W. B. Saunders,
1*
D. M. Work,
2
S. V. Nikolaeva
3
The septal sutures of 588 genera of Paleozoic ammonoids showed a
1600 percent increase in mean complexity over 140 million years. Within
475 ancestor/descendant pairs, descendants were more than twice as
likely to be more complex than their ancestors. Twelve subclades (373 genera) averaged 34 percent increased complexity. These patterns are
compatible with an active or driven system of long-term bias for
increased complexity. Mass extinctions acted in opposition to this
long-term trend, tending to eliminate more-complex forms and resetting
the trend with each extinction event.
1 Department of Geology, Bryn Mawr College, Bryn
Mawr, PA 19010, USA.
2 Cincinnati Museum Center,
Geier Collections and Research Center, Cincinnati, OH 45202, USA.
3 Paleontological Research Institute, Russian
Academy of Sciences, Profsoyuznaya 123, 117647 Moscow, Russia.
*
To whom correspondence should be addressed. E-mail:
wsaunder@brynmawr.edu
Two long-held evolutionary
generalizations are that size and complexity have tended to increase
through time (1, 2). Two mechanisms have been
proposed for producing large-scale trends such as this. One is a random
or passive process of diffusion away from bounded minima (the
"left-wall effect," where the only way to go is to the right), and
the other is a nonrandom, active, or driven process of biased branching
toward increased size or complexity
(2-6). However, there have been few
empirical studies of such trends, and those that exist present
contrasting conclusions [for example (3,
7)]. Some documented trends appear compatible with
passive diffusion away from a minimum (8, 9), whereas others seem to represent active or driven selection
(10, 11). However, this dual view may be found to
be simplistic; it has been argued that passive (or random) trends so
dominate evolutionary history that if driven trends do occur, they are rare, incidental by-products of contingency
(5). An alternative view is that active trends are
real, and may reflect evolution away from unstable equilibria and
toward optima, or even attractors (3, 4).
We report the results of tracking the evolution of complexity in the
septal sutures of Paleozoic ammonoids (12) over 140 million
years and spanning three mass extinctions. We have largely followed the
lines of testing passive versus driven trends suggested by McShea
(4), which involves tracking changes in minima
through time; comparing the proportion of increases versus decreases in
ancestor/descendant pairs; and examining the skewness of subclades
drawn from a right-skewed parent clade (4).
Paleozoic ammonoids comprise 588 genera ranging over 140 million years,
from their appearance in the Lower Devonian to their near-termination at the Permian/Triassic boundary (Fig. 1) (13). This large clade of extinct mollusks was among the
fastest evolving groups known in the fossil record
(14). The occurrence of three mass extinctions over
this period (15, 16) provides an
opportunity to evaluate the effects of external processes on this
long-term record. Because these extinctions violate stochastic
constancy (4), Devonian ammonoids were segregated
from Mississippian-Permian ammonoids, which comprise a taxonomically
discrete clade bracketed by the Devonian/Mississippian (D/M) and
Permian/Triassic (P/Tr) extinctions.
Fig. 1.
Ammonoid genus diversity through the Paleozoic.
Arrows and expanded spindles show Frasnian/Famennian (367 Ma),
Devonian/Mississippian (354 Ma), and Permian/Triassic (250 Ma) mass
extinctions (13, 19). Intervals 1 to 14 correspond to chronostratigraphic divisions in Figs. 2 and 3; for
abbreviations see (20).
[View Larger Version of this Image (14K GIF file)]
We identified 475 ancestor/descendant genus pairs (165 Devonian and 310 Mississippian-Permian) on the basis of
well-established phylogenies (13), which rely partly on
similarities in the configuration of the suture, but not on overall
complexity. There was no presumption of increased complexity in
selecting A/D pairs, or within subclades; indeed, many complexity
decreases are known (13). Twelve subclades were segregated
for closer examination (Table 1). To
examine survivors of the P/Tr extinctions, we included basal Triassic
ammonoids (10 genera) in some aspects of the analysis (13).
Table 1.
Selected Paleozoic ammonoid subclades (1 to 4, Devonian; 5 to 12, Mississippian-Permian). N, number of genera in
subclade; A/D, phylogenetic ancestor/descendant genus pairs; SCI, mean
suture complexity index of subclade; SK, subclade skewness ( negative
skew; 0, symmetric distribution; + positive skew); Net %, mean net
change in suture complexity; I:D(S), ratio of increases to decreases
(stasis = <5%).
|
Subclade |
N |
A/D |
SCI |
SK |
Net
% |
I:D(S) |
|
1. Agoniatitina |
23 |
18 |
2.0 |
1.6 |
+19.3 |
11:5(2) |
2. Anarcestina |
66 |
55 |
5.8 |
2.6 |
+27.9
|
32:20(3) |
3. Goniatitida |
52 |
43
|
3.4 |
1.8 |
+16.4 |
23:10(10) |
4. Clymeniida |
64 |
43 |
2.5 |
1.6
|
+18.0 |
21:15(7) |
Mean |
51
|
40 |
3.4 |
1.9 |
+20.4 |
22:12(6)
|
5. Schistocerataceae |
18 |
13 |
8.7 |
1.6
|
+25.7 |
6:3(4) |
6. Neoicocerataceae |
28 |
25 |
6.1 |
1 |
+ 9.9 |
13:8(4)
|
7. Adrianitaceae |
18 |
15 |
15.5 |
0.2
|
+48.6 |
12:3(0) |
8. Marathonitaceae |
15 |
13 |
21.1 |
1.2 |
+41.8
|
8:4(1) |
9. Prolecanitida |
40 |
36
|
33.4 |
0.7 |
+38.6 |
28:5(3) |
10. Cyclolobaceae |
18 |
14 |
61.8 |
2.4
|
+63.0 |
13:0(1) |
11. Ceratitida
|
21 |
7 |
9.3 |
1.4 |
+26.6 |
5:2(0)
|
12. Shumarditaceae |
10 |
9 |
21.3 |
0.9
|
+75.4 |
9:0(0) |
Mean |
21 |
17
|
22.2 |
1.2 |
+41.2 |
12:3(2) |
|
Considerable emphasis has been placed on the "behavior of the
minimum" in evaluating long-term trends (2, 4, 9-11). In an active or driven system, minimum values will
tend to increase through time, whereas in a passive system the minimum
will tend to show only passive diffusion (with decreases, stasis, or
even slight increases) through time. Minimum suture complexity is 1. For comparison, living Nautilus has a suture complexity
index (SCI) of about 1.3. The sutures of the earliest ammonoids (Lower
Devonian) were about as simple as they could be: 97% had SCI < 3 and 67% had SCI < 2 (four genera had sutures less complex than
that of Nautilus). Ignoring the effects of extinction
events, complexity minima increased slowly through the Paleozoic, from
SCI 1.2 to 2.6, but jumped to SCI 7 after the P/Tr extinction (Fig.
2). Maximum complexity increased rapidly
during the Pennsylvanian and Permian, when many new suture patterns
emerged (11), reaching ammonitic levels (SCI >300) by the
end of the Permian. Overall, mean complexity increased 1600% between
the Lower Devonian-Upper Permian, and there is a strong correlation
between absolute time and mean complexity (r2 = 0.70, t ratio = 6.3, P > t < 0.0001; F
ratio = 28.1, P > F 0.0002). This
trend was a combined product of greatly increased variance and steady
attrition (by extinction) in the proportion of simple sutured genera
(SCI < 4), which declined from ~80% in the Devonian to ~10%
by the Permian (Fig. 3).
Fig. 2.
Plots of minimum, mean (±SE), and maximum suture
complexity through the Paleozoic (13). Representative
sutures are Gyroceratites (SCI 1.7), Irinoceras
(3.7), Branneroceras (6.1), Tabantalites
(13.5), Metaperrinites (47.3), and Timorites
(203).
[View Larger Version of this Image (23K GIF file)]
Fig. 3.
Frequency distribution of Lower
Devonian-basal Triassic ammonoids (598 genera), showing decline
in proportion of simple sutures (SCI < 4, shaded).
[View Larger Version of this Image (27K GIF file)]
In a passive system with no bias, less-complex descendants should be as
frequent as more-complex ones (4). In 159 simple-sutured Devonian A/D pairs (mean SCI 3.7), complexity increased +20% on average, with 55% of descendants showing increases compared with 31% decreases (hypothetical mean = 0: t test = 5.847, degrees of freedom (df) = 164, P < 0.0001). Stasis (less than 5% change) occurred in 14% of
descendants. However, because Devonian sutures were on average so
simple (and hence close to left-wall minima), these early increases in
complexity could reflect either passive or driven trends.
Among 310 moderately complex Mississippian-Permian A/D pairs (mean SCI
9.6) there was an average complexity gain of +22%, with more than
twice as many descendants (58%) showing increases as decreases (24%);
18% exhibited stasis (t test = 8.369, df = 309, P < 0.0001) (Fig. 4). In
a subset of 71 Mississippian-Permian A/D pairs segregated to minimize
any left-wall influence (SCI >10), the trend was even stronger: Mean
net change was +36%, with 71% showing increases, 23% decreases, and
6% stasis (t test = 5.393, df = 70, P < 0.0001). When net change is plotted through time,
the strong bias for increased complexity is readily apparent (Fig. 5).
Fig. 4.
(left). Change in
suture complexity in 310 Mississippian-Permian
ancestor/descendant genus pairs. More than twice as many descendants
(58%) showed increases as decreases (24%), and 18% showed stasis
(<5% change, in black).
Fig. 5.
(right). Change in complexity
(percent) in 310 Mississippian-Permian ancestor/descendant genus
pairs; gray line connects the mean for each interval (overall change
was +22%).
[View Larger Version of this Image (21K GIF file)]
In a driven system, the subclade test assumes that the skew of subclade
distributions drawn from the upper part of a positively skewed parent
distribution will also be positive; the system is probably passive if
average subclade skew is neutral (symmetric distribution) or negative
(4). All four major Devonian subclades show positive
skew (mean SK 1.9) (Table 1). However, because the majority of Devonian
taxa are simple-sutured (SCI ~1 to 3) and might reflect the influence
of minimal bounds, the Devonian subclade results are not regarded as
conclusive.
By contrast, Mississippian-Permian ammonoids (389 genera) have an
essentially unbroken (~100 million years) evolutionary history, they
show much higher average suture complexity (mean SCI 12.5) than their
Devonian counterparts, and their overall frequency distribution is
strongly skewed (SK 7). Of eight subclades with mean SCI 6 to 62 segregated for closer analysis, distributions of seven are positively
skewed, and one is neutral (no skew; Table 1). Inasmuch as these
subclades had complexity values far from left-wall minimum values, each
could theoretically have evolved reduced suture complexity. But each
subclade showed increased complexity through time (averaging +41%),
increases outnumbered decreases by 4:1, and the magnitude of
the increases averaged +59% compared with 21% for decreases. The
subclade data suggest there was pervasive bias for increased
complexity.
In general, mass extinctions eliminated highly complex sutures, but
each event exerted its own influences.
1) Upper Devonian Frasnian/Famennian [367 million years ago (Ma)].
Surprisingly high levels of suture complexity had evolved by the Upper
Devonian; four Frasnian families reached SCI >20. But only five genera
(all simple-sutured, SCI ~2.6) survived the Frasnian/Famennian (F/F)
extinction, which reduced complexity by half (mean SCI ~6 to 3;
minimum ~2 to 1), and maximum SCI declined by 75% (SCI ~35 to 9).
If the F/F extinction had not occurred, ammonitic levels of complexity
may have become commonplace by the Mississippian.
2) Devonian/Mississippian (354 Ma). After the F/F extinction was the
most diverse ammonoid radiation in the Paleozoic: More than half of 116 Famennian genera are clymeniids, an enigmatic clade that first appeared
in the mid-Famennian, but was extinct by the end of the stage. If the
D/M extinction had not eliminated clymeniids, the late Paleozoic may
have been dominated by these simple-sutured (SCI ~3) forms. This
extinction nearly eliminated ammonoids altogether; only three
simple-sutured goniatitids survived (SCI ~3.6), giving rise to a long
interval of low complexity (Fig. 2).
3) Permian/Triassic (250 Ma). The organic effects of the P/Tr
extinction are widely known (16), and ammonoids were affected as severely as any other group. Only two Upper Permian genera
survived: highly complex Episageceras (SCI 57.8), which became extinct shortly thereafter, and Xenodiscus (SCI 7.7),
which was ancestral to all Mesozoic clades. This extinction had several effects: Minimal complexity was ratcheted upward from SCI ~3 to 7;
maximum complexity fell from SCI >300 to ~60; and mean complexity declined from SCI ~32 to 18, equivalent to being set back ~50 million years. The only long-term P/Tr survivor was a ceratitid with a
simple, serrate suture; this might have eliminated old developmental
constraints and introduced a new Mesozoic sutural template that was
quite different from that of its Paleozoic predecessors.
Despite differential survival of simple-sutured genera during mass
extinctions, the trend toward increased complexity started anew (or
resumed) after each extinction event. It is remarkable that ammonoids
survived these events at all, and that after each extinction they
radiated once again. This rise-and-fall diversity persisted through the
Mesozoic, although it appears that complexity stabilized after the P/Tr
extinctions (9), possibly suggesting that optima were
reached, sensu (3), by the time of their final extinction at
the Cretaceous/Tertiary boundary.
Active or driven trends may reflect a number of influences,
including selection, differential survival or extinction, phylogeny or
development, and functional constraints (6). Our results indicate that most of these factors were involved: (i) There
was selective extinction of low-complexity genera through time (Fig.
3); (ii) descendants favored increased complexity by at least
2:1 (Figs. 4 and 5); and (iii) increased complexity
prevailed within individual subclades (Table 1). But evaluating the
role of functionality remains elusive, as it confronts the "ammonoid
suture problem": What was the function of the ammonoid suture and why
were more-complex sutures selected for? Although this 160-year-old
controversy resists unequivocal explanation, it has been widely
accepted that more-complex septa provided greater buttressing effects
against hydrostatic pressure (17). Recently,
however, finite element stress analysis has shown that any departure
from a hemispherical shape (a straight suture) yields higher, not
lower, hydrostatic stresses on a septal surface, which is the weakest
part of the chambered shell (18). Thus, the evolution of
septal complexity involved a trade-off: Increasingly complex sutures
meant lower septal strength and hence shallower depth limits. This
might explain why complexly sutured forms were more susceptible to mass
extinctions, which often coincided with eustatic events (15,
16), and why simple-sutured nautilaceans seem to
have been largely unaffected by extinction events and persist even
today in deep-water habitats.
These results show that there were several nonrandom processes
operating in apparent opposition during the course of Paleozoic ammonoid evolution. Overall, there was pervasive long-term bias for
increased complexity, both within individual subclades and across the
ammonoid clade as a whole. But during times of biotic crisis, there was
an opposing tendency to selectively eliminate more-complex sutures.
This had the effect of periodically setting back or even reversing, but
not halting, the driven long-term trend toward increased complexity.
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29 June 1999; accepted 14 September
1999