vol. 164, no. 4
the american naturalist

october 2004
A Test of Simpson’s “Rule of the Survival of the Relatively
Unspecialized” Using Fossil Crinoids
Lee Hsiang Liow*
Committee on Evolutionary Biology, University of Chicago,
Chicago, Illinois 60637
Submitted December 10, 2003; Accepted June 1, 2004;
Electronically published September 7, 2004
Online enhancements: appendixes, tables, figures.
abstract: Temporally long-ranging (plong-lived) taxa have been
postulated to have unusual properties that aid their prolonged
geologic survival. Past studies have examined dispersal capabilities,
geographic ranges, and single-character morphological adaptations
as factors that may contribute to geologic longevity. Here, I test
whether long-lived fossil crinoid taxa are morphologically unusual
using a whole suite of morphological characters. I define long-lived
taxa in several explicit, comparative ways. I find that long-lived
crinoid genera and families are often less distant from mean morphologies of their crinoid orders than their shorter-lived relatives;
that is, they are relatively less specialized. I also compare the morphology of crinoid genera relative to basal members of their respective orders; mean morphological distances of long-lived genera
from basal morphologies are seldom distinct from those of their
shorter-lived relatives. I observe that long-lived crinoid genera are
less distant from mean morphologies of their temporal cohorts
compared with shorter-lived genera but not in a statistically significant manner. I conclude that long-lived crinoids are relatively
unspecialized, in the sense that they are relatively closer to mean
morphologies of their taxonomic groups.
Keywords: long-lived taxa, persistence, morphology, fossil.
Prolonged stasis in a world of change is a puzzling biological phenomenon. Extremely long-lived or geologically
long-ranging taxa have been a popular subject of discussion for paleontologists and neontologists alike ever since
Darwin ([1859] 1964) coined the term “living fossils.”
Authors including Ruedemann (1918, 1922a, 1922b),
Simpson (1944, 1953), Stanley (1979), Wake et al. (1983),
* E-mail: lhliow@midway.uchicago.edu.
Am. Nat. 2004. Vol. 164, pp. 431–443. 䉷 2004 by The University of Chicago.
0003-0147/2004/16404-40222$15.00. All rights reserved.
Eldredge and Stanley (1984), and Avise et al. (1994) have
discussed “living fossils” and the related phenomena of
arrested evolution, bradytely, and morphological stasis or
conservatism.
Long-lived taxa are commonly thought to survive
longer than related shorter-lived taxa because they are
unique, unusual, or exceptional in some significant way.
They allegedly reside in unusual habitats (Selander et al.
1970; Parsons 1994) or have distinctive morphological
features not shared by shorter-lived taxa (Ward and Signor 1983; Kammer et al. 1998). Many previous studies
on “living fossils” have characterized them as paradoxical, relictual, primitive, or special (e.g., McKenzie 1967;
Mooi 1990; King and Hanner 1998; Eisner 2003) without
exploring the phenomenon of longevity in a comparative
and quantitative manner. Here, I use a quantitative approach to examine whole clades in order to discover any
shared patterns among long-lived taxa. I use three explicit
definitions of “long lived” (see “Data Treatment”). Longlived taxa defined as such are not necessarily designated
by other authors as “living fossils.”
Crinoids (feather stars and sea lilies) belong to the exclusively marine phylum Echinodermata. Crinoids have
been chosen as an illustrative taxon for several reasons.
First, crinoids are monophyletic (Janies 2001). Second,
they are morphologically conservative enough to allow
meaningful comparative analysis. Third, they are diverse
enough to provide large samples for quantitative study.
Fourth, they can be divided into recognized taxonomic
subgroups for further comparisons without sacrificing the
adequacy of sample sizes. Fifth, there exists a large morphological database of fossil crinoid species and their first
and last geologic appearances, sampled quite evenly across
all crinoid subgroups (Foote 1999). Sixth, certain crinoids
are considered “living fossils” (Roux 1987; Heinzeller et
al. 1996; Ameziane and Roux 1997; Laille et al. 1998).
Others are thought to exhibit extreme morphological conservatism (Simms 1988) or phenotypic bradytely (Kammer
2001). Seventh, the crinoid fossil record spans almost the
entire Phanerozoic, beginning definitively in the Ordovician, peaking in taxonomic richness during the Carbon-
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The American Naturalist
iferous (Lane and Webster 1980; Hess et al. 1999; Guensburg and Sprinkle 2003), continuing through the Cenozoic
into the Recent (Ameziane and Roux 1997). However, an
overwhelming majority of crinoid genera originated and
went extinct during the Paleozoic (Moore and Teichert
1978). This minimizes problems arising from one-sided
range truncations, where taxa originating closer to the
Recent have shorter geologic durations due to unfinished
histories. Last, crinoids have relatively high fossilization
and preservation potentials. Although fossil crinoid specimens are frequently disarticulated, confident assignments
to species or at least genus are often possible (Ausich et
al. 1999; Ausich and Kammer 2001).
Simpson implicitly took a comparative approach when
he wrote about the “rule of the survival of the relatively
unspecialized” (1944, p. 143). He thought that unspecialized subgroups of a clade seem to persist for longer
periods of geologic time but did not explicitly define “specialization.” Here, I quantify specialization by comparing
individual morphologies to a group mean; the closer a
morphology is to a group mean, the less specialized it is.
I ask whether long-lived genera (taxa A and B in fig. 1A)
in any given crinoid order occupy regions of morphospace
that are random with respect to the mean morphology of
that order. Could survival be correlated with morphological bizarreness or a deviant morphology (fig. 1B, taxon
A)? Or would long-lived genera have morphologies close
to the mean morphology (fig. 1B, taxon B)?
I find that the morphologies of long-lived crinoid genera
are, in general, closer to mean morphologies than shorterlived genera in the same order. This is in agreement with
Simpson’s rule of the survival of the relatively unspecialized. The “long-lived, deviant” quadrants (LL-t in fig. 1C)
of morpho-duration plots (fig. 1B, 1C) are often empty
and the members in the “long-lived, unspecialized” quadrant (LL-b in fig. 1C) are closer to mean morphologies
than expected by chance.
Similarly, but from a completely different conceptual
perspective, I ask whether long-lived crinoid genera in any
given crinoid higher taxon (e.g., suborder, order) occupy
regions of morphospace that are random with respect to
a basal morphology of that higher taxon. I find that mean
morphological distances of long-lived genera from basal
morphologies are seldom distinct from those of their
shorter-lived relatives.
In this article, I also discuss the influence of taxonomic
hierarchy and temporal divisions on the observed patterns,
followed by the relationship between mass extinctions and
longevity. Finally, I examine the potential biases in this
study and consider various definitions of “long lived.”
Material and Methods
There is no available phylogenetic framework for comparing rates of character transformation in the global pool
of fossil crinoids. Likewise, there are no detailed samples
of crinoid lineages in a stratigraphic column for investigating character reversals, convergence, or the lack thereof.
However, data for a quantitative, comparative study are
available as follows.
The Data
I use previously compiled data from a database containing 1,195 crinoid species representing 752 genera, together with their first and last fossil appearances and 90
morphological characters from the column, cup, and
arms (Foote 1999; http://geosci.uchicago.edu/∼foote/
MORPHDAT/CRINOID.DAT). In addition, I code seven
crinoid genera not already represented in this database
(app. A in the online addition of the American Naturalist). I follow the character system used by Foote (1999),
which in turn is based on the traditional homologies used
in the Treatise on Invertebrate Paleontology (Moore and
Teichert 1978). These seven genera are coded using photographs and descriptions from Moore and Teichert
(1978); Schubert et al. (1992); Ausich (1998) and Guensburg and Sprinkle (2003). I choose either the earliestappearing taxa or what are believed to be ancestral taxa
by crinoid workers (to the best of my knowledge of the
current literature) as taxa bearing basal morphology (table C1 in the online edition of the American Naturalist).
Multiple taxa are used as basal taxa when there is uncertainty in the literature over the identity of the most
basal taxon for a group.
The characters are binary, ordered multistate, or unordered multistate. Not all characters are applicable to all
species. For instance, most comatulids and all of those
coded in Foote (1999) have no columns, and hence their
columns characters are coded as “inapplicable.” The morphological characters used here are not assumed to be
strictly homologous but are assumed to reflect only general
fossilizable morphology determined consistently within
the crinoid bauplan (Foote 1999).
The geologic duration for each taxon (henceforth “duration” in millions of years [Ma]) is the difference between
the bottom of the geologic stage of the first occurrence to
the top of the stage of the last appearance of the taxon.
Relative durations rather than absolute durations are of
greatest importance in this comparative framework. The
timescale is based mainly on Harland et al. (1990), but
other references are also used for stratigraphic correlation
(see Foote 1994a, p. 322). Genera with first and last appearances not resolved to stage level are omitted (79 of
Survival of Unspecialized Crinoids 433
Figure 1: A, Schematic diagram showing the geologic ranges (solid lines) of 10 related taxa. The dotted lines project the multivariate morphology
of each of the taxa onto a two-dimensional plane. The open circle marks the location of the mean morphology of all 10 taxa considered. By
plotting the distances between the open circle and each taxon versus their durations, a morpho-duration plot as shown in B is obtained. In A
and B, A represents a long-lived taxon that is morphologically deviant relative to the group mean, and B represents a long-lived taxon that is
not deviant relative to the group mean. Dotted lines in B show the median duration value (Med), midrange duration value (Mid), and the
duration greater than those associated with the 10% most long-lived genera (10-g). C shows the naming of morpho-duration plot quadrants
that will be used in this article. Quadrant SL-t houses the shorter-lived, deviant taxa; SL-b houses the shorter-lived but nondeviant (unspecialized)
taxa; LL-t houses the long-lived, deviant taxa; and LL-b houses the long-lived but nondeviant taxa (unspecialized). The deviation quantified
can be relative to either a group mean or a basal morphology.
752 genera; ∼10%). Results do not change qualitatively if
these genera are included.
Crinoid family durations are extracted from an updated
version of J. J. Sepkoski’s family database (Sepkoski 1982;
personal communication, M. Foote), Benton’s Fossil Rec-
ord 2 (1993), and updated using Webster’s online database
(Webster 2003) where inconsistencies due to taxonomic
revisions or range extensions are apparent. Average and
median genus durations in families are calculated based
on the genera sampled in Foote (1999). It should be noted
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The American Naturalist
that family durations are less updated than genus durations, but durations in each set are updated to the same
extent.
Data Units
I use the genus as the basic data unit. I mainly analyze
crinoid genera grouped in higher taxa (orders and cladid
suborders) and compare results from these separate analyses. Where sample sizes permit, I analyze the data grouped
as families. Genera are convenient units of analysis because
data on their fossil durations are more complete than data
for species. The morphological distances between fossil
crinoid genera are more than the morphological distances
among species within the same genus (personal communication, M. Foote), suggesting there is nothing unusually problematic with the genus-level justification.
I focus most of the analyses on genera grouped as orders
because multivariate morphologies between different crinoid orders can be dramatically different. Characters relevant to one order may be wholly inapplicable to another,
making comparisons dubious because only a few characters can be used to calculate distances. Another reason
to use orders instead of suborders or families is to keep
genus sample sizes large enough for analyses to be robust
to resampling (table 1). The sample sizes of genera in
families and most suborders are mostly too small.
Following Foote (1999), I delineate orders (table 1)
based mainly on the Moore and Teichert (1978) treatise.
This grouping is still widely accepted today (Simms 1999).
I omit Encrinida and Hybocrinida for order-level analyses
because they were both represented by !10 species and
only four and five genera, respectively, in Foote (1999).
The cladids are a very large and diverse order. For the sake
of comparability of sample sizes and morphological ranges
with other orders, I divide them in two ways for most of
the analyses, in addition to analyzing them as an entire
set (table 1). First, I divide them into Ordovician to Devonian, lower Carboniferous, and upper Carboniferous to
Permian subsets. There is little overlap of cladid genera
between these time intervals. Second, I divide them into
the suborders Cyathocrinina, Dendrocrinina, and Poteriocrinina (Moore and Teichert 1978; Ausich et al. 1999).
It should be noted that current researchers no longer believe that Dendrocrinina and Poteriocrinina are monophyletic (e.g., Simms 1999).
Data Treatment
Most genera (71%) in the database were coded with one
species. Where genera are represented by more than one
species (or families by more than one genus), an “average”
genus (or family) was determined by taking averages of
the character states for each character. Characters are averaged by: (i) taking the arithmetic mean of binary and
ordered characters and (ii) taking the modal value of unordered characters unless the character states are equally
common, in which case a state is chosen randomly. When
there are more unknown or inapplicable states than known
ones among the species representing a genus, the character
is coded as “not applicable” for that genus. However, if
known states are in the majority, they are treated as in (i)
and (ii) but averaged as if there are no nonapplicable states.
Detailed information on the morphological characters and
sampling issues can be found in Foote (1994a, 1994b,
1995a, 1995b, 1999).
I define long-lived taxa in three ways for the purpose
of analysis: first, taxa having durations greater than the
median duration (Med) of the taxa within the group being
examined; second, taxa having durations greater than the
midrange (Mid) duration of the same; and third, the most
long-lived 10% of genera within the group (fig. 1B).
Morphological Deviations from Group Means
I convert the original discrete character matrix for genera
into a euclidean distance matrix. Missing or nonapplicable
characters are not used when calculating distances (per
taxon pair). Subsequently, I perform principal coordinates
analyses (PCO; Gower 1966) by executing principal components analyses on the euclidean distance matrix subdivided into (sub)orders and time intervals. I then calculate morphological distances for each genus by taking
the sum of absolute differences between the genus PCO
scores and the mean PCO scores for the (sub)order or the
time interval, and I term these “morphological deviations.”
The improvement in fit between pairwise distances of discrete characters and principal coordinate scores trails off
after the first 10 PCO scores (see Foote 1999, his fig. 44).
Thus, only the first 10 PCO scores (accounting for about
75% of the variance) are used in all calculations.
I also summarize morphology using nonmetric multidimensional scaling (NMDS), where only rank order information of the distance matrix is used (Kruskal 1964).
I calculate NMDS-based morphological deviations for each
genus with respect to their order mean of NMDS scores,
as done with the PCO scores described above. Results using
NMDS are not qualitatively different from those using
PCO and are not reported here. Concordant results from
these different methods with different assumptions indicate that patterns observed are not affected by the multivariate method used.
To summarize morpho-duration relationships graphically, I plot the resulting morphological deviations versus
durations of respective crinoid taxa (morpho-duration
Table 1: The crinoid orders (and suborders of cladids) represented in the database and the morpho-duration plot distributions of their genera
Subclass, order, suborder
Articulata:
Roveacrinida
Cyrtocrinida
Comatulida
Millericrinida
Isocrinida
Inadunata:
Cladida:
All
Cyathocrinina
Dendrocrinina
Poteriocrinina
Disparida
Camerata:
Diplobathrida
Monobathrida
Flexibilia:
Taxocrinida
Sagenocrinida
All genera
N
R
SL-b SL-t LL-b LL-t
Med
(Ma)
Med
proportion
Mid
(Ma)
Mid
proportion
10-g
(Ma)
10-g
proportion
r
12
28
36
8
17
K
P(m)–Pale
T(u)–Mi
T(l)–J(u)
T(l)–Mi
.38
.32
.64
.13
.70
.23
.36
.11
.75
.18
.23
.14
.23
.13
.12
.13
.18
.00
.00
.00
18
25
24
10
37
.176
.000
.000
.000
.000
24
47
52
34
120
.249
.115
.001
.000
.151
41
88
67
65
206
.178
.168
.023
.000
.150
.026
⫺.309
⫺.557***
⫺.683*
⫺.206
262
71
83
112
37
34
179
80
O(l)–P
O-D
Carb(l)
Carb(u)-P
O(u)–P(m)
O(u)–P(m)
.73
.80
.86
.79
.76
.56
.37
.58
.21
.13
.04
.14
.08
.06
.36
.38
.03
.07
.1
.04
.03
.35
.06
.03
.02
.00
.01
.04
.14
.03
.02
.03
20
13
33
20
14
15
20
15
.003
.002
1.000
.000
1.000
.001
.000
.890
55
45
53
57
54
45
53
43
.958
.342
.750
.993
1.000
.320
.010
.427
41
41
59
42
93
41
42
41
.809
.045
.752
.962
1.000
.374
.003
.068
⫺.203***
⫺.296**
⫺.084
⫺.131
⫺.088
.026
⫺.111
.031
38
80
O
O(m)–Ste
.82
.60
.10
.30
.08
.08
.00
.01
11
21
.000
.000
33
47
.046
.129
30
46
.023
.053
⫺.277
⫺.223*
11
48
671
O(m)–Ste
O–P
O–Mi
.25
.29
.78
.38
.64
.01
.23
.03
.21
.13
.03
.00
18
14
116
.000
.990
.709
26
60
18
.182
.403
.451
46
51
50
.287
.946
.994
⫺.263
.065
⫺.030
Note: N p number of genera sampled, and R p sampled geologic ranges (J p Jurassic, K p Cretaceous, Mi p Miocene, O p Ordovician, Pale p Paleocene, P p Permian, T p
Triassic, Ste p Stephanian; l, m, u in parentheses indicate lower, middle, and upper, respectively). Columns SL-b–LL-t are the quadrants named in figure 1C, and numbers indicate their
proportion occupation. Med, Mid, and 10-g are cutoff points for durations of long-lived genera defined in “Material and Methods.” Numbers in the “proportion” columns indicate the
proportions of rarefied samples of shorter-lived genera that are less deviant (or more unspecialized) than long-lived genera for each definition of long lived. r p rank order correlation
coefficient between morphological deviations and durations from the empirical data. Note that the total number of genera is greater than the orders summed because of the uncertain higher
level taxonomic assignments of some genera. The last row shows the same values for all genera considered.
* P ! .1.
** P ! .05.
*** P ! .01 when comparing with randomized data.
Survival of Unspecialized Crinoids 437
plots as in fig. 1B). I also plot character states versus durations for each character within each order.
I compare means of morphological deviations of each
set of long-lived taxa with rarefied samples of their corresponding shorter-lived relatives. This is because apparent
patterns may be due to sampling artifacts (there are fewer
long-lived taxa than shorter-lived ones). For instance, if
there are four long-lived taxa in an order, defined as Mid,
I randomly sample, without replacement, four taxa from
the corresponding shorter-lived pool. This is repeated
10,000 times for each order and for each definition of long
lived. Means of morphological deviations of the 10,000
rarefied samples of shorter-lived taxa are compared with
the means of long-lived taxa to see how often the latter
have smaller values than the prior.
I also calculate rank order correlation coefficients between morphological deviations and durations. To compare empirical values with a null expectation, I use the
method “randomization” by resampling with replacement
from morphological deviations. I then do the same for
durations separately, drawing the number of data pairs
corresponding to the number of genera (or families) represented in the empirical data of the higher taxon (order,
subclass, or class) 1,000 times to form null distributions
(Efron and Tibshirami 1993). I calculate the same rank
order correlations for the randomized data sets and compared them with the empirical data sets. Because the resulting morpho-duration plots appear exponential, I also
fit exponential decay curves to obtain best-fit parameters
(k and m in y p me⫺kx). This is to provide an alternative
to comparing distributions using a linear fit as implied by
the calculation of correlation coefficients. Conclusions are
no different using a linear fit and are not further reported.
As an alternative test, I divide the morpho-duration plots
into four equi-area quadrants to conduct x2 tests. I use the
most and least deviant and the shortest- and longestlived genera to delimit the occupied area on the plot. Then
I divide this area into four equi-area quadrants by drawing
a vertical line thorough the midrange duration and a horizontal line through the midrange morphological deviation
(fig. 1C). I then compare the density of the four quadrants
of empirical and randomized data sets using x2 tests.
Morphological Deviations from Basal Morphology
To investigate the morphological deviation of genera from
putative basal morphologies of their orders, I calculate
pairwise euclidean distances from data on raw morphological characters. I also calculate Manhattan and Canberra
distances (Sneath and Sokal 1973); results did not differ
from euclidean distances and are not further reported. I
then plot the distances of each genus from the basal member(s) versus the duration of each genus (fig. 1B). I compare 10,000 rarefied samples from shorter-lived taxa with
long-lived taxa as described above for mean morphologies
in each case. I also calculate and compare rank order correlation coefficients from empirical and randomized data
sets as described above. Last, I also perform x2 tests as
described above.
Results and Discussion
Morphological Deviations from Group Means
There are wide ranges of morphological deviations of
shorter-lived genera from their order means. Longer-lived
taxa have smaller ranges of morphological deviations from
the order means (fig. 2). Most taxa are shorter lived and
morphologically average. In other words, the bottom left
of morpho-duration plots (SL-b) are often the most dense
(table 1; fig. 2).
When the definition of long lived is taken as having
a duration greater than the median value (Med), 12 of
17 (sub)orders have long-lived genera that at best have
a 0.003 proportion chance of being more deviant than
shorter-lived genera (table 1). In other words, in 12 of
17 cases, long-lived taxa are less specialized when compared with shorter-lived taxa. If the Mid definition is
taken with a 0.1 proportion chance as a cutoff, six of 17
cases have long-lived genera that are less deviant than
shorter-lived genera. Finally, if we take the last definition,
10-g, there are 10 of 17 cases. Note that temporal and
suborder divisions of cladids both have morphologically
deviant long-lived taxa, but these cases cannot necessarily
be taken as independent.
I conclude that long-lived genera are often less specialized than expected. However, as the definition of long
lived becomes more stringent such that fewer longer-lived
taxa are included (from a most relaxed definition, Med,
to more stringent definitions, Mid and 10-g), the above
conclusion holds true for fewer cases.
However, when all crinoid genera are examined in concert, long-lived genera are more deviant, under the 10-g
definition of long lived, than rarefied samples of shorter-
Figure 2: A, Morphological deviation of each monobathrid genus from its order mean versus the duration of each genus. B, Morphological deviation
of each disparid genus from its order mean versus the duration of each genus. Solid lines show the delimiting of the plot into four equi-area
quadrants (as in fig. 1C). Dotted lines show the median duration value (Med), midrange duration value (Mid), and the duration greater than those
associated with the 10% most long-lived genera (10-g).
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The American Naturalist
lived ones. Using the definitions 10-g and Mid, the chances
of being deviant are even (table 1). Note that fewer characters can be universally compared when all genera are
lumped in a single analysis and that this shortcoming may
obscure potential patterns.
Correlations between morphological deviations and
durations are negative for 13 of 17 cases (table 1), and
five of those 13 are significant at a P 1 .1 level. This test
is sensitive to the density of the lower left quadrant; thus
there are few significant correlations. However, the direction of the correlation agrees with the previous observation that longer-lived taxa are less morphologically
distant from the mean morphology of their group than
shorter-lived taxa when using a rarefaction approach. In
contrast, none of the cases are significantly different from
random using a x2 test (data not shown), indicating that
the pattern is blurred when the distribution within each
quadrant is ignored. However, the distribution of taxa in
each of the four quadrants gives us a quick view of the
emptiness of the long-lived, deviant (LL-t) quadrant (table 1; fig. 1C).
Plots of character states of each character versus durations for each order show that the vast majority of rare
character states are associated with shorter durations (plots
not shown). Viewed alternatively, morphologically deviant
taxa suffer extinction sooner.
Morphological Deviations from Basal Morphology
Long-lived taxa typically do not appear very different
from taxa having basal morphologies (LL-t is often very
empty; table C1 in the online edition of the American
Naturalist). The majority of genera are present in the
quadrant SL-b in many of the crinoid (sub)orders examined, irrespective of the basal taxon used (table C1).
Despite that, rarefied samples of shorter-lived taxa show
that long-lived taxa do not necessarily have morphologies
that are less deviant from ancestors than shorter-lived
taxa. Morphological deviations from basal members are
highly contingent upon the morphology of the putative
basal member used.
I illustrate with Sagenocrinida as an example (fig. C1
in the online edition of the American Naturalist) of how
the distribution of genera in the morpho-duration plot
shifts according to the basal taxon used as a reference.
Protaxocrinus has been confidently placed as a model of a
direct ancestor to the clade of sagenocrinids (Lane 1978).
The cloud of points shifts from being closer to the basal
morphology in the comparison with Protaxocrinus to being
in a more distant position with Cupulocrinus, which is
ancestral to Protaxocrinus (Moore and Teichert 1978).
However, when a very distant basal taxon is used, the
spread of genera decreases because they are all distant from
the reference taxon (Glenocrinus), and few characters are
comparable between Glenocrinus and Sagenocrinids. This
explicitly illustrates that when long-lived forms are assessed for their primitiveness, our conclusions are affected
by how far removed the basal states are from the taxa
being compared. For each of the basal taxa and each definition of long-lived taxon used, long-lived Sagenocrinids
tend to be more deviant than rarefied samples of shorterlived forms at least 82% of the time (table C1), even
though a x2 test does not indicate any significant difference
from random (data not shown, as with all the other comparisons in other taxa).
Influence of Taxonomic Hierarchy
Analyses done at different taxonomic ranks potentially
show different patterns of morpho-duration plot occupation. For family-within-order comparisons, as fewer
long-lived taxa are included (from Med to the more stringent definitions Mid and 10-g), the observation that longlived taxa are morphologically less deviant holds true less
often (table 2), as with genus-within-order comparisons.
Under Med, Articulata, Cladida, Disparida, Camerata, Sagenocrinida, and Flexibilia (Sagenocrinida and Taxocrinida) have long-lived families that are likely to be less specialized than shorter-lived ones 9% of the time at most
(table 2, six of eight cases).
The distributions are not significantly different from
null distributions of random expectations using randomized data (table 2) and a x2 test (data not shown), except
in cladid families. This is again despite the fact that SL-b
is the most densely filled quadrant and LL-t the sparsest,
and rank order correlations of morphologies and durations
are negative in all cases.
Patterns can also be modified depending on the inclusiveness of the higher taxon. The pattern of morphoduration plot occupation for orders by either genera or
families remains qualitatively similar (e.g., Cladida, Disparida, and Monobathrida), but there are are exceptions
(e.g., Sagenocrinida; cf. tables 1, 2). Also, when both camerate orders, Diplobathrida and Monobathrida, are combined in a single analysis, the quadrant SL-t becomes 15%
more occupied than when Monobathrida is considered
alone, at the expense of SL-b and LL-t (table C2). This
illustrates the inherent problem of empirical morphospaces where sampling strongly influences the shape of the
space (McGhee 1999).
Temporal Divisions and Mass Extinctions
Dividing the genera into geologic periods instead of
taxonomic grouping illustrates that the occupation of
morpho-duration plot is quite stable through time (fig.
Survival of Unspecialized Crinoids 439
Table 2: Crinoid families and their morpho-duration plot distributions
Med
Med
Mid
Mid
10-g
10-g
SL-b SL-t LL-b LL-t (Ma) proportion (Ma) proportion (Ma) proportion
Group
N
Articulata
Cladida
Disparida
Monobathrida
Camerata (pMonobathrida ⫹
Diplobathrida)
Sagenocrinida
Flexibilia (pSagenocrinida ⫹
Taxocrinida)
Crinida (pall families)
28
59
17
18
.54
.64
.47
.33
.29
.15
.29
.17
.04
.05
.06
.17
.14
.15
.18
.33
45
32
42
41
.000
.000
.080
.533
94
81
89
44
.261
.724
.477
.537
145
104
161
83
.760
.946
.761
.116
⫺.23
⫺.23*
⫺.06
⫺.17
29
11
.48
.18
.31
.27
.00
.09
.21
.46
17
88
.088
.011
66
81
.032
.021
83
127
.095
.695
⫺.29
⫺.36
14
147
.21
.59
.29
.33
.07
.05
.43
.04
72
39
.022
.117
81
122
.021
.985
128
121
.216
.998
⫺.43
⫺.01
r
Note: N p number of families sampled. SL-t–LL-t are the quadrants as named in figure 1C, and numbers indicate their proportion occupation. Med, Mid,
and 10-g are cutoff points for durations of long-lived genera as defined in “Material and Methods.” Numbers in the “proportion” columns indicate the
proportions of rarefied samples of shorter-lived families that are less deviant (or more unspecialized) than long-lived families for each definition of “long
lived.” r p rank order correlation coefficient between morphological deviations and durations from the empirical data.
* P ! .1 when comparing with randomized data.
C2 in the online edition of the American Naturalist). Just
as in previous analyses when genera are grouped according
to orders, genera in each period are mostly short lived.
However, rarefied samples of shorter-lived genera through
each period inform us that the long-lived taxa can be more,
less, or equally deviant compared with shorter-lived taxa
of an equivalent sample size (table C2).
Genera that are extremely long lived within each order
are also more likely (Wilcoxon rank test a p 0.05, P K
.0001) than other genera in the database to have passed
through one or more mass extinctions (Raup and Boyajian
1988), even though passing through mass extinctions does
not necessarily ensure persistence (e.g., Monachocrinus and
Alisocrinus; data not shown).
Post-Paleozoic orders (Isocrinida, Comatulida, Cyrtocrinida) are more likely to have longer-lived families than
Paleozoic ones. This is consistent with the trend of a secular increase in longevity through time (Gilinsky 1994),
which is probably due to a decrease in extinction rates
throughout the Phanerozoic (Raup and Sepkoski 1982).
It also corroborates the claim that the likelihood of the
occurrence of “living fossils” or long-lived taxa increases
with time (Holman 1999).
Potential Biases
The database has many inapplicable character entries and
unknown characters. These entries result from the effort
to sample as many crinoids as possible and to include
characters that describe them both comprehensively and
comparatively. One concern expressed in earlier work is
that long-lived taxa may simply be characterized by fewer
characters and are likely to be results of taxonomic lumping (Schopf et al. 1974). However, a plot of the percentage
of inapplicable entries and unknown characters shows no
consistent relationship with the duration of sampled genera (fig. C3 in the online edition of the American Naturalist; Spearman’s rank correlation r p 0.09, P p .99).
Plotting the same data separately for each order yields the
same results (data not shown).
Geologically older stratigraphic stages are longer than
more recent ones (Sepkoski 1975), so that longer apparent
durations may be related to early first appearances. No
such problem exists in this database. On the contrary, laterappearing (geologically younger) genera tend to be somewhat longer-lived, although the correlation is not significant (Spearman’s rank correlation r p 0.264, P p .99;
data not shown).
Long-lived genera are represented by significantly more
species than genera with shorter durations (Wilcoxon rank
test a p 0.05, P K .0001; one-tailed t-test a p 0.05,
P K .0001 ). This could potentially be a problem for the
conclusions drawn because long-lived genera could have
had their morphologies “averaged out” by multiple representative species. However, when single random species
are used as representatives for each long-lived genus (instead of averaging multiple species), no change is seen in
the patterns (data not shown).
Finally, some of the post-Paleozoic crinoids have truncated range distributions; that is, their histories have not
ended because they are still extant. However, more Paleozoic crinoids are represented at both ordinal and genus
levels in this study (table 1). Moreover, most of the postPaleozoic crinoid genera represented are already extinct
(Foote 1999). Those that are extant (Isocrinus, Chladocrinus, Cyathidium) are already longer lived than the extinct
taxa, except in the case of Comatulida, where the extant
440
The American Naturalist
other definitions to delimit long-lived taxa: midrange or
median duration values, an obvious break in the duration
distribution of the group in question, the ability to pass
through mass extinctions, or statistical tests for outliers
(e.g., Grubb’s test; see Sokal and Rohlf 1995; fig. 3). “Living
fossils” or clades that persist for long periods displaying
little evolution (as defined by Stanley 1979) sometimes but
not always are also long-lived taxa (app. B in the online
edition of the American Naturalist). Similarly, longest-lived
genera do not necessarily reside in long-lived families (defined as the most long-lived 10% of families in the data
set), although they will if the definition of a long-lived
family is relaxed.
In summary, longevity is relative and dependent on taxonomic inclusiveness. These important axioms are often
neglected in articles that address extreme persistence or
morphological conservatism.
Conclusions
Figure 3: Histogram shows the frequency of occurrence of long-lived
genera of monobathrids, depending on the definition of “long lived.”
The categories 5%, 10% (p10-g), 15%, and 20% are percentages of the
most long-lived genera with respect to all the monobathrids sampled.
The change in frequency is not even because some genera have the same
calculated durations. Med p taxa having durations more than the median
value. Mid p taxa having durations more than the midrange value.
Br p taxa occurring at durations greater than the break in longevity
distribution. Com p monobathrid genera identified in appendix B in the
online edition of the American Naturalist (combination approach).
Me p taxa passing through at least one mass extinction. G(.1) and G(.05)
are genera that pass Grubb’s test (Sokal and Rohlf 1995) at P p .1 and
.05, respectively. 1.5UQV refers to genera having durations 11.5 times
the seventy-fifth percentile of the genera. Note that Com does not necessary equal Br, although in the case of monobathrids, they are equivalent.
Hatched bars indicate categories that were quantitatively analyzed in this
article.
genera Atelecrinus, Pterometra, and Himerometra are considered shorter-lived.
Explicit Definitions of Long-Lived Taxa
Thus far, long-lived taxa have been defined in three explicit
and distinct ways (hatched bars, fig. 3). Other definitions
of long lived can lead to selection of different sets of genera
(fig. 3 with Monobrathida as an example). As expected,
identifying a greater percentage of genera as long-lived
increases the number of long-lived genera. However, the
steps of increase are not always equal even though I show
increases in steps of 5% (fig. 3; 5%–20%). This is because
genera occasionally have the same numeric value of duration (in this case, many that fall in the 20% category
are listed as having a duration of 34 Ma) due to issues of
stratigraphic resolution of age dating. We can also use
Longevities of crinoid species and genera have been linked
to their ecology (Baumiller 1993; Kammer et al. 1997,
1998). This research extends the scope of those studies to
include post-Paleozoic crinoids and multiple morphological characters (cf. Baumiller 1993). I also use multiple
analytical methods to check the robustness of the relationship between morphology and longevity in order to
decrease the likelihood that conclusions drawn are artifacts
of the methodology employed.
The following general conclusions can be drawn. First,
most taxa (genera and families) are short lived and “average” so that SL-b (fig. 1C) is the most densely filled
quadrant of the mopho-duration plot. In contrast, the
sparsest quadrant is LL-t, which implies that experiments
in morphology are usually not long lived. Second, longlived genera within orders are often less morphologically
deviant or less specialized than expected when compared
with rarefied samples of corresponding shorter-lived genera. In other words, long-lived genera are not only not
unusual, some are unusually average! Third, patterns of
morphological deviations from basal morphologies versus
durations are unclear. Details of morpho-duration plot
occupation vary according to the basal member employed
in the analyses. Despite this uncertainty, the short-lived,
nondeviant quadrant of the morpho-duration plot (SL-b)
is still much denser than the long-lived, deviant quadrant
(LL-t), in general. Fourth, morpho-duration plot occupation through time (as in the case for generawithin-order and families-within-order) follows the density order of SL-b, SL-t, LL-b, LL-t. This pattern holds
true even though comparisons of rarefied samples do not
show that long-lived genera are comparatively more or
less deviant as a rule. Fifth, taxonomic ranks and inclu-
Survival of Unspecialized Crinoids 441
siveness of higher taxa are critical factors when discussing
longevity because identities of long-lived taxa may dramatically change according to these factors. Last, identities
of long-lived taxa may change with respect to which definitions of longevity are used. This may or may not (as
was the case for this article) change conclusions being
drawn on long-lived taxa.
Small size, ecological tolerance, wide geographical
ranges, large population sizes, planktotrophic larvae, and
deeper depth distributions may lower extinction risk (Boucot 1975; Buzas and Culver 1984; Jablonski 1986; Stanley
1986; Raup and Boyajian 1988; Schopf 1994; Oji 1996;
Jeffery and Emlet 2003). Also, recovery genera of the postPaleozoic seem to have greater temporal longevities (Miller
and Foote 2003). Perhaps extinctions are not biologically
random (Jablonski 1989, McKinney 1995), which implies
that persistence is not, either. Based on the results of the
current study, I rule out the idea that long-lived genera
are morphologically deviant or unusual when compared
within the realm of an order.
There are of course many unanswered questions. This
study focused on persistence, but there is no available
information on actual rate of character evolution. Do longlived taxa experience rapid rates of character reversals or
zig-zag evolution (Henningsmoen 1957), such that apparent persistence is only a sampling artifact, or does persistence necessarily mean slow change or cryptic change
(Knowlton 2000)? Can the morpho-duration plot patterns
in crinoids be extrapolated to other organisms? To remain
similar enough to an ancestor so a lineage retains a single
taxonomic identity requires whole chains of more or less
identical events (Gingerich 2001), but what causes these
identical developmental events to occur generation after
generation? What relative proportions do ecology, biogeography, morphology, and phylogenetic inertia contribute
to longevity? Patterns and statistical correlations do not
imply causation; tests using techniques from fields ranging
from paleontology and phylogenetics to molecular biology
and genetics need to be designed to investigate the existence and workings of mechanisms that promote longevity.
Acknowledgments
My deepest gratitude to S. Lidgard, who dedicated his time
and insights to this article. I thank M. Foote for sharing
his database and expertise and B. Chernoff, D. Jablonski,
J. Martin, L. Van Valen, and P. Wagner for their advice.
F. Gahn painstakingly checked the character matrix. I also
thank W. Ausich, T. Baumiller, K. Boyce, F. Gahn, P. Harnik, G. Hunt, A. McGowan, R. Price, and F. Schram for
reviewing and discussing various versions of the manuscript. J. J. Emerson and C. Simpson helped with computing issues. A special note of thanks to C. Marshall, who
suggested improvements in methods of analyses and reviewed the manuscript in great detail.
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