Deuterostomia I: Origins and Ambulacraria
Living Members: Living deuterostomes were first identified by "deuterostomous" developmental characters:
- Radial cleavage
- Formation of the anus from the blastopore, with the mouth arising as a secondary opening
- Enterocoelous development of the coelom
- Cephalochordata - Amphioxus
- Urochordata - tunicates
- Craniata - vertebrates and their closest relatives (right)
Leopard sea cucumber Bohadschia argus
- Crinoidea - sea lilies
- Asteroidea - starfish
- Echinoidea - sea urchins
- Ophiuroidea - brittle-stars
- Holothuria - sea cucumbers (right)
Acorn worm from The Telegraph
- Enteropneusta - acorn worms (right)
- Pterobranchia - pterobranchs and graptolites
Yet wonderfully, the illumination of Cambrian fossils on the stems of each of these groups has provided significant, if imperfect resolution. Of particular importance:
Vetulicolians by Skelefrog from Deviant Art
- Lacking hard parts, but with an outer skeleton of plates of cuticle.
- Body divided into a barrel-shaped front portion and a tail with seven distinct segments.
- At the front is a large mouth without feeding appendages. (Indeed, their are no appendages at all.)
- The front portion encloses a large open space
- Five pairs of openings penetrate the sides of the front segment along a pair of grooves.
- The tail is a laterally compressed and moved from side to side.
The consensus interpretation (see Vinter et al., 2011) is that:
- The front segment represents a pharynx - a large chamber through which particulate-laden water is filtered for feeding.
- The tail is homologous to the tails of chordates
Vetulicolians (along with a few other oddballs) are either:
- on the stem leading to the common ancestry of Deuterostomia, or
- The sister taxon of Urochordata (Garcia-Bellido et al., 2014.)
Deuterostomia:(Cambrian - Rec.) Whatever vetulicolians are, exactly, their morphology illuminates the ancestral state of deuterostomes. Vertebrate paleontologists have long predicted that the ancestral vertebrate would be, in essence, a swimming pharynx. This seems to describe deuterostomes in general. This information enables us to propose morphological synapomorphies of Deuterostomia:
- A pharynx with phayrngeal openings
- A segmented tail that undulates laterally
Note: Literature older than ten years has been rendered obsolete by molecular analyses that dispelled once and for all the notions the other creatures with three-part coeloms, including brachiopods, phoronids, and chaetognaths (arrow worms) might also be deuterostomes.
Why we care:
- Echinodermata: After mollusks and arthropods, the most commonly fossilized bilaterian taxon. Indeed, disarticulated echinoderm plates are major constituents of Phanerozoic carbonates, especially from the Early Carboniferous. Moreover, echinoderms are appealingly bizarre.
- Chordata: Contains the creatures that dominate animal biomass, occupy top of terrestrial and marine food chains, and serve as keystone species, ecologically.
We will spend considerable time on these two major deuterostome groups. First, let's put them in their context.
Deuterostome phylogeny is characterized by two major groups:
- Ambulacraria: Echinodermata and Hemichordata
- Chordata: Vertebrates and their relatives.
Tornaria (left) and auricularia (right) larvae from University of Saskatchewan
Ambulacraria:Recent molecular phylogenies indicate sister taxon relationship between Echinodermata and Hemichordata. Most members are suspension or deposit feeders, although some obtain food in more interesting ways.
Potential synapomorphies of hemichordates and echinoderms:
- Molecular characters
- Feeding appendages (proboscis and feeding appendages of hemicordates, ambulacra of echinoderms) containing coelomic extensions
- Auricularia larvae of holothurians resemble tornaria larvae of enteropneusts.
Hemichordata:(Cam - Rec.) Solitary or colonial suspension and deposit feeders who use ciliated appendages to concentrate particle-rich water in pharynx, where it is filtered.
- Bodies divided into proboscis, collar, and trunk, each of which is invested with its own part of the three-part coelom (right):
- Cilia on the proboscis move food particles to mouth.
- Collar encircles mouth and proboscis.
- Trunk contains a large pharynx with pharyngeal openings (homologous to gill slits)
- Open circulatory system present, with blood propelled by contractions of primary blood vessels. No hemoglobin.
- Cilia on the proboscis move food particles to mouth.
- Dorsal nerve cord, hollow in some parts of collar.
- Portions of the genome that code for the expression of pharyngeal slits are homologous in Hemichordata and Chordata (Simakov, et al., 2015.)
Enteropneust from Filmati di Mare
Enteropneusta: "Acorn worms": (Middle Cambrian - Quaternary)
- Largish (5 cm - >2m) worm-like burrowing suspension or deposit feeders.
- Pharynxes large and perforated by many pairs of gill openings.
- Acorn-shaped proboscis gives common name
- Invariably solitary.
- Infaunal, inhabiting U-shaped burrows. Probably responsible for many U-shaped Diplocraterion-style domichnia.
- Poorly-known as fossils, although probably enteropneusts are known from the Middle Cambrian and Late Carboniferous (Maletz, 2013)
Rhabdopleura from Physical and Biological Sciences, U. C. Santa Cruz
- Tiny (<2 mm.) colonial critters that secrete branching colony consisting of proteinaceous tubes.
- The proboscis is developed into a cephalic shield, used to secrete the proteinaceous material of the colony structure.
- The collar is developed into one to five pairs of ciliated lophophore-like arms, each housing an extension of the coelom. Arms sport cilia-covered tentacles that transport food particles to mouth.
- Only one pair of pharyngeal openings.
- The gut is U-shaped.
- Each individual zooid lives in a cylindrical zooidal tube.
- Unlike bryozoans, zooids are able to move around on the outside of the colony, attached by a strand of contractile tissue, the peduncle to a common tissue thread, the stolon. When the colony is alarmed, individuals are quickly "reeled in." Cute.
- Note that Hox genes expressed in the chordate tail are expressed in the pterobranch stalk.
- Pterobranch growth. The stolon grows from the peduncle of the ancestral zooid. New zooids bud off from the stolon. As the stolon grows, it is encased in a creeping tube secreted by a specialized zooid, the terminal bud. Other, regular zooids bud from the stolon and secrete their own zooidal tubes.
Reflect. In the year 2000, conventional wisdom held that hemichordates shared the synapomorphy of the pharynx and pharyngeal openings with chordates, but not with echinoderms, and so were viewed as more closely related to chordates. But molecular analyses recovered a strong grouping of hemichordates with echinoderms. Now that we have vetulicolians, we can see that the pharynx is, in fact, a plesiomorphy that has been (apomorphically) lost in echinoderms.)
There was another big surprise about this time.
Graptolithina:(Cam. - Carb.) first known as enigmatic fossils of the Early Paleozoic. Typically compressed into two dimensions and displaying a geometric regularity that gave them the common name "graptolite" - "writing stone."
- Very common and diverse in Ord - Sil with pelagic global distribution. The premier index fossils and bases of formal biozones of these periods.
- Discovery of three-dimensionally preserved specimens, and subsequent study of pterobranchs led to realization that graptolite rhabdosomes were colonies of zooids that secreted a proteinaceous hard structure very similar to that of pterobranchs. Implies very close relationship.
- Each zooid in the rhabdosome occupies a theca. The rhabdosome grows from an ancestral zooid whose theca is called the sicula. This takes the form of a cone with its opening facing downward. It has a long nema extending upward from its apex and a virgella extending downward from its aperture (right).
- Later thecae grow form a series called a stipe.
- BUT, because they had long been studied and used as index fossil prior to being biologically understood, they have their own set of terminology which is covered in lab. Geology majors note: You may use these some day even if paleontology isn't your thing.
Graptolite diversity: There are two major groups. (We spare you the minor groups.)
- Stipes branch many times in sequence, yielding a dendritic rhabdosome.
- The nema attaches the rhabdosome to the substrate.
- Thecae are dimorphic, with adjacent pairs of large autothecae and small bithecae (probably female and male zooids respectively.)
- Graptoloidea: (Ord. - Dev.)
- Stipes branch at most once. See lab for rhabdosome morphology terminology based on stipe angle to nema. BUT NOTE, in some, the stipes are scandent, - i.e. they grow up the sides of the nema.
- The nema attaches the rhabdosome to a floating object. (Some genera seem to have secreted siphonophore-style floats from which numerous rhabdosomes hung.)
- Thecae are uniform.
- Monograptid morphology an unbranched stipe growing up one side of the nema. Such rhabdosomes often assume spiral shapes. Perhaps they did not attach and depended on a slow sinking rate to remain in the photic zone.
- Biostratigrapher's delight: Peak abundance and diversity in Ord. - Sil. Key index fossils for this interval.
Didymograptus murchisoni from OldEarth.org
The record of well-known hemichordates is unsatisfactory in that it doesn't seem to record transitions between:
- Solitary mobile enteropneusts and colonial sessile pterobranchs.
- Swimming basal deuterostomes and squirming enteropneusts.
Herpetogaster collinsi from Wikipedia
- Two branching feeding tentacles.
- A segmented U-shaped body.
- A short stalk for attachment (temporary?) to the substrate.
Another further step may be represented by Oesia disjuncta of the Burgess Shale (Nanglu et al., 2016.) In this case, the animal looks like an enteropneust, but appears to have secreted a protective proteinaceous tube, and has a posterior "grasping organ" that might represent the first representation of the pterobranch stalk.
Yunnanozoans: A final fossil group from Chengjiang (Early Cambrian), these creatures (including Yunnanozoon (right) and Haikouella) were described in the 1990s and optimistically regarded as stem chordates or even craniates (i.e. "fish"). Recent reinterpretation by Shu et al. suggests something more interesting - that they were stem hemichordates (basal to the enteropneust/pterobranch split) with distinct collars, pharynges, and proboscis, capable os some swimming. Opinion remains divided, with Mallatt and Chen, 2003 maintaining that these are stem chordates. Nevertheless, the closer we get to the stem of Ambulacraria, the more we expect to find members whose overall form resembles that of vetulicolians.
Stereom from U C Berkeley Museum of Paleontology
- Exclusively marine: Echinoderms lack osmoregulatory mechanisms that might allow them to live in brackish or fresh water.
- Skeleton is internal test comprised of individuals plates of porous high-Mg calcite. In life, the pores are occupied by a protein matrix and dermal cells. Such skeletal tissue is known as stereom. Carbonate petrologists typically call the pores "meat holes." These are individual birefringent elements.
- Note: Echinoderm workers tend to not define Echinodermata phylogenetically. In practice, the term gets applied to any animal possessing stereom.
- One portion of the coelom develops into water vascular system. (Dissection)
- This system is passively involved in gas exchange, maintainance of posture, and locomotion.
- The latter is effected by outpouchings of the WVS that penetrate the body wall to form podia or tube feet that can be employed in suspension feeding or in locomotion, depending on the critter.
- Tube feet are arranged into five double-rows termed ambulacra. Typically, these converge on the mouth and/or anus.
- Muscles are used to pump water around the WVS, and each tube foot is equipped with small longitudinal muscles to help aim it, yet the hydrolic force of the WVS is what primarily effects movement in most echinoderms.
- The WVS obtains water from the outside. It is connnected by a calcite-reinforced stone canal that opens to the exterior in the hydropore. The hydropore is covered by a seive-like plate, the madreporite, that strains incoming water.
- The lining of the WVS is ciliated, allowing circulation of its fluid. thus, tube-feet function as gas exchange organs.
- The coelom (including the WVS) contains coelomocytes which attack foreign material and, in some cases, carry oxygen and CO2.
- Despite this weirdness, they are proper bilateralians with a mouth, flow-through gut, and anus.
- NOTE: In addition to the WVS, echinoderms also retain a normal enterocoelic coelom.
- All but most primitive have strong pentameral symmetry.
- Mutable collagen: A form of collagen that can be partially emulsified by the application of nervous action potentials is present in crinoids.
- The dominant echinoderms of the Paleozoic were suspension-feeders. Living crinoids still suspension feed, however eleutherozoans have other strategies. The feeding strategy of the first echinoderms is less clear, but recent discoveries suggest that they were deposit feeders.
Traditionally all stemmed echinoderms were lumped into "Pelmatozoa", and all non-stemmed to "Eleutherozoa". Only the latter is monophyletic. A more cladistic phylogeny of Echinodermata appears at right.
Major Groups:Early echinoderms represent a strange assemblage of experiments with different body forms. First, we survey the range of diversity, then try to make sense of it.
Helicoplacus guthi from Palaeos
- Body is helically-built (hence name) of small plates that were held together by soft tissue.
- Thought to be sessile suspension feeders - Possibly among the last "hangers-on" to the Ediacaran algal mat environment.
- Ambulacral groove spiralling along body. If, in your mind, you "unroll" a helicoplacoid, you find three ambulacra converging on a point about 2/3 up the body.
- Position of the mouth is debated, as it is not positively identified. Possibilities:
- It is at the convergence of the three ambulacra.
- It is at the top (by analogy with other sessile suspension feeders.)
- The location of the anus is a mystery.
Edrioasteroidea: (Cam. - Late Carb.)
- Sessile, benthic, attached to hard substrates like the surfaces of brachiopods, mollusks, etc.
- The body took the form of a lens-like blister or a bulb sitting on a short broad stalk.
- Have five ambulacra, like more derived forms. Close examination show that two pairs of these actually converge some distance from the mouth. Thus, only three ambulacra actually converge at the mouth. Edrios, therefore, provide a morphological bridge between the triradiate helicoplacoids and the proper, pentamerally symmetrical later echinoderms. NOTE: A line bisecting the edrio mouth and anus shows the primordial plane of bilateral symmetry that can be hard to recognize in other echinoderms.
- Paraphyletic group of basal stalked echinoderms
- Ones with brachioles (tiny tentacles surrounded by calcitic rings, only rarely preserved, visible in Gogia (right)) may actually be basal blastozoans (see below).
- Others, with simple arms (which house extensions of the coelomic cavity), may be sister taxa to Crinozoa + Eleutherozoa
Pentremites pyriformis from Humboldt State University Natural History Museum
- Ambulacra are lined with brachioles.
- Stalks present (although not all are developed for attachment to substrate.)
- Tend to have relatively complex internal breathing structures developed from the WVS.
- Main bodies called thecae may be large but typically spherical or ellispoidal without "arms' containing extensions of normal coelom.
- Three major clades:
Pentremites without brachioles from Different Directions
- Blastoidea (Ord. - Perm.):
- Strong pentameral symmetry and beautiful geometric regularity.
- The mouth is surrounded by five spiracles that act as outlets to the hydrospires and exits for gametes from gonads.
- One spiracle is larger than the others. It is a joint spiracle - anus, the anispiracle.
- Blastoid stalks allowed them to attach to the substrate.
- Evolutionary trends: Blastoids became common in the Early Carboniferous (a great time for stalked echinoderms generally) declined, then resurged in the Permian before being stomped by the Permian extinction.
The remaining groups are traditionally termed "cystoids." Non-monophyletic, but similar in having a stem that didn't terminate in a holdfast. Apparently they crawled around then stuck their thecae up when they found a good place to suspension-feed. Generally, their thecae were somewhat irregular and slightly flattened (i.e with a top and bottom.) We see two clades.
- Rhombifera: (Ord. - Late Dev).
Respired through >pectinirhombs (Rhomboidal arrays of parallel slits in theca that gave access to hydrospire-like infoldings of the WVS)
Early Ordovician to Late Devonian, respired through diplopores (paired holes giving access to WVS.)
Evolutionary trends: Rhombiferans and dipoporites were never common, but achieved their peak early - in the Ordovician, then declined slowly to be extinguished in the Late Devonian.
- Blastoidea (Ord. - Perm.):
Homolazoa:(Cam. - Dev.)
Going farther toward the base of the echinoderm tree you wold expect to find creatures that connect them to other deuterostomes. Instead, things get just ugly. Homalozoa is a problematic group of Early Paleozoic echinoderms. True apples of discord with:
- no symmetry of any kind.
- Appendages and body openings representing the ultimate paleontological Rorschach test.
- Depending on whom you ask:
What we DO know:
- Tend to have flattened thecae.
- Some with appendages including:
- aulacophore - a feeding or locomotion appendage. (See "arm" in illustration at right.)
- Stele - yet another feeding or locomotion appendage. (right)
- Although some roughly approximate bilateral symmetry (right), none possess it. Others have no obvious plane or axis of symmetry. NONE are pentamerally symmetrical.
The following groups have been regarded as "members" of "Homalozoa":
Stylophorans from Palaeos
- flattened theca
- elongate three-part stele ("tail")
- large openings to the left of the stele and at the opposite side from it.
- Numerous small pores on dorsal side.
Syringocrinus from Palaeos
- an smaller appendage, the aulacophore opposite the stele.
- elongate stele.
- large opening near the stele.
Trochocystites from Eternal Menagerie
- Bilaterally symmetrical ambulacra and mouth on dorsal surface opposite the stele.
- But the skeletal elements are not symmetrical.
- Stele is short and stiff.
- Some indications that the stele may have ended in a holdfast.
Ctenocystis from Palaeos
- Anterior and (more or less) posterior openings - mouth and anus.
- Two anterior bilaterally symmetrical ambulacra.
- Although the overall profile is more or less bilaterally symmetrical, the skeletal elements aren't.
I have only described "homaozoan" features and named a few. No homologies with other organisms have been proposed. This is where the trouble starts. Consider the stylophoran stele. It could be:
- an ambulacrum bearing feeding structure like the arm of a crinoid.
- a tail, used for propulsion, homologous to the chordate tail.
Similar things could be said about any of the openings of the theca, which could be mouths, anuses, pharyngeal slits, hypropores, etc. Into this chasm of ignorance steps the human imagination.
During the 1980s, Richard Jeffries of the British Museum interpreted the various homalozoans as ancestral to the vertebrates (making vertebrates a polyphyletic group within Echinodermata). This hypothesis (sort of) rests on his convictions about the homologies of the structures. Consider the stylophoran stele.
His conclusion: Chordates are derived from these primitive echinoderms. Indeed, in his scheme, specific homalozoans gave rise to specific chordate groups. To emphasize the propinquity of the relationship, he coined the term Calcichordate. This hypothesis of "calcichordate" phylogeny was developed in the early days of cladistics, and Jeffries does not seem to have used a parsimony analysis.
Objections to his scheme include:
- Morphological interpretation seems far-fetched.
- The transition from them to chordates involves:
- Reorganization of body for 180 deg. change of direction of movement.
- Switch from calcium carbonate to calcium phosphate skeleton.
- Even if we accept his morphology at face value, his preferred phylogeny of deuterostomes is far from the most parsimonious tree.
- Jeffries, himself, seems to approach the issue with the style of a true-believer.
When you add "calcichordates" to the mix, the basic pattern of deuterostome phylogeny seems completely up for grabs.
As of 2011, echinoderm systematists agreed that Jeffries' phylogeny is wrong. But were all over the map otherwise. Some maintained that his assessment of homology may, in part, be right. The Clausen and Smith, 2005 analysis of the stylophoran appendage suggests that it is, indeed, a locomotor appendage. Others, such as David et al., 2000, asserted that the stylophoran appendage is an ambulacrum on a crinoid-like arm, pure and simple, and that Ctenocystoidea have blastozoan-like brachioles. To them, Homalozoa is polyphyletic and its members belong to better known groups.
In the last five years some illumination came from new fossils:
- Ctenoimbricata is bilaterally symmetrical.
- Its mouth is definitely in front and its anus is definitely in the rear.
- an echinoderm-style calcite internal skeleton with stereom and
- bilateral symmetry.
But was that all? Rahman et al., 2015 modeled the feeding behavior of the cinctan Protocinctus mansillaensis to determine that its feeding apparatus was ineffective unless water was actively propelled through its oral/pharyngeal cavity by ciliary action.
Helicocystis moroccoensis from slate.com
- Helicocystis' mouth is surrounded by an array of oral plates like those of edrioasteroids, and instead of three ambulacra, it has five.
- In addition to its upper helical ambulacrum-bearing segment, Helicocystis has a body with cup resembling the theca of an eocrinoid, and a stem.
Now, finally, a coherent speculative picture of early echinoderm evolution is emerging. From a vetulicolian-like "swimming pharynx" ancestor, one can picture the evolution of a deposit-feeding ancestral ambulacrarian with an anterior ciliated feeding appendage for concentrating food that that give rise to:
- Soft-bodied enteropneust-like deposit feeders
- Deposit-feeding creatures like Ctenoimbricata with an internal skeleton, that concentrated food by means of the ambulacrum but retained the pharynx.
- Some early echinoderms became attached suspension-feeders that relied on the ambularra exclusively. (helicoplacoids)
- Among those, some like Helicocystis evolved the rudiments of five-part symmetry and the body divisions characteristic of later stalked echinoderms.
Now our great wish is for a clearer picture of the evolution of Eleuthrozoa - the non-stalked motile echinoderms.
We turn to crown-group Echinodermata in the next lecture.
- Jean-Bernard Caron, Simon Conway Morris, and Degan Shu. 2010. Tentaculate Fossils from the Cambrian of Canada (British Columbia) and China (Yunnan) Interpreted as Primitive Deuterostomes. Plos|One 2010; 5(3): e9586
- Sebastien Clausen and Andrew B. Smith. 2005. Palaeoanatomy and biological affinities of a Cambrian deuterostome (Stylophora). Nature 438, 351-354
- Bruno David, Bertrand Lefebvre, Rich Mooi, and Ronald Parsley. 2000. Are homalozoans echinoderms? An answer from the extraxial-axial theory. Paleobiology 26(4):529-555
- Diego C Garcia-Bellido, Michael S Y Lee, Gregory D Edgecombe, James B Jago, James G Gehling, and John R Paterson. 2014. A new vetulicolian from Australia and its bearing on the chordate affinities of an enigmatic Cambrian group. BMC Evolutionary Biology 14:214
- Jörg Maletz. 2013. Hemichordata (Pterobranchia, Enteropneusta) and the fossil record. Palaeogeography Palaeoclimatology Palaeoecology 398:16-27
- Jon Mallatt and Jun-yuan Chen. 2003. Fossil Sister Group of Craniates: Predicted and Found. Journal of Morphology 258(1):1-31
- Karma Nanglu, Jean-Bernard Caron, Simon Conway Morris, and Christopher B. Cameron. 2016. Cambrian suspension-feeding tubicolous hemichordates. BMC Biology 14:56
- Imran A. Rahman, Samuel Zamora, Peter L. Falkingham, Jeremy C. Phillips. 2015. Cambrian cinctan echinoderms shed light on feeding in the ancestral deuterostome. Proceedings of the Royal Society B 282(1818).
- Marcello Ruta. 1999. Brief review of the stylophoran debate. Evolution and Development 1(2): 123-135.
- Oleg Simakov, Takeshi Kawashima, Ferdinand Marletaz, Jerry Jenkins, Ryo Koyanagi, Therese Mitros, Kanako Hisata, Jessen Bredeson, Eiichi Shoguchi, Fuki Gyoja, Jia-Xing Yue, Yi-Chih Chen, Robert M. Freeman, Akane Sasaki, Tomoe Hikosaka-Katayama, Atsuko Sato, Manabu Fujie, Kenneth W. Baughman, Judith Levine, Paul Gonzalez, Christopher Cameron, Jens H. Fritzenwanker, Ariel M. Pani, Hiroki Goto, Miyuki Kanda, et al.. 2015. Hemichordate genomes and deuterostome origins. Nature 527, 459-465
- Andrew Smith and Samuel Zamora. 2009 Rooting phylogenies of problematic fossil taxa; a case study using cinctans (stem-group echinoderms). Palaeontology 52(4): 803-821.
- Andrew Smith and Samuel Zamora. 2013 Cambrian spiral-plated echinoderms from Gondwana reveal the earliest pentaradial body plan. Proceedings of the Royal Society B 280(1765).
- Jakob Vinter, M. Paul Smith, and David A. T. Harper. 2011. Vetulicolians from the Lower Cambrian Sirius Passet Lagerstätte, North Greenland, and the polarity of morphological characters in basal deuterostomes. Palaeology 54(3): 711-719
- Samuel Zamora, Imran A. Rahman, Andrew B. Smith. 2012. Plated Cambrian Bilaterians Reveal the Earliest Stages of Echinoderm Evolution. PLOS|one June 6, 2012
To Previous Lecture.