Increasing morphological complexity in multiple
parallel lineages of the Crustacea
Sarah J. Adamowicz*†, Andy Purvis*, and Matthew A. Wills‡§
*Division of Biology, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, United Kingdom; and ‡Department of Biology and Biochemistry,
University of Bath, The Avenue, Claverton Down, Bath BA2 7AY, United Kingdom
Edited by James W. Valentine, University of California, Berkeley, CA, and approved January 31, 2008 (received for review October 2, 2007)
The prospect of finding macroevolutionary trends and rules in the
history of life is tremendously appealing, but very few pervasive
trends have been found. Here, we demonstrate a parallel increase
in the morphological complexity of most of the deep lineages
within a major clade. We focus on the Crustacea, measuring the
morphological differentiation of limbs. First, we show a clear trend
of increasing complexity among 66 free-living, ordinal-level taxa
from the Phanerozoic fossil record. We next demonstrate that this
trend is pervasive, occurring in 10 or 11 of 12 matched-pair
comparisons (across five morphological diversity indices) between
extinct Paleozoic and related Recent taxa. This clearly differenti-
ates the pattern from the effects of lineage sorting. Furthermore,
newly appearing taxa tend to have had more types of limbs and
a higher degree of limb differentiation than the contemporane-
ous average, whereas those going extinct showed higher-than-
average limb redundancy. Patterns of contemporary species diver-
sity partially reflect the paleontological trend. These results provide
a rare demonstration of a large-scale and probably driven trend
occurring across multiple independent lineages and influencing
both the form and number of species through deep time and in the
present day.
Arthropoda 兩 correlates of diversity 兩 disparity 兩
macroevolutionary trend 兩 tagmosis
M ost of the natural sciences operate by documenting pat-
terns and trends and thereby formulating general rules.
Evolution, however, is an essentially contingent process, mean-
ing that evolutionary trajectories can rarely be predicted. Pro-
posed evolutionary trends, such as Cope’s rule for evolutionary
size increase within lineages, have generally turned out to be only
weakly predictive, either resulting from passive diffusion away
from some barrier (1–4) or applying only at local temporal and
taxonomic scales (5–9). Here, we demonstrate a remarkable and
pervasive trend for increasing morphological complexity in
multiple parallel lineages of the Crustacea [the major arthropod
group with the longest and most disparate fossil record (10)]
throughout the Phanerozoic. Previous studies by Cisne (11) and
Wills et al. (10) have shown that average complexity, as indexed
by the serial differentiation and specialization of limbs along the
body axis (a process known as tagmatization or tagmosis),
increased from the Cambrian to the present. However, this
pattern could have resulted from nothing more than random
diffusion from a minimum boundary (1, 12, 13) or from the
differing fortunes of a small number of clades that happen
coincidentally to differ in complexity, rather than from a per-
vasive and driven trend within most clades (see Fig. 1). This work
uses recently available phylogenetic evidence that allows us to
distinguish between these (and other) possibilities.
To understand the mechanisms by which the average com-
plexity of crustaceans increased throughout the Phanerozoic,
this article addresses a range of related questions. Did many
parallel lineages evolve from a condition of serial limb
homonomy toward increasing serial differentiation, or were less
morphologically complex clades replaced wholesale by more
complex ones (Fig. 1)? Did the degree of tagmosis differentially
4786 – 4791 兩 PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12
A B C
Time
Time
Time
Clade
extinct
Clade
originated
Complexity Complexity Complexity
Fig. 1. When is a shift in the mean a trend? (A) A large clade displays an
overall increase in the complexity of its constituent subclades. Over time, the
distribution of complexity values is shifted to the right, and an apparent trend
for increasing complexity results. However, this pattern can derive from two
very different although not exclusive processes. (B) Increasing mean complex-
ity of the clade can result from the fortuitous extinction and origination of a
small number of constituent major subclades, which coincidentally, have very
different mean complexity values. (C) A driven trend results from a parallel
increase in complexity within all or most of the constituent subclades. This
mechanism is the dominant one in our crustacean data. Determining the
relative contributions of this process and the process in the Center requires a
phylogenetic approach, which has hitherto been lacking.
affect diversification or extinction rates? How do limb number
and the numbers of limb types contribute to the trend? Is the
extent of tagmosis related to present-day diversity? We conclude
that increasing complexity of appendage composition represents
a rare demonstration of a pervasive and long-term trend that has
helped to shape patterns of diversification since the Cambrian.
Results
Complexity Increases Throughout the Phanerozoic. The degree of
tagmosis (appendage complexity), as measured by using the
Brillouin index [see supporting information (SI) Appendix A],
has increased significantly from the Cambrian to the present
among free-living crustaceans (Fig. 2 and SI Appendix B), with
linear regressions explaining 25.0% of the variability over time.
Among the six morphological indices used, the strongest tem-
poral pattern was for the number of limb types (R2 ⫽ 0.322),
whereas average disparity per limb (i.e., degree of differentiation
from neighboring limbs) and total disparity of limb form also
revealed significant, positive trends. The average number of
types per limb displayed a positive but marginally nonsignificant
Author contributions: S.J.A., A.P., and M.A.W. designed research; S.J.A. and M.A.W. per-
formed research; S.J.A., A.P., and M.A.W. analyzed data; and S.J.A., A.P., and M.A.W. wrote
the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
†Towhom correspondence may be sent at the present address: Department of Biology,
University of Waterloo, 200 University Avenue West, Waterloo, ON, Canada N2L 3G1.
E-mail: sadamowi@gmail.com.
§To whom correspondence may be addressed. E-mail: m.a.wills@bath.ac.uk.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0709378105/DC1.
© 2008 by The National Academy of Sciences of the USA
www.pnas.org兾cgi兾doi兾10.1073兾pnas.0709378105
 A B C
80
Tagmosis (Brillouin index)

Total number of limb pairs

2.5 14
70

Number of limb types

60 12
2.0
50 10
40
1.5 8
30
6
1.0 20
10 4

0.5 0 2
-560 -460 -360 -260 -160 -60 -560 -460 -360 -260 -160 -60 -560 -460 -360 -260 -160 -60
Time (My) Time (My) Time (My)

D E F

Average disparity per limb

3.5 40
Limb types per limb

1.0

Total disparity score

3.0 35
0.9
2.5 30
0.8
2.0 25
0.7
1.5 20
0.6
1.0 15
0.5 0.5 10

EVOLUTION
0.4 0 5
-560 -460 -360 -260 -160 -60 -560 -460 -360 -260 -160 -60 -560 -460 -360 -260 -160 -60
Time (My) Time (My) Time (My)

Fig. 2. Regression analysis of limb diversity through the Phanerozoic, based on fossil origination times of 66 free-living crustacean orders. (A) Brillouin tagmosis value
(R2 ⫽ 0.250, P ⬍ 0.0001). (B) Total limb number (R2 ⫽ 0.00046, P ⫽ 0.865). (C) Number of limb types (R2 ⫽ 0.322, P ⬍ 0.0001). (D) Number of limb types per limb (R2 ⫽
0.049, P ⫽ 0.074). (E) Average disparity per limb (R2 ⫽ 0.091, P ⫽ 0.014). (F) Total disparity across all limbs (R2 ⫽ 0.291, P ⬍ 0.0001). For full regression statistics, see SI
Appendix B.

trend. By contrast, there was no trend in the total number of exception is the total number of appendages) showed a signif-
limbs over time. icant positive trend, with the extant groups exhibiting greater
The variables tested for trends are not independent of one limb diversity than their earlier relatives in 10 or 11 of 12 cases
another (SI Appendix C). The number of limb types is the (Table 1 and Fig. 3; see SI Appendix E). Thus, the overall increase
strongest correlate of Brillouin tagmosis values (r ⫽ 0.862; P ⬍ in mean tagmosis values resulted from a parallel trend in many
0.0001), whereas total limb number was the only index negatively lineages (as depicted in Fig. 1C), rather than from wholesale
and also nonsignificantly related to Brillouin tagmosis (r ⫽ replacement of a few less tagmatized clades by more highly
⫺0.196; P ⫽ 0.115). The degree of tagmosis was not correlated tagmatized ones (as depicted in Fig. 1B). Moreover, increases
with fossilization potential among living crustaceans (SI Appen- were observed in lineages starting from intermediate and low
dix D), and results were similar when including only those taxa tagmosis values, suggesting that diffusion from a minimum
having a fossil record. boundary cannot fully explain the trend.
Comparing the tagmosis values from the first third of the taxa
to originate (mean ⫽ 1.542 ⫾ 0.37 SD; n ⫽ 22) with those of the Relative Complexity Differs at Origination and Extinction. Newly
most recent third (mean ⫽ 2.104 ⫾ 0.26 SD; n ⫽ 22) by using originated taxa tended to have higher tagmosis values (by a
Welch’s two-sample t tests confirmed the trend toward increas- median difference of 0.17 unit), more limb types (0.66 more),
ing Brillouin tagmosis (t ⫽ ⫺5.795, df ⫽ 37.979, P ⬍ 0.001). and a higher total disparity score (1.9 points higher) than average
Significant increases were also found in the number of limb types for their contemporaries, in more than two-thirds of cases for all
and in the total disparity score, but nonsignificant increases were of these traits (see Table 2). These results were significant in both
observed in the number of limb types per limb and average sign and Wilcoxon tests (all P ⬍ 0.004). By contrast, at extinction,
disparity per limb. Total limb number averaged 12.88 pairs taxa showed no significant difference from average in these traits
(⫾7.015 SD) among the taxa originating earlier and 15.14 but tended to have a lower number of limb types per limb and
(⫾4.00) among the more recent originations (t ⫽ ⫺1.307, df ⫽ lower disparity per limb (i.e., higher limb redundancy) (P ⬍ 0.015
33.369, P ⫽ 0.20). Thus, there was no sustained tendency for limb for both Wilcoxon and sign tests).
number to increase substantially during the course of crustacean
evolution, even though the faunas at a select few of the earliest Contemporary Species Richness Is Correlated with Complexity. Bril-
stages possessed smaller numbers of limbs on average (⬇10–12 louin tagmosis scores showed a significant positive association with
limbs) than those of more recent stages (⬇17–19 limbs). present-day species richness and explained 16% of the variation in
diversity among clades (regression analysis: F1,36 ⫽ 7.08, P ⫽ 0.012;
Complexity Increases Within Many Independent Lineages. Compar- see SI Appendix F). Overall, 23 Brillouin tagmosis contrasts were
ing ancestors with their descendants can illuminate the dynamics positive, whereas 14 were negative (sign test: P ⫽ 0.188). The
of evolutionary trends (6, 12, 13). Unfortunately, the fossil number of limb types per limb (F1,36 ⫽ 4.52, R2 ⫽ 0.112, P ⫽ 0.040)
record is rarely complete enough to identify ancestors with any and average disparity per limb (F1,36 ⫽ 4.42, R2 ⫽ 0.109, P ⫽ 0.043)
confidence. However, our phylogenetically independent com- were also both positively associated with diversity (SI Appendix F).
parisons of early fossils with their closest extant relatives are The slope of the relationship between species diversity and the
useful proxies. Five of the six parameters (again, the sole total number of limbs was near zero (⫺0.01) and nonsignificant

Adamowicz et al. PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12 兩 4787
Table 1. Matched-pairs analysis of patterns of crustacean tagmosis evolution
Sign test Wilcoxon test (vs. H0: median ⫽ 0)

No. of differences
Median rate,
Trait Increases Decreases No change P value billion years⫺1 V P value

Brillouin tagmosis value 10 2 0 0.0386 0.682 68 0.0210

Total no. of limbs 5 4 3 1.00 0 19 0.722
No. of limb types 10 1 1 0.0117 4.466 59 0.0234
No. of types per limb 10 1 1 0.0117 0.301 61 0.0145
Average disparity per limb 10 2 0 0.0386 1.044 75 0.00244*
Total disparity across limbs 11 1 0 0.00635* 11.633 70 0.0122

Twelve fossil crustaceans were matched with Recent taxa (see Methods and SI Appendix E) to investigate whether the trend in tagmosis is repeated across
independent lineages.
*Results remaining significant after sequential Bonferroni correction.

(F1,36 ⫽ 1.15, R2 ⫽ 0.03, P ⫽ 0.29), indicating that limb number
is not associated with diversification (SI Appendix F).
Discussion
Increasing Complexity as a Major Trend Through the Phanerozoic. The
fossil record of the Crustacea, from the Cambrian to the present,
documents a clear trend of increasing appendage diversity within
individuals. Moreover, we have demonstrated that this trend has
been instrumental in patterning both the form and diversity of
species over time. Because the extant biota is a well studied but
unrepresentative sample of the history of life, trends detected in
the fossil record are rarely reflected in contemporary diversity
patterns. The significant relationship between tagmosis values
and modern diversity is therefore all the more striking.
Our results allow three principal inferences about the trend of
complexity in the Crustacea. First, parallel increases in tagmosis
values across separate evolutionary lineages contributed to the
overall trend, indicating that the temporal pattern does not
simply result from limited faunal turnover. As such, tagmatiza-
tion may constitute a constraint-driven trend (see ref. 14). Given
that increases were observed even in lineages whose tagmosis
values were far above theoretical or observed minimum values,
and given the evidence for increases in minimum tagmosis values
in arthropods over time (10, 11, 15), this pattern may be
3 contribute to the trend. The diversity of limb types in newly
1 time. It is possible that some new limb types constituted key
4 innovations that opened up new adaptive zones (19, 20). By
Complexity (Brillouin index)
considered an active trend, at least in part (see refs. 12 and 16).
Another possibility is that the trend resulted from a random
walk, but we consider it unlikely. In particular, our sampling
scheme masks the huge number of crustacean species that
existed throughout much of the Phanerozoic. If thousands of
lineages of crustaceans were free to wander randomly up and
down the complexity gradient, we would expect at least a small
number of free-living extant species to have secondarily revisited
the less-complex patterns of the Paleozoic. The fact that none
have done so and that almost all nonparasitic crustaceans retain
(at very least) strongly differentiated cephalic and anterior trunk
appendages suggests strongly that the trend in complexity is
driven. Moreover, complex forms, once originated, appear to be
maintained by some mechanism (17), which might be some
combination of developmental canalization (18) and ecological
competition. With reference to this last possibility, we note that
many species in marginal habitats (e.g., cave forms) often have
reduced complexity.
Second, increasing complexity is primarily a function of the
increasing number of limb types that accrue at the rate of ⬇4.5
per billion years, according to the phylogenetic analysis, rather
than any trend in total limb number. This finding concurs with
a broader but less detailed study that sampled Cambrian and
extant taxa from across all major arthropod groups (11).
Third, patterns in both origination and extinction of orders
originated taxa is significantly greater than average for any given

2.5 5
8 contrast, taxa going extinct tend to display a lower than average
2 2
6 6 number of limb types per limb; i.e., limb redundancy may be
3 12
4 3 disadvantageous and is associated with those taxa going extinct.
2
1 7&9 The fact that tagmatization is implicated as a correlate of both
5&9 origination and extinction rates suggests that the trend is at least
8
partly caused by clade selection among species and higher clades
1.5 7 (21) as well as within populations of individuals.
10
10 11
12 Complexity and Diversification. Differences in limb complexity
1 explained ⬇16% of the variation in contemporary species di-
11 versity among clades, making the degree of tagmosis a relatively
strong single correlate of diversity compared with others so far
0.5 investigated (e.g., see refs. 22–25). Our results regarding species-
Earlier Later level diversity therefore parallel Cisne’s (11) conclusions, based
on taxonomic analysis only, that increasing tagmosis was asso-
ciated with mounting ordinal-level diversity through the fossil
0
record. Although causation is difficult to establish, it is possible
Fig. 3. Changes in complexity over time for 12 phylogenetically matched that the evolution of new limb types may have been instrumental
pairs of fossil and living crustaceans, measured in Brillouin units. Numbers in promoting diversification (the key innovation hypothesis)
refer to the matched pairs listed in SI Appendix E. (e.g., ref. 26; for review, see ref. 20). Perhaps greater intraindi-

4788 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0709378105 Adamowicz et al.

Table 2. Relative tagmosis values of crustacean orders (compared with the contemporaneous average) at their time of origin
and extinction
Sign test Wilcoxon test

No. of differences
Median difference
Trait Positive Negative Zero P value (H0 ⫽ 0) V P value

Relative value at origination; n ⴝ 66 (51)

Brillouin tagmosis value 46 (35) 20 (16) 0 (0) 0.0019* (0.0110*) 0.172 (0.184) 1564 (935) 0.0034* (0.0109*)
Total no. of limbs 33 (29) 30 (19) 3 (3) 0.801 (0.193) 0.667 (1.882) 1231 (800) 0.128 (0.0300)
No. of limb types 47 (37) 18 (13) 1 (1) 0.00042* (0.00094*) 0.660 (0.989) 1655.5 (990.5) 0.00014* (0.00067*)
Mean no. of limb types per limb 32 (21) 33 (29) 1 (1) 1.00 (0.322) ⫺0.00790 (⫺0.0420) 948 (506) 0.418 (0.206)
Average disparity per limb 28 (19) 38 (32) 0 (0) 0.268 (0.0919⬃) ⫺0.146 (⫺0.163) 843 (452) 0.0942 ⬃ (0.0485)
Total disparity score 46 (36) 20 (15) 0 (0) 0.0019* (0.0046*) 1.910 (2.50) 1569 (976) 0.0031* (0.0034*)
Relative value at extinction; n ⴝ 25
Brillouin tagmosis value 12 13 0 1.00 ⫺0.0283 159 0.937
Total limb number 16 9 0 0.230 1.609 1015 0.565
No. of limb types 13 12 0 1.00 0.125 166 0.936
Mean no. limb types per limb 6 19 0 0.0146 ⫺0.115 67 0.00882*
Average disparity per limb 4 21 0 0.00091* ⫺0.454 40 0.00103*
Total disparity score 10 15 0 0.424 ⫺1.438 129 0.375

For the origination analyses, the first values are for results including all taxa (with living taxa having no fossil record being recorded as originating in the
Holocene), and the numbers in parentheses are the results excluding taxa lacking a fossil record. Significant (P ⬍ 0.05) results are highlighted in bold.
*Results remaining significant after sequential Bonferroni correction (performed across the six traits within each category of analysis).

vidual limb diversity could contribute to the further ‘‘evolvabil-
ity’’ or ‘‘versatility’’ (27) of a lineage, allowing new and different
functions to arise more readily and promoting niche diversifi-
cation. New limb types may also increase the scope for complex
sexual display and copulation, potentially amplifying any role of
sexual selection, which has been linked with diversification in
vertebrates (28, 29). However, it may be that particular habitats
limit diversification in some groups. For example, the Remipedia
have one of the lowest tagmosis values among extant free-living
crustaceans, but their confinement to deep caves connected to
the sea (30) may have been the main factor determining their
diversity.
Future Directions. Although the Phanerozoic trend for increasing
limb complexity in the Crustacea is well supported, there are
several outstanding questions.
Is complexity still increasing? The maximum contemporaneous tag-
mosis value has been quite consistent since the Devonian (when
it reached ⬇2.52 Brillouin units with the appearance of the
decapods, climbing only slightly to 2.56 with the origin of the
amphipods in the mid-Tertiary, and again to 2.64 in the Recent
Amphionidacea). Thus, tagmosis values have not approached
their theoretical maximum (e.g., 3.05–3.35 for individuals with
20–25 limbs that are all different). Although some stasis in the
maximum is expected toward the present (as we examined this
trait at a high taxonomic level), the observed degree of stasis is
not inevitable; many new orders have appeared since the De-
vonian. It is unclear whether further increases are precluded by
inflexible developmental programs, whether all of the major
types of viable body plans have already been explored, or
whether further increases in complexity would not confer any
additional functional advantages. An analysis of trends at lower
taxonomic levels would help to address this question.
What are the mechanisms of tagmosis increase? Do new lineages have
an intrinsic tendency to be more serially differentiated, or do
those that happen to be so have a better chance of becoming
established? Insights from developmental biology may help to
address this issue. Oligomerization specifically refers to the
tendency for repeated structures (such as segments within
appendages) or armature (such as spines and setae) to evolve by
loss, fusion, or reduction (31, 32). This trend has been recognized
EVOLUTION
for some time, although maximum likelihood analysis in the
Crustacea has demonstrated that the trend is relatively weak,
with many lineages evolving in the opposite direction (33).
Nonetheless, oligomerization may be one of the main mecha-
nisms by which limbs evolve novel morphologies and diversify.
However, the strength of this link and the developmental
underpinnings of both of these trends require further attention.
Is the trend for increasing complexity present in other taxa? Increases in
modularity and in numbers of independently evolving parameters
have apparently occurred in a variety of traits and lineages (16),
including molluscan shells (27), cichlid jaws (34), and parrot cranial
morphology (35). Increasing tagmosis, specifically, may also be a
more general phenomenon than documented here; for example,
differentiated trunk regions evolved multiple times independently
within the trilobites (36). However, further investigation is required
because previous treatments of tagmosis across arthropod taxa (10,
11) were not broken down into independent lineages (16), as here;
nor has the relationship between tagmosis values and contemporary
diversity been explored. In addition to other arthropods, annelids
would be an excellent subject for study because they also have a
serial body plan and tagmosis (31, 37). Moreover, ‘‘Williston’s law’’
(the differentiation of structure and function by reduction and
specialization) may apply to the evolution of vertebrate limbs as well
(38, 39). Indeed, the duplication and evolutionary differentiation of
sister copies are pervasive processes at all levels of organization:
from genes to segments, somites and limbs, and up to genomes and
entire body plans. Exploring these mechanisms will be a key
endeavor in understanding the evolution of the diversity of biolog-
ical forms.
Methods
Measures of Complexity. Our measures of complexity quantify limb diversity
within individuals. Because all of the limbs constitute a complete sample for
that individual, following Cisne (11), we first used the Brillouin index, which
has its origin in information theory (see 40, 41):
HB ⫽ 共ln N! ⫺ 冘 ln n i!兲/N [1]
where N is the total number of limb pairs, and n is the number of limb pairs of
the ith type. For fossil and extant free-living crustaceans in our sample, this
index ranges from 0.656 to 2.641. Values for parasitic taxa are sometimes
lower, and some parasites entirely lack limbs.

Adamowicz et al. PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12 兩 4789
 The Brillouin index combines several aspects of limb diversity into a single
measure (10, 11). To understand the trends in detail, we considered three more
specific measures: the total number of limbs, the number of limb types, and the
average number of types per limb. By convention, the ‘‘number of limbs’’ and
‘‘number of types,’’ etc., always refer to the number of pairs of limbs.
Coding the number of limb types is inevitably subjective. As imple-
mented by Cisne (11), successive limbs were compared down the length of
the body, and at some critical level of difference, they were deemed to be
different. The critical level of difference was quite small, and no attempt
was made to define it. We have refined this approach significantly here,
coding the magnitude of the differences between successive limb pairs on
a subjective scale of 0 –5, by using the following approximate definitions.
The codes therefore provide an ordinal scale of differences: 0, no differ-
ence (and grouped together into the same type for the Brillouin index); 1,
a small difference in form and/or numbers of endites; 2, a difference in the
number of podomeres; 3, a difference in the number/identity of rami and
number of podomeres; 4, a difference in the number/identity of rami,
number of podomeres, and/or a moderate difference in gross form; and 5,
a large difference in gross form.
All of the scoring was performed by one investigator (M.A.W.), and the
coding was checked by recoding after an interval of 1 month.
Two simple indices of limb diversity have been devised to summarize these
limb disparity data. The first is simply the average disparity per limb, an index
that is analogous to one of the simplest and best measures of diversity
turnover in ecological studies (41, 42). The second is the sum of disparity scores
across all pairs of adjacent limbs along the body axis, providing an index of
‘‘total disparity’’ for each taxon (for all limb formulae and indices, see SI
Appendix A).
Correlation coefficients (Pearson’s product–moment correlations) were
calculated between all pairs of variables to assess their interrelationships (see
SI Appendix C).
Taxon Sampling and Stratigraphic Ranges. A largely ordinal-level approach to
sampling crustaceans was adopted because previous studies found little
variation in tagmosis values within orders (10, 43). The taxonomic systems
of Schram (30) and Martin and Davis (44) were primarily used for fossil and
living crustaceans, respectively, whereas further details regarding sources
and sampling strategy can be found in SI Appendices A and G. Sixty-six
nonparasitic taxa were included in most analyses. (Parasites were retained
in our dataset in SI Appendix A for completeness and to facilitate future
research.)
Stratigraphic ranges of orders were mainly from Benton (45), with
additions from Wills (46) and others (see SI Appendix A). We used the
midpoint stage ages from Gradstein et al. (47). Records designated by
question marks were included here because they mainly involved only
slight extensions to the more solid ranges. Crustaceans range from the
Caerfi in the Lower Cambrian to the Holocene, spanning 77 epochs and
stages. (For further details regarding our inclusion of a few recently
described fossil taxa, see SI Appendix A.)
Characterizing the Overall Trend. We quantified the slope of the overall trend
by plotting tagmosis values against the midpoint age of the series or stage in
which the taxon first appeared in the fossil record. Least-squares linear
regression analysis was performed for all six limb indices. Because multiple
traits were examined, sequential Bonferroni correction (48) was performed.
Regressions were repeated omitting any outliers, those points whose Studen-
tized residuals were ⬎3 SD away from zero.
Approximately one-third of all living higher taxa have no fossil record.
Because ordinal-level taxa are highly unlikely to have arisen in the Holo-
cene, the origination dates for taxa lacking fossils are almost certainly
wrong. Therefore, we tested for a bias in fossilization potential in associ-
ation with tagmosis values by comparing living taxa having a fossil record
(n ⫽ 26) with those lacking a record (n ⫽ 15). None of the indices showed
a significant difference (Welch’s t tests; SI Appendix D). We repeated the
taxonomic regression analyses omitting taxa with no fossils for comparison
with the more comprehensive analyses, but the results were very similar
(data not shown).
To test for overall differences between the earliest and most recent crus-
taceans, we used t tests to compare trait values of the earliest third and most
recent third of taxa.
Matched-Pairs Analysis. Any trend detected above could either result from the
replacement of less serially differentiated lineages by more complex ones, or
it could reflect parallel evolution in every lineage (13). To discriminate be-
4790 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0709378105
tween these scenarios, we tested for a trend in phylogenetically matched pairs
of extinct and extant crustaceans (for the list of pairs, see SI Appendix E).
Our analysis used the phylogeny of Wills (46), which includes the largest
number of fossil and living taxa. We used a method derived from that of Hone
et al. (8) to pair extinct taxa with extant counterparts originating later in the
fossil record. No minimum temporal separation was imposed because all pairs
were ⬎300 million years apart. Extinct and extant taxa in each pair were
compared to determine the change in Brillouin tagmosis (and other indices).
The direction of change was tested against the null expectation (increases as
common as decreases) by using a sign test. We also determined the slope,
dividing the difference in each parameter by the age of the fossil group. (The
origination ages of the living taxa were not subtracted from the numerator
because our data are for extant representatives.) We compared the median
slope across pairs to a null expectation of zero by using a Wilcoxon test.
Origination and Extinction. Because trends in tagmosis values are tested at a
high taxonomic level and over long time scales, it is possible that clade-level
patterns of origination versus extinction (rather than, or in addition to,
evolution within lineages) are involved in any trends. Thus, we tested whether
relative tagmosis values are associated with the probability of origination or
extinction of higher taxa. From the tagmosis value for each taxon, we first
subtracted the contemporaneous mean at its time of origination to create a
set of differences. The numbers of positive and negative differences were then
compared with a null expectation of equal numbers by using a sign test. We
also used a Wilcoxon test to determine whether the median differences
deviated significantly from zero. We repeated these steps for periods of
extinction. For the origination analyses, we repeated the tests excluding taxa
without a fossil record.
Complexity and Species Diversity. To assess any potential association between
the degree of tagmosis of lineages and their contemporary species diversity,
it is necessary to account for phylogeny because taxa of the same rank are
often of different evolutionary ages. Moreover, pseudoreplication can be a
problem when trait differences occur at internal nodes and closely related
lineages are similar (7). Therefore, we used phylogenetically independent
contrasts, in which the differences in diversity values within each sister-clade
pair in a phylogeny are compared with the corresponding differences in the
value of the trait (49). We used the total-evidence cladogram of Wheeler et al.
(50) (their Fig. 17.6A), with some taxa placed according to other studies (for
details and the phylogeny, see SI Appendix G). Species richness values were
taken primarily from Bowman and Abele (51) and Schram (30) (see SI Appen-
dix G). Sensitivity analyses employing alternative phylogenies and set of
species richness data produced results very similar to those reported here (data
not shown).
Independent Contrasts Analysis. We used MacroCAIC (49) to generate the
contrasts in both diversity and tagmosis values. Because branch length esti-
mates were not available for our composite phylogeny, branch lengths were
set to unity, and the proportional dominance index (PDI) was used to measure
diversity differences among clades, as recommended by Isaac et al. (52) for
such cases. The resulting PDI values were calculated such that positive con-
trasts are obtained when the more diverse clade has the higher trait value
compared with its sister clade, and negative contrasts are produced when the
more diverse clade has the lower trait value. Although the sign of PDI depends
on the direction of the tagmosis value relationship, the magnitude depends
on the difference in diversity.
We analyzed the contrast data in R by using three statistical tests with
increasingly stringent assumptions: a sign test on the direction of PDI con-
trasts, a Wilcoxon test of median PDI against a null expectation of zero, and
regression through the origin (53) on the diversity and tagmosis value con-
trasts. We had no predictions about the direction of the tagmosis value–
diversity relationship. Cisne (11) documented a concordant increase in both
ordinal diversity and average tagmosis value over time since the Cambrian,
which he discussed in light of increasing complexity of ecological roles and
global communities. However, this large-scale pattern may have merely been
the result of a passive trend arising from increased variance in tagmosis values
over time. Therefore, we used two-tailed tests in all cases.
ACKNOWLEDGMENTS. We thank Timothy Barraclough, Doug Erwin, Richard
Fortey, Laurence Hurst, Armand Leroi, Todd Oakley, and Stuart Reynolds for
helpful discussions and suggestions at various stages during the long gesta-
tion of this project. This work was supported by a Beit Scientific Research
Fellowship, a Natural Sciences and Engineering Research Council of Canada
Scholarship, an Overseas Research Scholarship (to S.J.A.), and a Biotechnology
and Biological Sciences Research Council grant (to M.A.W.).
Adamowicz et al.
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Appendix A. Details on the limb diversity data set on fossil and living Crustacea

Datasets on limb diversity from Cisne (1) and Wills et al. (2) were used as starting points, with all limb formulae verified or rescored
for this study by M.A.W. To provide even coverage of the entire range of body plan diversity in both fossil and Recent Crustacea,
many additional taxa were coded. We adopted largely an ordinal-level approach because previous workers found little variation in
tagmosis values within orders (1, 3). Although one must be cautious of circularity when using a taxonomic approach to sampling
morphologies, we suggest that this is not a major issue here. Although limbs can be among the defining features of orders, many other
characters are generally also used to designate orders (e.g., carapace and somite features) (see 4). Moreover, the degree of limb
differentiation along the body axis cannot be inferred from particular limb traits.

We initially coded one representative from each order, following the taxonomic scheme of Martin and Davis (5) for living
representatives. However, additional exemplars were coded in a number of orders. In most cases, the limb formulae were identical or
very similar (resulting in a difference of <0.1 Brillouin tagmosis units), and just one representative was selected. However, there was
more variation observed in the Brachypoda, Anaspidacea, and Diplostraca. In the first two cases, the indices from two exemplars were
averaged to provide the values used for these orders in all analyses. The case of Diplostraca was more complex.

Although it was preferable to use ordinal definitions according to one set of authors for consistency, the diplostracans are anomalous
in their level of tagmosis diversity (>1.0 Brillouin tagmosis units). Moreover, the ranks of the taxa in this group have been the subject
of much discussion, with several key branchiopod works adopting a system that includes seven different orders of “diplostracans” (6-
8). Therefore, we sampled a representative of each of these seven orders and used a phylogenetically weighted average to calculate a
single value for the Diplostraca. The topology [Laevicaudata, Spinicaudata, Cyclestherida (Haplopoda, Onychopoda), (Anomopoda,
Ctenopoda)] was selected because of its support in maximum likelihood (ML), Bayesian, and maximum parsimony analyses based on
six genes (9) and in ML and Bayesian analyses involving two ribosomal genes (10). Although the Notostraca fell within the
Diplostraca in some of these phylogenies, we retained the exemplar of this order as separate (as in ref. 5).

Many problematic fossil taxa are not formally assigned to orders, or they are treated very differently by several authors. These, by
their very nature, often preserve unique combinations of characters, unfamiliar patterns of serial limb differentiation, and distinctive
and/or apomorphic appendage morphologies. Their inclusion was vital to encompass the full disparity of tagmosis patterns. Schram
(4) provided the most recent classification including all fossil Crustacea, to which we added several problematic, anomalous, or more
recently described fossils (11-14). The affinities of the Euthycarcinoidea (13) are, at best, uncertain, with a number of authors allying
them to the hexapods or myriapods, and others resolving them as stem-group mandibulates (14). None of the trends or conclusions
discussed in this paper is materially affected by their omission. In addition, the ostracod taxonomy was revised according to Liebau
(15). Geological ranges were according to Benton (16), updated using taxon-specific sources and more recent evidence (11-14, 17-22).
All data are presented in Table A1.

There are approximately five ordinal-level taxa of which we are aware that are missing from our current dataset. In a few cases, these
absences are caused by inadequate preservation of limb structure. Anything less than the most exceptional preservation could bias
toward an underestimate of the disparity of appendage types in fossils, whereas more compromised preservation might underestimate
the number of limb pairs.

Because most of the primarily parasitic higher taxa have very low tagmosis values for their classes (and sometimes even no limbs at
all), parasites were omitted from analyses unless otherwise indicated. However, they were included in Table A1 for a more complete
record of the range of morphological diversity found in the Crustacea.
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57-65.

3. Flessa KW, Powers KV, Cisne JL (1975) Paleobiology 1:71-81.

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15. Liebau A (2005) Hydrobiologia 538:115-137.

16. Benton MJ (1993) The Fossil Record 2 (Chapman & Hall, London), 2nd Ed, pp 321−356.

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Table A1. Limb formulae and limb diversity indices for all crustacean taxa included in the work.
The limb formulae specify the number of limbs of each limb type (from anterior to posterior), while numbers in parentheses indicate
the disparity (i.e., differentiation) score of each of limb pair from the adjacent, posterior limb pair. Primarily parasitic or commensal
groups are designated after the order name (PAR) and were excluded from most analyses.

Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Class Branchiopoda
Lipostraca† PRA-PRA Lepidocaris 1(3),1(4),1(4),1(4), 2.334 18 11 0.6111 1.444 26
rhyniensis† 1(2),2(1),3(1),5(3),
1(2),1(2),1
Kazacharthra† CRN-TOA Almatium gusevi† 1(3),1(4),1(3),1(3), 2.031 17 9 0.5294 1.353 23
1(4),1(1),5(1),5(4),
1
Anostraca LUD-HOL Artemia salina 1(4),1(4),1(3),1(3), 1.514 18 8 0.4444 1.333 24
1(4),11(3),1(3),1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Notostraca KAS-HOL Lepidurus lynchi 1(2),1(4),1(3),1(3), 1.174 78 11 0.1410 0.359 28
1(5),1(2),1(2),9(2),
60(4),1(1),1
Diplostraca BER-HOL Lyncaeus 1(4),1(4),1(4),1(2), 1.275 19 7 0.3684 1.158 22
(Laevicaudata) brachyurus 1(4),13(4),1
Diplostraca LOK-HOL Limnadia 1(4),1(4),1(4),1(2), 1.001 28 7 0.250 0.786 22
(Spinicaudata) lenticularis 1(4),22(4),1
Diplostraca HOL-HOL Cyclestheria 1(4),1(4),1(4),1(2), 1.201 21 7 0.333 1.048 22
(Cyclestherida) hislopi 1(4),15(4),1
Diplostraca BER-HOL Daphnia pulex 1(5),1(4),1(4),1(3), 2.079 10 9 0.900 2.5 25
(Anomopoda) 1(3),1(1),2(2),1(3),
1
Diplostraca TTH-HOL Sida crystallina 1(5),1(4),1(4),1(3), 1.827 12 8 0.667 2.0 24
(Ctenopoda) 1(4),5(1),1(3),1
Diplostraca HOL-HOL Leptodora kindtii 1(5),1(4),1(4),1(5), 2.061 11 9 0.818 2.455 27
(Haplopoda) 1(2),3(2),1(2),1(3),
1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Diplostraca HOL-HOL Cercopagis pengoi 1(5),1(4),1(4),1(5), 1.921 10 8 0.800 2.5 25
(Onychopoda) 1(1),3(3),1(3),1
Diplostraca LOK-HOL Phylogenetically 1.284 20.47 7.188 0.388 1.202 22.41
(composite used for weighted average
taxonomic analyses) of the seven taxa
above
Class Remipedia
Nectiopoda HOL-HOL Speleonectes 1(3),1(3),1(4),1(4), 1.347 27 9 0.333 0.889 24
ondinae 1(2),1(1),1(4),19(3
),1
Enantiopoda† VIS-MOS Tesnusocaris 1(5),1(5),1(3),1(1), 1.201 21 7 0.333 0.952 20
goldlichi† 1(5),15(1),1
Class Cephalocarida
Brachypoda HOL-HOL Hutchinsoniella 1(3),1(4),1(4),1(2), 1.663 15 8 0.533 1.4 21
macracantha 8(3),1(2),1(3),1
Brachypoda HOL-HOL Sandersiella 1(3),1(4),1(4),1(2), 2.051 15 10 0.667 1.533 23
acuminata 6(1),1(1),1(3),1(2),
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
1(3),1
Brachypoda HOL-HOL Average of the two 1.857 15 9 0.6 1.467 22
(composite used for taxa above
all analyses)
Class Maxillopoda
Infraclass Facetotecta HOL-HOL N/A (no limbs in
(PAR) adults)
Laurida (Infraclass CMP-HOL Synagoga normani 1(4),1(4),1(3),1(4), 2.114 11 9 0.818 2.273 25
Ascothoracida) (PAR) 1(3),1(2),2(1),2(4),
1
Dendrogastrida TUR-HOL Ascothorax 1(4),1(4),1(3),1(3), 2.205 11 10 0.909 2.455 27
(Infraclass ophioctenis 1(3),1(2),2(2),1(2),
Ascothoracida) (PAR) 1(4),1
Apygophora ANS-HOL Trypetesa lateralis 1(3),1(1),1(5),1(5), 1.589 8 6 0.75 2.25 18
(Superorder 3(4),1
Acrothoracica)
Pygophora LOK-HOL Weltneria hessleri 1(3),1(1),1(5),1(5), 1.488 10 6 0.6 1.8 18
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
(Superorder (female) 5(4),1
Acrothoracica)
Kentrogonida HOL-HOL Sacculina carcini N/A (no limbs in
(Superorder adults)
Rhizocephala) (PAR)
Akentrogonida HOL-HOL Chthamalophilus N/A (no limbs in
(Superorder delagei adults)
Rhizocephala) (PAR)
Pedunculata STD-HOL Lepas anatifera 1(5),1(3),1(1),1(5), 1.662 10 6 0.6 1.7 17
(Superorder 3(3),3
Thoracica)
Sessilia (Superorder TTH-HOL Balanus 1(5),1(3),1(1),1(5), 1.662 10 6 0.6 1.7 17
Thoracica) balanoides 3(3),3
Subclass HOL-HOL Basipodella 1(5),1 0.5 2 2 1 2.5 5
Tantulocarida (PAR) harpacticola
Arguloida (Subclass HOL-HOL Argulus foliaceous 1(4),1(4),1(5),1(5), 1.721 10 7 0.7 2.5 25
Branchiura) (PAR) 1(4),4(3),1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Cephalobaenida MER-HOL* Cephalobaena 1(1),1 0.5 2 2 1 0.5 1
(Subclass tetrapoda
Pentastomida) (PAR)
Porocephalida HOL-HOL Sebekia sp. 1(1),1 0.5 2 2 1 0.5 1
(Subclass
Pentastomida) (PAR)
Mystacocaridida HOL-HOL Derocheilocaris 1(3),1(2),1(3),1(1), 1.879 11 8 0.727 1.455 16
typicus 1(2),1(2),4(3),1
Platycopioida HOL-HOL Platycopia 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.154 28
(Subclass Copepoda) inornata 1(3),1(3),4(1),1(4),
1(4),1
Calanoida HOL-HOL Calanus 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.154 28
(Copepoda) finmarchicus 1(3),1(3),4(1),1(4),
1(4),1
Misophrioida HOL-HOL Misophria pallida 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.231 29
(Copepoda) 1(3),1(3),4(2),1(4),
1(4),1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Cyclopoida HOL-HOL Cyclopinoides 1(4),1(4),1(3),1(3), 2.150 13 10 0.769 2.385 31
(Copepoda) longicornis 1(3),1(3),4(3),1(4),
1(4),1
Gelyelloida HOL-HOL Gelyella droguei 1(3),1(4),1(3),1(3), 2.061 11 9 0.818 2.455 27
(Copepoda) 1(3),1(3),3(4),1(4),
1
Mormonilloida HOL-HOL Mormonilla 1(3),1(4),1(3),1(3), 2.021 12 9 0.75 2.25 27
(Copepoda) phasma 1(3),1(3),4(4),1(4),
1
Harpacticoida MMI-HOL Canuella perplexa 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.231 19
(Copepoda) 1(3),1(3),4(2),1(4),
1(4),1
Poecilostomatoida HOL-HOL Clausidium 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.308 30
(Copepoda) (PAR) vancouverense 1(3),1(3),4(3),1(4),
1(4),1
Siphonostomatoida APT-HOL Asterocheres 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.154 28
(Copepoda) (PAR) reginae 1(3),1(3),4(1),1(4),
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
1(4),1
Monstrilloida MMI-HOL Monstrilla 1(3),1(4),1(3),1(3), 2.150 13 10 0.769 2.231 29
(Copepoda) (PAR, helgolandica 1(3),1(3),4(2),1(4),
juveniles, adults are 1(4),1
free-living)
Class Ostracoda
Palaeocopida TRE-TAT None with
appendages
preserved
Punciocopida TRE-HOL Manawa staceyi 1(2),1(3),1(4),1(3), 1.589 8 6 0.75 1.75 14
3(2),1
Platycopida TRE-HOL Cytherella 1(3), 1(4), 1(3), 1(3), 1.757 7 7 1 2.857 20
abyssorum 1(3), 1(4), 1
Podocopida ARG-HOL Macrocypris 1(2), 1(4), 1(3), 1(4), 1.582 6 6 1 2.833 17
maddocksae 1(4), 1
Cypridinida LLY-HOL Cypridina norvegica 1(4), 1(4), 1(3), 1(4), 1.912 8 8 1 3.625 29
1(4), 1(5), 1(5), 1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Halocypridida WEN-HOL Halocypris pelagica 1(2). 1(4), 1(3), 1(2), 1.912 8 8 1 2.375 19
1(2), 1(2), 1(4), 1
†
Leperditicopida ARG-FAM None with
appendages
preserved
Bradoriida CRF-TRE Kunmingella Tentatively: 1.245 7 4 0.571 1.286 9
†
(Ostracoda) † maotianshanensis 1(4),3(3),1(2),2
(excluded from
analysis because of
poor preservation)
Class Malacostraca
Archaeostraca† TRE-TAT Nahecaris† 1(3),1(4),1(2),1(1), 1.818 19 8 0.421 1 19
1(3),8(3),5(3),1
Hoplostraca† VIS-MOS Kellibrooksia Tentatively: 1.976 19 9 0.474 1.263 24
(excluded from macrogaster† 1(2),1(3),1(2),1(2),
analysis because of 1(5),1(4),7(3),5(3),
poor preservation) 1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Leptostraca KAZ-HOL Nebalia 1(3),1(3),1(3),1(3), 2.010 20 9 0.45 1.2 24
pugettensis 1(3),8(4),4(4),2(1),
1
Aeschronectida† VIS-GZE Kallidecthes 1(3),1(4),1(2),1(2), 1.818 19 8 0.421 0.947 18
richardsoni† 1(2),8(2),5(3),1
Palaeostomatopoda† FAM-SPK Tyrranophontes 1(2),1(3),1(3),1(1), 2.246 19 10 0.526 1.474 28
theridion† 1(3),1(5),4(4),3(4),
5(3),1
Stomatopoda SPK-HOL Squilla mantis 1(4),1(4),1(3),1(4), 2.352 19 11 0.579 2.105 40
1(4),1(5),1(4),3(4),
3(4),5(4),1
Eocaridacea† GIV-MOS Eocaris socialis† 1(3),1(5),1(3),1(1), 1.818 19 8 0.421 1.211 23
1(4),8(4),5(3),1
Belotelsonidea† TOU-MOS Belotelson 1(3),1(5),1(3),1(1), 1.944 20 9 0.45 1.3 26
magister† 1(4),8(4),5(3),1(3),
1
Palaeocaridacea† VIS-KUN Acanthotelson 1(3),1(4),1(3),1(1), 2.207 19 10 0.526 1.211 23
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
stimpsoni† 1(2),1(2),2(3),5(3),
5 (2),1
Bathynellacea HOL-HOL Bathynella natans 1(2),1(3),1(3),1(2), 2.271 16 11 0.688 1.625 26
1(3),2(2),5(3),1(2),
1(3),1(3),1
Anaspidacea ANS-HOL Anaspides 1(3),1(4),1(3),1(3), 2.260 19 11 0.579 1.474 28
tasmaniae 1(4),1(2),1(1),5(3),
1(1),5(4),1
Anaspidacea ANS-HOL Parastygocaris 1(3),1(4),1(3),1(3), 2.103 14 10 0.714 1.857 26
andina 1(4),1(2),1(1),5(3),
1(3),1
Anaspidacea ANS-HOL Average of the two 2.182 16.5 10.5 0.646 1.666 27
(composite used for taxa above
all analyses)
Spelaeogriphacea TOU-HOL Spelaeogriphus 1(3),1(4),1(2),1(2), 2.474 19 12 0.632 1.579 30
lepidops 1(3),1(3),3(2),3(2),
1(3),4(3),1(3),1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
Spelaeogriphacea TOU-SPK Acadiocaris 1(3),1(3),1(3),1(3), 2.0714 19 9 0.474 1.368 26
(included in matched- novascotica† 1(4),2(3),6(3),5(4),
pairs analysis; this 1
taxon formerly in
separate order
Anthracocaridacea†)
Thermosbaenacea HOL-HOL Thermosbaena 1(3),1(3),1(3),1(3), 2.197 14 10 0.714 1.929 27
mirabilis 1(2),1(3),1(3),4(3),
2(4),1
Lophogastrida MOS-HOL Eucopia 1(3),1(4),1(3),1(3), 2.350 20 11 0.55 1.8 36
sculpticaudata 1(4),1(4),4(4),3(3),
1(4),5(4),1
Mysida CLV-HOL Mysis relicta 1(3),1(4),1(3),1(3), 2.124 19 10 0.526 1.526 29
1(4),1(3),1(1),6(4),
5(4),1
Pygocephalomorpha† TOU-TAT Anthracaris 1(3),1(4),1(2),1(2), 2.184 20 10 0.5 1.4 28
gracilis† 1(3),2(4),6(3),5(3),
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
1(4),1
Mictacea HOL-HOL Mictocaris halope 1(3),1(3),1(3),1(2), 2.207 19 10 0.526 1.316 25
(female) 1(3),1(3),5(1),2(3),
5(4),1
Amphipoda PRB-HOL Gammarus 1(2),1(4),1(3),1(3), 2.557 19 12 0.632 1.579 30
locustus 1(4),1(3),2(2),2(1),
3(3),3(3),2(2),1
Isopoda MOS-HOL Whoia angusta 1(2),1(4),1(3),1(3), 2.474 19 12 0.632 1.579 30
1(4),1(3),1(2),3(1),
3(3),1(3),4(2),1
Tanaidacea VIS-HOL Apseudes spinosus 1(2),1(4),1(3),1(4), 2.352 19 11 0.579 1.842 35
1(4),1(5),1(3),3(2),
3(4),5(4),1
Cumacea SPK-HOL Cyclaspis bacescui 1(2),1(3),1(3),1(3), 2.435 19 12 0.632 1.632 31
1(4),1(4),1(4),1(2),
2(1),3(3),5(2),1
Euphausiacea HOL-HOL Meganyctiphanes 1(3),1(4),1(4),1(2), 2.234 20 11 0.55 1.7 34
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
norvegica 1(3),6(4),1(4),1(5),
5(2),1(3),1
Amphionidacea HOL-HOL Amphionides 1(3),1(4),1(3),1(4), 2.641 19 14 0.737 2.053 39
reynaudii 1(3),1(4),1(2),2(2),
1(2),2(3),1(4),1(3),
4(2),1
Decapoda FAM-HOL Homarus 1(3),1(4),1(3),1(3), 2.518 19 13 0.684 2.053 39
americanus 1(3),1(3),1(3),1(5),
1(3),2(1),2(4),5(4),
1
? FAM-FAM Angustidontus 1(4),1(5),1(2),2(5), 2.194 19 9 0.474 1.579 30
seriatus† 1(5),3(1),4(4),5(4),
1
Taxonomy uncertain
Canadaspidida† CRF-STD Canadaspis† 1(2),1(4),1(5),2(1), 1.432 14 6 0.4286 1.143 16
8(4),1
Canadaspidida† CRF-STD Perspicaris* 1(2),1(4),1(5),10 1.039 14 5 0.3571 1.071 15
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
(4),1
Euthycarcinida† CRF-CRN Smithixerxes 1(5),1(3),1(4),11 0.792 14 4 0.2857 0.8571 12
pustulosus*
? STD-STD Odaraia*† 2(5),1(5),1(1),1(4), 0.816 36 6 0.1667 0.5556 20
30(5),1
? STD-STD Waptia*† 1(3),1(3),1(3),1(1), 1.886 16 8 0.5 1.1875 19
1(3),4(3),6(3),1
? MER-MER Skara* 1(3),1(1),1(2),2(1), 1.614 7 6 0.8571 1.286 9
1(2),1
? MER-MER Martinssonia* 1(3),3(1),1(2),1(3), 1.388 7 5 0.7143 1.286 9
1
? MER-MER Cambropachycope 1(4),1(3),2(4),1(1), 1.415 6 5 0.8333 2 12
clarksoni* 1
? MER-MER Bredocaris* 1(3),1(2),1(3),1(3), 1.773 13 8 0.6154 1.154 15
1(1),6(1),1(2),1
? MER-MER Rehbachiella* 1(3),1(2),1(2),1(2), 1.147 17 6 0.3529 0.6471 11
12(2),1
Order Stratigraphic Scored taxon Limb formula Tagmosis Total No. of No. of Average Total
range (Brillouin no. of limb types disparity disparity
index) limbs types per per limb score of
limb limb
differences
? EMS-EMS Cambronatus 1(5),4(5),11(5),1 1.088 17 4 0.235 0.882 15
brasseli†
? EMS-EMS Wingertshellicus 1(3),1(4),1(4),1(4), 0.656 40 6 0.15 0.5 20
backesi† 35(5),1

? EMS-EMS Eschenbachiellus 1(3),1(3),13(3),1 0.732 16 4 0.25 0.562 9

wuttkensis†
Phosphatocopida† MER-MER Hesslandonia 1(4), 1(2), 1(4), 1(3), 1.757 7 7 1 2.286 16
†
unisulcata 1(1), 1(2), 1
† †
Phosphatocopida MER-MER Vestrogothia sp. 1(3), 1(2), 1(2), 1(2), 1.757 7 7 1 1.857 13
1(1), 1(3), 1
Phosphatocopida† MER-MER Average of two taxa 1.757 7 7 1 2.071 14.5
(composite used for above
analysis)
†
Extinct.
*It is unclear to which subclass (Cephalobaenida or Porocephalida) the upper Cambrian pentastomid larvae belong, and so they were
assigned randomly because the choice made no difference to our results.
Appendix B. Full regression statistics for ordinal tagmosis values through the Phanerozoic

Table B1. Overall pattern of tagmosis evolution in the Crustacea throughout the fossil record for 66 free-living, ordinal-level
taxa (see also Fig. 2)
Regression on crustacean taxa at the time of origin
Trait Intercept Slope, billion Standard error, F-stat R2 P value
yrs−1 slope
Brillouin tagmosis 1.560 1.207 0.261 21.321,64 0.250 <0.0001*
Total no. of limbs (results 16.443 1.049 (1.358) 6.146 (3.859) 0.02921,64 0.00046 0.865
omitting 1 outlier) (15.43) (0.124 1,63) (0.00196) (0.726)
No. of limb types 6.992 6.673 1.211 30.381,64 0.322 <0.0001*
No. of types per limb 0.539 0.234 0.129 3.3071,64 0.0491 0.0737 ~
Average disparity per limb 1.387 0.932 (1.058) 0.368 (0.331) 6.3911,64 0.0908 0.01395*
(results omitting 1 outlier) (1.324) (10.211,63) (0.139) (0.00219*)
Total disparity across limbs 18.613 20.446 3.985 26.321,64 0.291 <0.0001*

The geological ages were coded with the midpoint of the first Cambrian period (Caerfi) as time 0, such that slopes coincide with the
intuitive direction of the pattern over time. When outliers (those points whose Studentized residuals were more than 3 SD from zero)
were present, regression analyses were repeated omitting those points.
* Results remaining significant after sequential Bonferroni correction.
Appendix C. Test for correlation among morphological indices

Table C1. Correlation coefficients (Pearson’s product−

−moment correlations) among measures of limb number and diversity
for 66 free-living crustacean orders

Brillouin tagmosis Total limb number No. of limb types No. of limb types Average disparity
per limb per limb
Total limb number −0.196 (P = 0.115)
No. of limb types 0.862 (P < 0.0001) 0.253 (P = 0.0402)
No. of limb types 0.585 (P < 0.0001) −0.662 (P < 0.0001) 0.200 (P = 0.108)
per limb
Average disparity 0.524 (P < 0.0001) −0.561 (P < 0.0001) 0.270 (P = 0.0286) 0.888 (P < 0.0001) --
per limb
Total disparity 0.757 (P < 0.0001) 0.254 (P = 0.0399) 0.895 (P < 0.0001) 0.131 (P = 0.295) 0.382 (P = 0.00157)
score
P values are provided for simple regression analysis of each pair of characters.
 Appendix D. Comparison of living crustacean taxa with and without a fossil record.

Living taxa with a fossil record are compared with living taxa without a fossil record. There is no difference for any of the six traits
(Table D1), indicating that tagmosis values are not associated with fossilization potential. However, because ordinal-level taxa are
highly unlikely to have arisen in the Holocene, the origination dates for taxa lacking fossils are obviously wrong. Therefore, the
taxonomic regressions (as in Appendix B) were repeated omitting taxa with no fossil record; results (not shown) were very similar to
those from the whole dataset.

Table D4. Test of whether living crustacean taxa without a fossil record are different from those with a fossil record

Trait Mean for living Mean for living t df P-value

taxa with a fossil taxa with no fossil
record (n = 26) record (n = 15)
Brillouin tagmosis 1.977 2.098 −1.126 37.98 0.267
Total limb number (repeated omitting 16.88 (14.44) 15.27 (15.27) 0.564 (-0.544) 32.90 (33.72) 0.576 (0.590)
the notostracan exemplar, which
has an anomalous 78 limbs)
No. of limb types 9.180 10.00 −1.415 38.98 0.165
Mean no. limb types per limb 0.657 0.686 −0.562 38.45 0.578
Average disparity per limb 1.883 1.891 −0.0473 36.58 0.962
Trait Mean for living Mean for living t df P-value
taxa with a fossil taxa with no fossil
record (n = 26) record (n = 15)
Total disparity score 26.17 27.53 −0.701 36.74 0.488

All tests are two-tailed Welch’s t tests.

Appendix E. List of fossil and living matched pairs

Table E1. List of phylogenetically matched pairs of fossil and living crustacean taxa,
used for analysis presented in Table A1
Pair Class Order Exemplar
1. Fossil Malacostraca Belotelsonidea Belotelson magister
1. Living Malacostraca Amphionidacea Amphionides reynaudii
2. Fossil Malacostraca Paleostomatopoda Tyrranophontes theridion
2. Living Malacostraca Stomatopoda Alima
3. Fossil Malacostraca Pygocephalomorpha Anthracaris gracilis
3. Living Malacostraca Mysida Mysis relicta
4. Fossil Malacostraca Anthracocaridacea Acadiocaris novascotica
4. Living Malacostraca Anthracocaridacea Spelaeogriphus lepidops
(formerly in order
Spelaeogriphacea)
5. Fossil Malacostraca Aeschronectida Kallidecthes richardsoni
5. Living Malacostraca Decapoda Homarus americanus
5. Living Malacostraca Euphausiacea Meganyctiphanes norvegica
6. Fossil Malacostraca Paleocaridacea Acanthotelson stimpsoni
6. Living Malacostraca Cumacea Cyclaspis bacescui
6. Living Malacostraca Mictacea Mictocaris halope
7. Fossil ? ? Martinssonia
7. Fossil ? ? Skara
7. Living Maxillopoda Mystacocaridida Derocheilocaris typicus
7. Living Maxillopoda (multiple copepod pooled copepod value
orders)
8. Fossil Branchiopoda Lipostraca Lepidocaris rhyniensis
8. Living Cephalocarida Brachypoda Hutchinsoniella macracantha
9. Fossil Malacostraca Archeostraca Nahecaris
9. Living Malacostraca Leptostraca Nebalia pugettensis
Pair Class Order Exemplar
10. Fossil Remipedia Enantiopoda Tesnusocaris goldlichi
10. Living Remipedia Nectiopoda Speleonectes ondinae
11. Fossil ? ? Odaraia
11. Living Branchiopoda Diplostraca Pooled value
12. Fossil Branchiopoda? ? Rehbachiella
12. Living Malacostraca Bathynellacea Bathynella natans
When more than one taxon is listed in either the “fossil” or “living” category, these taxa
form a clade and were averaged for the analysis.
Appendix F. Full results of independent contrasts analysis on tagmosis-diversity relationship

Table F1. The relationship between tagmosis and the diversity of extant crustacean clades.

Sign test Wilcoxon test Regression (n = 37 contrasts)

No. positive No. negative Neutral P value (H0: median = 0)
Trait contrasts contrasts contrasts V P value slope F-stat R2 P value

Brillouin tagmosis 23 14 0 0.188 478.5 0.0563~ 1.501 7.085 1,36 0.162 0.0121

Total no. of limbs 15 17 5 0.86 251.5 0.822 -0.0135 1.151 1,36 0.0310 0.290

No. of limb types 20 14 3 0.392 376 0.185 0.103 0.802 1,36 0.022 0.376

No. of types per 17 20 0 0.743 333 0.786 2.144 4.524 1,36 0.112 0.0403
limb

Average disparity 17 19 1 0.868 364 0.632 0.713 4.416 1,36 0.109 0.0427
per limb

Total disparity 16 19 2 0.736 334 0.762 0.00765 0.049 1,36 0.0014 0.826
across limbs

Positive trait contrasts are those for which the more diverse clade has the larger trait value, while negative contrasts are those for
which the less diverse clade has the larger value. Neutral contrasts (no trait difference) are omitted from the sign and Wilcoxon tests.
Regressions were repeated following data transformation (square, square root, or log transformations as appropriate) to improve the
distribution of residuals; findings were similar (results not shown).
Appendix G. Phylogeny and notes on species richness sources

Wheeler et al. (1) provide one of the most data-rich analyses of arthropod phylogeny to date,
incorporating 808 morphological characters and more than 2,000 nucleotides from 18S and 28S.
Moreover, their analyses offer much denser taxon sampling than most other treatments of the
Crustacea, inferring relationships for most of the groups in our study. We used their total
evidence tree as a starting point (their Fig. 17.6A), adding the small number of taxa not
considered by them. The Facetotecta were introduced as the sister taxon to the remaining
Thecostraca (2), and the Pentastomida were added as the sister taxon to the Branchiura (3). We
also resolved relationships within the order Diplostraca to a lower level, based on phylogenetic
works for the class Branchiopoda (4, 5) (see also SI Appendix A). Relationships among copepod
orders were also resolved (their Fig. 4.3.2 and their preferred hypothesis). Our composite
phylogeny used for independent contrasts analysis, along with relative species richness
estimates, is presented in Fig. G1 (in a separate file). A few terminals in our phylogeny contained
multiple orders because of a lack of phylogenetic resolution; trait data from Appendix A were
averaged for these. Because parasitic taxa tend to have fewer limbs than free-living crustaceans,
or no limbs at all, their tagmosis values tend to be anomalous for their clades. Moreover, in the
Crustacea, a parasitic mode of life has been associated with lower-species richness than observed
in free-living sister clades (7). Therefore, parasitic taxa were entirely cut from the dataset before
analysis.

Data on the species richness of terminal clades were needed for the independent-contrasts
analysis. Rates of discovery and description indicate that crustaceans are an incompletely
described group (8), with many more species in nature than are currently known to science.
However, at least for the branchiopods, described diversity is a fairly accurate assessment of
levels of relative diversity among groups, with diversity differences of more than 1.5-fold robust
to the variability of the taxonomic description process (9). Therefore, we sought species diversity
estimates from a single source at a specific year in the history of taxonomic description. We
selected Bowman and Abele (10) because this was the most recent work to provide species
richness estimates for all major groups of crustaceans. However, because a few taxa were not
considered by these authors, values were added for a few orders from a slightly later source (11).
In a few other cases, we included clades at a lower taxonomic level than did Bowman and Abele
(10). Therefore, we used the species richness ratios in these groups that were provided in other
sources (ref. 9 for the branchiopods), but we corrected the total diversity of these groups to equal
levels in the 1982 reference. In addition, species were subtracted from the Cyclopoida and added
to the small order Gelyelloida, which was formerly included among the cyclopoids; this was
repeated for the order Platycopioida, formerly part of Calanoida.

Independent-contrasts analyses were repeated using alternative phylogenetic hypotheses. For

example, we repeated analyses using Fig. 17.6B in Wheeler et al. (1) and also using a tree similar
to our Fig. G1 but with the deeper nodes rearranged according to a three-gene maximum
likelihood tree (12). We also repeated the analyses using species richness estimates from a
different source (13). These analyses produce qualitatively similar results and are not reported.

1. Wheeler WC, Giribet G, Edgecombe GD (2004) in Assembling the Tree of Life, eds Cracraft J,
Donoghue MJ (Oxford Univ Press, New York), pp 281-295.

2. Pérez-Losada M, Hoeg JT, Kolbasov GA, Crandall KA (2002) J Crust Biol 22:661-669.

3. Lavrov DV, Brown WM, Boore JL (2004) Proc R Soc London B 271:537-544.

4. deWaard JR, Sacherová V, Cristescu MEA, Remigio EA, Crease TJ, Hebert PDN (2006) Mol
Phylogenet Evol 39:491-502.

5. Stenderup JT, Olesen J, Glenner H (2006) Mol Phylogenet Evol 41:182-194.

6. Huys R, Boxshall G (1991) Copepod Evolution (Ray Society, London), pp 371-422.

7. Adamowicz SJ (2006) Diversity and direction: Macroevolutionary patterns in the Crustacea

PhD thesis (Imperial College London, UK).

8. Martin JW, Davis GE (2006) Crustaceana 79:1347-1368.

9. Adamowicz SJ, Purvis A (2005) Global Ecol Biogeogr 14:455-468.

10. Bowman TE, Abele LG (1982) The Biology of Crustacea. I. Systematics, the Fossil Record,
and Biogeography, ed Abele LG (Academic, New York), pp 1-27.

11. Schram FR (1986) Crustacea (Oxford Univ Press, New York).

12. Regier JC, Shultz JW, Kambic RE (2005) Proc R Soc London B 272:395-401.

13. Waterman TH, Chace FA, Jr (1960) The Physiology of Crustacea, ed Waterman TH
(Academic, New York), pp 1-33.

Fig. G1. Composite crustacean phylogeny used for independent contrasts analysis. Taxa that are
primarily parasitic are not included. Species richness estimates according to 1982 levels (see
text) are shown in parentheses.
Anostraca (180)
Notostraca (11)
Anomopoda (390)
Ctenopoda (36)
Onychopoda (23)
Haplopoda (1)
Cyclestherida (2)
Spinicaudata (150)
Laevicaudata (28)
Acrothoracica (50)
Thoracica (700)
Mystacocaridida (9)
Ostracoda (5648)
Platycopioida (11)
Calanoida (2289)
Gelyelloida (2)
Cyclopoida (448)
Misophrioida (3)
Mormonilloida (2)
Harpacticoida (2800)
Nectiopoda (6)
Brachypoda (9)
Leptostraca (10)
Bathynellacea (100)
Anaspidacea (15)
Stomatopoda (350)
Amphionidacea (1)
Decapoda (10000)
Euphausiacea (85)
Lophogastrida (52)
Mysida (728)
Amphipoda (6000)
Thermosbaenacea (9)
Isopoda (4000)
Cumacea (800)
Tanaidacea (500)
Mictacea (2)
Spelaeogriphacea (1)