Origin of the Class Crinoidea
Bill Ausich (Department of Geological Sciences, Ohio
State University)
Ohio State University, Columbus, Ohio
21 January 1999
Who
cares about the origin of crinoids?
One
of the most intractable problems in paleontology and evolutionary biology is
understanding the origin of groups.
One example: a recent Science
(November 27, 1998) has an article on a new angiosperm that pushes back the
origin of angiosperms; the cover of the issue illustrated the fossil.
This is a hot topic. The origins of things is really tough to figure
out. Charles Darwin, in his 1859 Origin of Species, described the
origin of angiosperms as an abominable mystery. We still haven’t solved
it in 1998. Origins are one of the tough, tough issues in evolutionary
biology.
Even
the origins that we thought we figured out, like the origin of birds being Archaeopteryx
- that is out of the window now. There are all sorts of questions now
about whether that is the transitional fossil, or whether it has the transitional
morphology or not.
We
want to know where groups came from. It is intellectually
challenging. The most highly funded areas in paleontology is human
paleontology, because we want to know where we came from.
Another
of the hot topics in paleontology today is macroevolution, which is trying to
find out different things that control evolution above Darwinian natural
selection; are there different groups of organisms, clades or evolutionary
lineages, that have a propensity for success versus others that don’t?
Are there characteristics of clades that can give you clues about success in
the evolutionary record? We are worried today about global change and
environmental change and climatic change, but if we don’t understand the
clades, understanding climatic change isn’t really going to help us predict the
future. What are the key things of taxa and groups that allow you
understand patterns in the evolution of life, and why things are
happening? If we don’t understand the origins, we don’t understand the
clades, and we can’t really understand these evolutionary changes, so it’s
important for us to sort out these problems.
Why
crinoids? Because that is the group that I like. Crinoids are
unarguably the most important echinoderm group in the Paleozoic and they are
arguably one of the more important groups in the Paleozoic, in terms of the
volume of rock that consists of echinoderm and crinoid skeletons.
There
are 5 living classes of echinoderms, though some people say it is four.
There are starfish,
ophiuroids, crinoids, echinoids, and holothurians.
This is just a whisper of a once rich class-level diversity of
echinoderms There were something like 21 classes of echinoderms if you
look at the whole history of life on Earth. Crinoids are one of the more
important Paleozoic groups.
Let’s
look at what crinoids are. They are basically a starfish on a
stick. The business end of the crinoid is the crown, and the guts and
gonads are up in the calyx or cup. There are arms that engage in
respiration and feeding. The crown is elevated above the bottom by a
stalk or a column, and it’s typically attached to the bottom by some sort of
holdfast.
I
have had the opportunity to go to the ends of the Earth to try and find
crinoids. If you want to find the modern Paleozoic analogue for crinoids,
you need to hop into a submersible and go down 100-200 meters to the bottom of
the ocean, and there they will be. Modern crinoids can be observed off
Grand Bahama Island. I’ve found crinoids in Antarctica, such as on the
McMurdo Iceshelf. Crinoids are living in a benthic habitat beneath the
ice. Things that come up through the ice include crinoids. Living
crinoids can be most easily observed by OSU people, perhaps, by going to the
Bahamas, to San Salvador Island, such as Snapshot Reef. Living comatulid
crinoids can be observed there. The South Pacific is a good place to see
living crinoids. Good sites are the Great Barrier Reef and Lizard
Island. Crinoids there are really, really common, and abundant. The
modern shallow-living crinoids have lost their stalk. Instead of a stalk,
they just have a few cirri at the base of their cup or calyx, and they attach
to objects. They can crawl around with their arms, and some can also
swim. The ones that appear during the day are typically very brightly
colored, which means “I taste bad” or “I’m poisonous to eat” to potential
predators. In the Caribbean, crinoids are typically nocturnal, so they
hide during the day, and they come out to do their feeding at night.
Crinoids
begin in the Early Ordovician with a 4-circlet crinoid. The phylogeny of
crinoids has the disparids coming from rhombiferan cystoids, and they go to
cladids, and the cladids give rise to camerates and flexibles early on.
At the end of the Paleozoic, as far as we know, 1 species survived the
Permian-Triassic extinction event. They then radiate into the modern
crinoids.
Showed
some examples of typical Paleozoic crinoids from the Ordovician of Tennessee,
Mississippian of Indiana.
Some
crinoids were pseudoplanktonic, and were floating or hanging down, attached to
floating logs. Example: Jurassic
Holzmaden of Germany. Showed a crinoid example from the Pennsylvanian
of Illinois.
One
of the wonderful things about crinoids that makes them better than almost any
other invertebrate group, in terms of doing ecology, is that their feeding
apparatus is a hard-part skeleton, unlike a brachiopod or a bryozoan or a
coral, where the feeding apparatus is soft-parts.
Showed
more crinoid examples from the Mississippian of Indiana, including an unusual
form with a helically twisted stem, rather than round, life-savers or cheerios
type of stem. Steve Riddle of OSU did a Master’s thesis understanding the
functional morphology of these unusual stems.
Another
crinoid example, from the Devonian of Ohio - Arthroacantha
carpenteri - has nubs that were spine bases where spines attached, like
an echinoid or sea urchin; very unusual. Some of the more unusual crinoid
forms appear about the same time that fish become important predators. In
the Paleozoic, crinoids go nuts with spines, probably an anti-predation
feature.
More
crinoid examples, including one showing a long anal tube, with an anus at the
tip, probably for sanitation purposes, as far as we can tell; it has no
hydrodynamic advantage.
The origin of crinoids
- the last major summary of crinoids was the Treatise of Invertebrate Paleontology,
published in 1978. Their idea of the origins of all the major groups of
crinoids has no connections - all dotted lines - who knows? What I’ve
been trying to do is to connect those lines, and in doing so, one of the
questions you have to ask is what their origin is. Is this a problem
unique to crinoids? Modern popular historical geology textbooks show
figures about the evolution of plants and mammals with lots of dotted
lines. It’s difficult trying to connect these groups and understand their
origins. I’ve already mentioned one good example of an origin story that
we thought we had - Archaeopteryx from the Jurassic Solnhofen Limestone
- it is no longer a good example of a transitional fossil.
Like
a good scientist, if I’m concerned about the origin of crinoids, I need to have
multiple working hypotheses. Sir
Walter Scott in a poem suggested that the origin of crinoids was Saint
Cuthbert making beads. The folklore from northeastern England was that crinoid
columnals (or Indian beads) were actually St. Cuthbert beads
(part of a rosary). And, in a story analogous to Rip Van Winkle, when one
hears thunder, it is not Rip Van Winkle bowling, but it is St. Cuthbert forging
out beads. Maybe. Or, maybe not. I have another option.
Showed a bouquet of sea-lilies.
I’ve
made a lot of waves lately, and we’ll see where it all ends up. I want to
talk about 3 different ideas that try to understand the origin of crinoids.
Recent proposals concerning the origins of crinoids: 1) Echmatocrinus
is not a crinoid (once accepted by many as a crinoid, but now accepted by few);
2) ancestral crinoid has 4 plate circlets; 3) rhombiferan echinoderms are crinoid
ancestors.
Echmatocrinus -
The first question here - if we’re to understand the early phylogeny of
crinoids, we’ve got to understand where they came from, and then you can
connect the lines. You have to have an outgroup; you have to have a
starting point, or a zero point. Echmatocrinus has been the
starting point for crinoids since 1973. Jim Sprinkle published this beast
from the Middle Cambrian Burgess Shale. There were two specimens - the
holotype and one other specimen. He described it then as a questionable
crinoid. In the 1978 Treatise, it got basically blazoned as the
oldest crinoid, and so it becomes the outgroup. We decided to see if we
agree with that. Loren Babcock and I published a work on Echmatocrinus
just this past year. It is from the famous Burgess Shale locality.
The holotype is attached to a worm tube. You can’t really tell what the
details of the holdfast are, but we have some sort of holdfast. The body
is conical; it is very, very flimsy; it is smashed flat as a pancake; its body
was very thin. It is probably composed of plates, but boy it’s tough to
tell what they are. If anything, they are imbricated, or maybe sutured a
little bit, but more or less imbricated. If you look at this in greater
detail, you’ll see a sort of a sandy texture of the surface. This was
thought to be stereomic microstructure. I disagree with that.
Basically, it has this conical structure. It lacks a stem, unlike other
crinoids. It does have appendages that have plates. But the problem
is that there are only 8 of these. Echinoderms have pentameral
symmetry. So, an 8-fold symmetry doesn’t sound too good. Another
interesting feature is that there are soft part things preserved in alternating
fashion off the sides of these appendages. These were thought, in 1973
and 1978 and by a few people today, to be remnants of the water vascular system
- the tube feet of an echinoderm (well seen in starfish or echinoids suckered
up against the glass wall of an aquarium).
Let’s
do some tests Echmatocrinus to see if it is a crinoid, or even an
echinoderm. We’ll look at synapomorphies, which are unique features that
a group has to have, that were inherited from its ancestors, and that nobody
else have. I would argue that Echmatocrinus lacks all echinoderm
synapomorphies (1. water vascular system; 2. pentameral symmetry; 3. calcite
endoskeleton; 4. stereomic microstructure). It lacks a water vascular
system. I have a better explanation for those appendages. It lacks
pentameral symmetry. You can’t tell for sure if it has a calcite or not a
calcite endoskeleton, because Burgess Shale material has all been replaced by a
phyllosilicate. So, we don’t know what the original mineralogy was.
It did have a skeleton. Did it have an endoskeleton or an ectoskeleton?
That is a key question, but we can’t tell. It definitely doesn’t have
stereomic microstructure. Echmatocrinus doesn’t have any of the
synapomorphies of an echinoderm. How can it even be a crinoid?
Well,
let’s look at crinoid synapomorphies, and compare them with Echmatocrinus.
Crinoid synapomorphies include:
1)
pentameral symmetry
2)
a holomeric or meric column
3)
a clear distinction between the column and the cup
4)
separate, sutured plates
5)
well organized plates that are in circlets that are offset by 36˚
6)
at least 1 plate in a calyx that is in a radial position (an arm comes down,
and it is attached to a plate in that position)
7)
erect, uniserial arms
Comparison with crinoids:
Echmatocrinus lacks pentameral symmetry; it has 8-fold symmetry.
It does not have a stem at all. At best, it has imbricate plates; plates
are completely irregular; there are no plates in a radial position
anywhere. And, it has appendages. So, it must be a crinoid,
right? Well, there are lots of things that have appendages. Why do
I say it is not an echinoderm? Comparing with Burgess Shale Gogia
(an eocrinoid) and Burgess Shale edrioasteroids - these are preserved in
three-dimensional detail as a mold and cast, and they look like any other
echinoderm preserved in this kind of rock anyplace else in the Paleozoic.
Therefore, no one should be confusing Echmatocrinus with
echinoderms. Furthermore, if you look at broken plates on Burgess Shale
edrioasteroids (Walcottidiscus), you can actually see on the inside
stereomic microstructure, which echinoderms are supposed to have. Echmatocrinus
doesn’t have this. So, Loren Babcock and I have concluded that on the
basis of these features, Echmatocrinus is not an echinoderm and it is
not a crinoid. So, what is it then?
Well,
we would like to propose that it is an octocoral,
which is a long, long way away from being an echinoderm. The
synapomorphies for octocorals are:
1)
8-fold symmetry
2)
pinnate arms - they have appendages, which are called arms or tentacles which
are pinnate (they have branches)
3)
unpaired mesenteries
4)
septae
The
mesenteries and septae are soft parts, and you can’t see those. But,
aren’t all octocorals colonial, and none of them have plates? Well, yes
for 99+% of all living octocorals. There is one living species of
solitary octocoral. And, there are several species that are
pseudosolitary, with one big feeding zooid and some small ancillary zooids that
are hard to see. Furthermore, there is a family of living octocorals that
live in the deep sea off New Caledonia called the primnoid
octocorals that are plated. The primnoids are colonial - they’re not
solitary, but they have imbricate plates, and some of them have uniserial
plates along the arms. The fabric or microstructure of the surface
overlaps with what we see on Echmatocrinus. I’m not suggesting
that Echmatocrinus is a primnoid octocoral. Loren and I would
conclude that given all of these characteristics, it makes an awful lot more
sense to conclude that Echmatocrinus is some sort of an octocoral.
It has 8-fold symmetry; it lacks echinoderm skeletons; it lacks a column; it
lacks any sort of organization in the plating, etc.
So,
if we get rid of the irregular, multiplated, non-stemmed, 8-fold symmetry as
the starting point of crinoids, it changes our whole idea of the origins and
early evolution of the crinoid group.
I
happen to believe in the fidelity of the stratigraphic record. Some
people don’t. But, let’s go back to the oldest crinoid. If Echmatocrinus
is out of the picture, what’s the next oldest crinoid? It turns out to be
Aethocrinus moorei from the Tremadoc of France. It has a column;
it has differentiation of the column and the calyx; it has arms, etc. It
is a crinoid. But it is a problematic crinoid. It’s problematic
because between the clear column and the starting points of the arms, there are
4 circlets. This has caused problems, because all crinoids have a maximum
of 3 circlets of plates. This has resulted in debate over the
years. In 1969, it was argued that one has to start at the stem and count
upward, and the arms shift over, which doesn’t happen in any other
crinoid. Others said this is incorrect, and that one has to begin at the
starting place for the arms and count downward, and the last circlet is really
part of the stem. In reality, it is simply a crinoid with 4 circlets of
plates. It is very simple (to me). I’ve named the new circlet of
plates lintels. The homologies of plates that I’ve put together based on
the earliest crinoids having 4 circlets is consistent when considering many
factors, including lumen angles (when column lumen is not round, the shape has
angles) and ontogeny (microcrinoids, which are crinoids in size below 2
mm). It turns out that there are other 4-circlet crinoids, but no one
ever thought to interpret them that way before.
Back
to this phylogeny - start with a 4-circlet crinoid origin. One branch
features the loss of one interradial circlet, which produces the disparid
crinoids. The loss of another interradial circlet, the lowest circlet -
the lintels, which produced all the other groups of crinoids.
Where
did Aethocrinus come from? This is basically a dilemma. See
Sprinkle & Guensburg (1997).
I
would prefer to find the origin of crinoids among other stalked
echinoderms. This seems logical to me. Maybe even a group that even
has 4 circlets of plates. The choices now seem to be among the following:
eocrinoids,
paracrinoids,
some rhombiferan
cystoids, maybe some diploporan cystoids.
And then one goes off into more improbable things, like edrioasteroids
or holothurians or echinoids. It’s really hard to imagine origins from
the latter groups.
The
conclusion that I arrive at is that crinoids originated from some rhombiferan
cystoid that looks something like Scoliocystis (very unusual - does not
have erect arms; has a stem; the anus is on the side, instead of on the top; it
has some specialized rhomb structures; some of the ambulacra, instead of being
on the arms, are on the surface of the calyx) or from something like an early
ontogenetic phase of Caryocystites, which has a 4-circlet calyx.
Both of these are possible ancestors. Paedomorphosis or neoteny of a
juvenile form of one of these could be the origin of crinoids.
The
synapomorphies that are present in both these rhombiferans and the earliest
crinoids that support this idea are a 4-circlet calyx, and a C radial that is
smaller than the other radials, a clear distinction between cup and calyx;
there are also other characters as well.
The
other thing I’d like to discuss today focuses on a list of specialized
rhombiferan characters that occur in some crinoids. These are
characteristics that all good echinoderm experts would say are rhombiferan or
cystoid in character. These characters include: pore structures,
recumbent ambulacra, anal vent on the side of the calyx, four plates in the
lowest circlet for a very specialized type of column. Such features occur
in a variety of early crinoids. I’d like to suggest that this is a clue
to their origin.
Some
examples of this: Tetracionicrinus has four plates in the lowest circlet
and pore rhombs (rhombiferan characters, not crinoid characters). Porocrinus
has pore rhombs (this is a rhombiferan character - where the body wall is
corrugated; it’s thought to be a respiratory structure, just like your lungs,
which have a convoluted wall that increases the surface area and makes for
efficient gas exchange). Crinoids don’t need pore rhombs for respiration
because they have arms. Recumbent ambulacra - Hybocystites has
erect arms and recumbent arms, like a cystoid. Self-respecting crinoids
shouldn’t have these features, but some do. Some crinoids retain their
four plates in the basal circlet. Some have an anus on the side.
These aren’t what is expected in crinoids. What we’re seeing here are
evolutionary reversals (reappearances). Once these characters reappeared
again, they get passed on and inherited. Putative reversals occur 18 times
in 16 genera, which is 16% of all Early Ordovician and Middle Ordovician
genera. Inherited reversals occur 12 times in 9 genera (9% of EO & MO
crinoid genera). Total reversed characters: 31 times on 23 genera, almost
a quarter of all the taxa in the Early & Middle Ordovician. This is
an incredible contribution to the morphological disparity of early crinoids.
Doesn’t
the idea of evolutionary reversals violates Dollo’s Law, which states that
evolution is irreversible? Evolution is not supposed to be
reversible. We know that that is now false. A lot of work has been
done on this point on living groups where such reversals have been
documented. You can’t recreate Tyrannosaurus rex, but you can have
reversal of characters. Explanation: the genotype/genetic code is
switched off, so it is not expressed phenotypically. But the genetic code
is still present, but it is not expressed. Suppressed or silenced genes
can remain in the genotype for ~10 my. Reversals are thus expected to occur
early on in a group’s history.
When
we plot up these character reversals on a family level tree of crinoid
phylogeny, we see that the 4 plates in the basal circlet (lintels) appears in
early crinoids 4 different times in different places; recumbent ambulacra occur
3 different times; an anal vent on the side occurs 2 or 3 different times; pore
rhombs occur 4 different times; a xenomorphic column occurs 5 different
times. These cystoid characters occur scattered all across the
family-level crinoid phylogeny. The most logical, or parsimonious, answer
for what is going on here (the principle of least astonishment) does not allow
all of these complex structures to have independently evolved several different
times in distinct groups. It is easier to turn off or on a silenced
genetic code in the genotype. One sees clustering of reversal characters
in some groups, such as in the flexibles and the disparids (the hybocrinids) -
usually see scattered occurrences of these reversals, but every once in a
while, there is a cluster in a family. Statistical tests show that this
is not a random distribution. Certain groups have a propensity for
reversals, which makes sense. If a genetic code gets turned on,
downstream of that code might be other characters that are linked, that will
also get turned on. Often times, you see 2 or 3 cystoid characters in 1
crinoid genus, not just 1 reversal character. This is consistent with
this hypothesis.
Rhombiferan
cystoids are the most likely ancestor of crinoids.
Another
way of doing this is cladistic analysis, using the parsimony technique, and we
get trees. Used crinoids, eocrinoids, diploporans, and 2 groups of
rhombiferans. Used Gogia as an outgroup. Got 9 equally
parsimonious trees. It would be nice to get just 1 possible tree.
But, this never happens. Well, only rarely. Get rhombiferans as
ancestors of crinoids on the consensus trees.
Not
everyone agrees with this scenario. One thing is certain, though. Echmatocrinus
is not a player in this story, but several people insist that it is.
