaws. By Wilson44691 (Own work) [CC0], via Wikimedia Commons
A human-like creature with arthropod oral anatomy. The mouth is a sphincter, and the pre-arm appendages are antennae (1), mandibles (2), maxillae with palps (3 and 4), and maxillipeds (5 and 6). Some appendages (antennae and mandibles) are pre-oral, and others are post-oral. The mandibles and maxillae process food while the maxillipeds and maxillary palps hold it in place. Standard arms and legs are also present. Compound eyes included for artistic reasons.
A human-like creature with arthropod oral anatomy. The mouth is a sphincter, and the pre-arm appendages are antennae (1), mandibles (2), maxillae with palps (3 and 4), and maxillipeds (5 and 6). Some appendages (antennae and mandibles) are pre-oral, and others are post-oral. The mandibles and maxillae process food while the maxillipeds and maxillary palps hold it in place. Standard arms and legs are also present. Compound eyes included for artistic reasons.

Arthropods take this model much farther.  One of arthropods’ major anatomical innovations is their trademark jointed appendages, in pairs from their first segment to their last.  Each group of arthropods has a different array of these appendages, but something they all have in common is that at least one pair is tightly associated with the mouth.  The vertebrate analogy would be if vertebrates had one to five pairs of arms emerging from the cervical spine and tightly folded around their faces, which were used almost exclusively for manipulating food.  Some arthropods, further, use not just the ends of their anterior appendages, but the bases of these appendages, to process food.  These “gnathobases” are usually located near the mouth and grind food between them, which one or more oral appendages can then bring to the mouth.  On a horseshoe crab, the gnathobases are on every limb, and food is processed in the middle of the animal’s body before a clawed limb brings it to the mouth.  A vertebrate with this model would have one or more sets of spiked shoulders doing what vertebrate teeth currently do and spend a lot of time grabbing tasty bits from between its shoulders to bring to its mouth.

A human-like creature with a different arthropod oral anatomy. The mouth is a sphincter. The appendages are antennae (1), mandibles with palps (2), pedipalps (3), and standard arms and legs. Most food processing takes place by movements of the shoulders, hips, and pedipalp attachments, grinding food between the gnathobases (4). The pedipalps bring food to the gnathobases and bring food particles below a certain size to the mandibles for further processing before ingestion.
A human-like creature with a different arthropod oral anatomy. The mouth is a sphincter. The appendages are antennae (1), mandibles with palps (2), pedipalps (3), and standard arms and legs. Most food processing takes place by movements of the shoulders, hips, and pedipalp attachments, grinding food between the gnathobases (4). The pedipalps bring food to the gnathobases and bring food particles below a certain size to the mandibles for further processing before ingestion.

A further arthropod specialization is that oral appendages can form a pre-oral “box.”   Whether through gnathobases or through dedicated oral limbs, many arthropods have a chamber anterior to the oral sphincter, and therefore outside the mouth and arguably outside the digestive tract, where food is chewed, ground, and otherwise processed prior to entering the animal’s actual, deeper mouth.  A vertebrate that showed this pattern would have a nest of limbs (some of which also have spiked shoulders) for a face, all surrounding a central, circular mouth that opens and closes the same way other digestive sphincters do.  The only vertebrates even close to this model are the Mobulinae.

Vertebrates and their chordate relatives are, one might surmise, the bearers of a very different bauplan.  Like arthropods, nematodes, and polychaete worms, vertebrates repurpose structures from elsewhere in the body to turn a digestive sphincter into a recognizable mouth, but the structures vertebrates borrow are quite different.  Teeth appear to have appeared as a repurposing of scaly or armored skin elements, migrating inward and becoming involved in feeding, analogous to the jaws of nematodes or polychaetes.  Jawed vertebrates have, in addition to that, seen radical restructuring of the mouth itself, highly dissimilar from the events that shaped the oral apparatus of invertebrates.

One of the key chordate innovations is a structure in the throat called the pharyngeal gill basket.  This organ is a basket-shaped skeleton supporting internal gills connected to the outside by spiracles.  Like arthropod limbs, the skeletal elements (hereafter “gill arches”) existed in multitudes and could therefore be specialized for new functions without compromising their previous tasks.  The expansion and contraction of the gill arches, used for breathing, meant that their movements affected the overall thickness of the animal and provided skeletal support not just to the gill apparatus itself, but to the whole region surrounding it, similar to ribs.  Over time, the whole apparatus moved progressively forward, until the first set surrounded the mouth and the second connected the first to the preexisting braincase.  In this way, part of the gill basket modified the mouth itself, enabling it to hinge open and closed, exert very different forces than a small, sucking sphincter, and otherwise become adapted to the rich variety of diets and functions found in vertebrates.  The rest of the gill basket, likewise, was now connected to the mouth, causing the mouth to become part of the respiratory apparatus in most vertebrates.  After the evolution of lungs from part of the digestive tract, the rest of the pharyngeal basket could be repurposed into additional strengthening bones in the skull and, in mammals, the middle-ear ossicles.

Illustration of how the anterior gill arches moved forward to become jaws.
Illustration of the evolution of vertebrate jaws from the gill arches of primitive, jawless vertebrates.

The jawed vertebrate mouth isn’t a digestive sphincter like that of most invertebrates.  It is a structure with a skeleton and joints that can hinge open and closed, and to which bony skin elements are attached in the form of teeth.  That is amazing.

One might wonder, then, why the vertebrates took such an unusual path to turn their feeding apparatus into a predatory apparatus.  After all, arthropods also have a highly adaptable oral apparatus, but their mouths are still mere sphincters.

The answer here is in the evolution of one set of limbs versus the other.  While both arthropods and chordates got their start as worm-like, tubular organisms, arthropod limb precursors appeared early and in huge numbers as their primary locomotor organs.  This early excess meant that arthropods could solve virtually all of their anatomical problems, other than flight, with specialized limbs.  Chordates did not develop an analogue for arthropod limbs until long after the evolution of jaws, thanks to swimming with flattened bodies like other worms.  Despite having segmentation of a sort in their muscles and skeletons, chordates do not have the same metameric organization as arthropods, which means they lack the same flexibility in limb development.  Fore- and hind-limbs have different articulation—notice that elbows and knees bend in opposite directions and shoulders and pelvises do not resemble one another.  Vertebrate limbs have been reforged into walking legs, paddles, rudders, grasping hands, three different kinds of wings, and compromise appendages that combine several functions, but their number is always four or fewer and the set with shoulders (if present) is always attached to the spine anterior to the set with hips (if present).

Mollusks, the third contender for the most flexible bauplan in the animal kingdom, have another approach.  Instead of a straight tubular body with internal organs, mollusks have four discrete body regions, with little evidence of even ancestral segmentation.  Mollusks have a head, a muscular foot, a visceral mass containing most of the organs, and a mantle which overlays most of the body, secretes the shell, and houses a “mantle cavity” in which the gills are protected.  Structures that must communicate with the outside, such as the mouth, reproductive orifices, and anus, are located on the head or foot and connect to long tracts leading to the associated internal organs in the visceral mass. Ancestrally, these would have been associated with the anterior and posterior ends of the visceral mass, but modern mollusks have relocated them to the head and foot.  Similarly, the nervous system has a central ganglion from which four nerve cords extend: two to the visceral mass, two to the foot.  This enables the foot to be wholly devoted to muscle action and the shell to protect the organs from harm.  Instead of having to infuse chitin or calcium salts into their entire bodies to become armored, mollusks can collect their most vulnerable structures into a single region and build armor around that region in particular.

Diagram of a generic mollusk likely to resemble the ancestral mollusk. The visceral mass sits atop the muscular foot and contains the organs, and the mantle secretes a shell atop the visceral mass.
Diagram of a generic mollusk likely to resemble the ancestral mollusk. The visceral mass sits atop the muscular foot and contains the organs, and the mantle secretes a shell atop the visceral mass.

This basic, four-part bauplan has been extensively modified in various mollusk groups.  In snails, the visceral mass is twisted, repositioning both the anus and the mantle cavity forward; the evolutionary and functional significance of this change is not yet clear.  Bivalve mollusks no longer have a distinct head, encompass the entire body in the mantle and shell, and embed the visceral mass within the foot.  Cephalopods undertake the most radical reorganization.  Cephalopod heads are located atop and partially within the foot, between the foot and the visceral mass, and the tracts previously connecting the mouth, anus, and reproductive organs in the visceral mass with their openings in the foot now pass through the head.  The foot is adapted into the cephalopods’ famous arms, tentacles, and muscular funnels, and often loses its locomotor function to become devoted to feeding.  In addition to its shell-secreting and gill-sheltering functions, cephalopod mantles are highly muscular and serve as jet-propulsion organs, directing water through the funnel to push the cephalopod forward.  In extreme cases, the shell is nearly or totally lost, and the mantle is wholly devoted to locomotion and respiration.  This movement mode means that many cephalopods have a functional orientation that does not correspond to their ancestral orientation, pointing the ancestral dorsal surface forward and rear surface downward to swim.

Bauplans are the basis on which the millions of specialized forms animals can take are built, and likewise serve as the basis through which those forms can be understood.  Identifying bauplans and the ways in which they have been modified in the face of highly variable evolutionary pressures was a key step toward a cladistic, hereditary model of animal classification, and it is absolutely vital for developmental biology.  This concept is one of comparative zoology’s greatest contributions to biology at large, and no understanding of animal diversity can be complete without it.

Certainly not one that purports to figure out the differences between vertebrates and arthropods.

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All in the Bauplan
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10 thoughts on “All in the Bauplan

    1. 2.1

      Signs currently point toward the protostome, mouth-first model being ancestral and the deuterostome model being derived. After all, an anus with no associated mouth is rather useless. However, there are two necessary caveats:

      1) The deep evolutionary history of animals is the subject of ongoing research, and genetic evidence has upended many previously tidy narratives and categories;

      2) It turns out the standard list of deuterostome-vs-protostome distinctions is MUCH fuzzier than most textbooks suggest, with most of the anatomical features associated with deuterostomy found in various other places (often the lophophorate phyla) in the animal kingdom. What actually does define the deuterostomes is their regionally-determined developmental biology, in which cell fates aren’t permanently decided until fairly late in development and can be rearranged by changing a particular cell’s neighbors.

  1. 3

    I really liked this post!
    I wanted to find out more, but unfortunately the Biology tag contains only two posts. Could you please add your previous biology articles to the tag?

    1. 3.2

      The Categories region accessible in the sidebar is much more consistent and thorough than my tags. Additionally, my other science posts are collected on the Quotidian Science page linked at the top of the main page and every post. My previous blog home didn’t place tags quite so prominently and older posts reflect that lack of priority. I may yet have time and energy sufficient to make the old ones look like the newer ones.

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