Paleobiology, 26(3), 2000, pp. 386–404
Bangiomorpha pubescens n. gen., n. sp.: implications for the
evolution of sex, multicellularity, and the Mesoproterozoic/
Neoproterozoic radiation of eukaryotes
Nicholas J. Butterfield
Abstract.—Multicellular filaments from the ca. 1200-Ma Hunting Formation (Somerset Island, arctic
Canada) are identified as bangiacean red algae on the basis of diagnostic cell-division patterns. As
the oldest taxonomically resolved eukaryote on record Bangiomorpha pubescens n. gen. n. sp. provides a key datum point for constraining protistan phylogeny. Combined with an increasingly resolved record of other Proterozoic eukaryotes, these fossils mark the onset of a major protistan
radiation near the Mesoproterozoic/Neoproterozoic boundary.
Differential spore/gamete formation shows Bangiomorpha pubescens to have been sexually reproducing, the oldest reported occurrence in the fossil record. Sex was critical for the subsequent success of eukaryotes, not so much for the advantages of genetic recombination, but because it allowed
for complex multicellularity. The selective advantages of complex multicellularity are considered
sufficient for it to have arisen immediately following the appearance of sexual reproduction. As
such, the most reliable proxy for the first appearance of sex will be the first stratigraphic occurrence
of complex multicellularity.
Bangiomorpha pubescens is the first occurrence of complex multicellularity in the fossil record. A
differentiated basal holdfast structure allowed for positive substrate attachment and thus the selective advantages of vertical orientation; i.e., an early example of ecological tiering. More generally,
eukaryotic multicellularity is the innovation that established organismal morphology as a significant factor in the evolutionary process. As complex eukaryotes modified, and created entirely novel, environments, their inherent capacity for reciprocal morphological adaptation, gave rise to the
‘‘biological environment’’ of directional evolution and ‘‘progress.’’ The evolution of sex, as a proximal cause of complex multicellularity, may thus account for the Mesoproterozoic/Neoproterozoic
radiation of eukaryotes.
Nicholas J. Butterfield. Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ,
United Kingdom. E-mail: [email protected]
Accepted:
7 February 2000
Introduction
The red algae are a study in extremes. Morphologically more diverse than any other
group of algae, they range from single cells to
large ornate multicellular plants (Woelkerling
1990). Uniquely among (nonfungal) eukaryotes they lack both flagella and centrioles, and
any evidence of ever having had them (Pueschel 1990). They show greater molecular sequence divergence than the kingdom Fungi or
the chlorophytes plus green plants (Ragan et
al. 1994), and exhibit a remarkable, often bizarre range of reproductive strategies (Hawkes 1990; Hommersand and Fredericq 1990).
Some species are capable of withstanding extreme environments, not least Bangia atropurpurea, which ranges from lacustrine to fully
marine habitats (Geesink 1973; Sheath and
Cole 1980). Their chloroplasts appear to be extremely primitive, having the same pigment
q 2000 The Paleontological Society. All rights reserved.
complexes and unstacked thylakoids as cyanobacteria (Pueschel 1990); the chloroplast of
Porphya purpureum retains more genes (and is
therefore presumably that much more primitive) than that of any other known eukaryote
(Reith 1995). Molecular phylogenetic analyses
further suggest the red algae occupy a relatively basal position among extant eukaryotes
(Stiller and Hall 1997). In addition to all this,
the oldest taxonomically resolved fossil eukaryote is a red alga, specifically a 1.2-billionyear-old filamentous bangiophyte from arctic
Canada. In all but detail, this fossil is indistinguishable from modern Bangia (Butterfield et
al. 1990) and thus stands as a key datum point
for considering early eukaryotic evolution.
Here I formally describe this fossil, Bangiomorpha pubescens n. gen., n. sp., and consider its
implications for understanding the evolution
of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes.
0094-8373/00/2603-0005/$1.00
MESOPROTEROZOIC SEX AND MULTICELLULARITY
387
FIGURE 1. Locality and local geology of the Hunting Formation, Somerset Island. The outcrop preserving Bangiomorpha pubescens n. gen. n. sp. (87-HU-ST) is arrowed.
Geological Setting
The fossils occur in the Hunting Formation,
the upper unit of a small Proterozoic inlier
that crops out on northwestern Somerset Island, arctic Canada (Stewart 1987) (Fig. 1).
These little-altered shallow-water carbonates
were part of a regional sedimentary basin that
includes late Mesoproterozoic units on nearby
Baffin Island and Greenland. The correlation
is recognized on the basis of detailed stable
isotope chemostratigraphy (Kah et al. 1999),
as well as closely comparable litho- and biostratigraphy (see Hofmann and Jackson 1991).
Pb-Pb dating of carbonates from the Huntingcorrelative Society Cliffs Formation on Baffin
Island has recently yielded a well constrained
age of 1198 6 24 Ma (L. Kah personal communication 1999), a major refinement on the
previous radiometric determinations, which
bracketed the Hunting Formation to between
1267 6 2 Ma and 723 6 3 Ma.
The 10001 meters of the Hunting Formation
are characterized by locally abundant microdigitate stromatolites, decimeter-scale fibroradiate tufa(?), mud-cracks, tepee structures,
and often pervasive diagenetic chert—all in-
dications of a shallow-water to emergent intertidal/supratidal environment. The fossils
reported here are from a ca. two-meter-thick
section, low in the formation (estimated 100 m
above the base), at the head of a secondary
tributary to the Hunting River (Fig. 1). The exposure is a gray, laminated to thin-bedded dolostone with relatively continuous layers of
dark-gray to black chert up to several centimeters thick. In thin-section, the dark chert
layers are seen to include two sediment types:
(1) faintly laminated fine sediment (originally
micrite?) containing streaks of compacted organic material but few fossils, and (2) discrete
but irregular laminations ranging from a few
tens of micrometers to several millimeters
thickness and often abundantly fossiliferous.
The tendency of this latter lithology to form
large (cm-sized) tabular intraclasts shows
them to have been early stabilized/mineralized crusts; the common clustering of Bangiomorpha colonies on these surfaces (Fig. 2)
points to an ecological preference for firm
substrates.
Petrographic thin-sections of these silicified
carbonates reveal an abundance of exception-
388
NICHOLAS J. BUTTERFIELD
FIGURE 2. Population of vertically oriented Bangiomorpha pubescens n. gen. n. sp. colonizing a localized firm substrate. Thin-section HUST-1C, England Finder coordinates O-41.
ally well-preserved fossils. Of the six locally
derived samples containing fossils, five were
dominated by associations of Bangiomorpha n.
gen. and the stalk-forming cyanobacterium
Polybessurus (Green et al. 1987). Subordinate
forms include both simple (Myxococcoides) and
sheathed spheroids (Gloeodiniopsis spp.,? Pterospermopsimorpha), large bilayered filaments
(Rugosoopsis), and two previously undocumented forms that may represent additional
multicellular eukaryotes (Butterfield in press).
Siphonophycus, the (almost) ubiquitous filamentous microfossil of Proterozoic microbial
mats, is conspicuously absent from all of the
Bangiomorpha-bearing samples.
Systematic Paleontology
All type and illustrated fossil specimens are
housed in the Paleobotanical Collections of
Harvard University (HUPC). Individual specimens, all in petrographic thin-section, are located using England Finder coordinates.
Domain Eucarya Woese, Kandler, and Wheelis, 1990
Division Rhodophyta Wettstein, 1924
Class Bangiophyceae Melchior, 1954
Order Bangiales Schmitz, 1892
Family Bangiaceae Nägeli, 1847
Genus Bangiomorpha n. gen.
Etymology. With reference to the marked
similarity with modern Bangia.
Type species. Bangiomorpha pubescens n. sp.
Diagnosis. Unbranched, vertically oriented
filamentous bangiaceans with a basal multicellular holdfast structure. Individual cells defined by thin, relatively dark walls; whole
plant enclosed in a thick translucent layer. Filaments uniseriate, multiseriate, or a combination of the two; positioning of cells in multiseriate portions reflects their derivation from
uniserial precursors. Uniseriate filaments constructed of stacked disk-shaped cells, paired
hierarchically into groups of two, four, and occasionally eight cells. Multiseriate portions of
filaments generally constructed of four to
eight radially oriented wedge-shaped cells; alternatively, of relatively few isolated spheroidal cells, or many close-packed spheroidal
cells.
Discussion. Bangiomorpha n. gen. is in all
substantial respects indistinguishable from
the modern bangiophyte red alga Bangia (Table 1). The key diagnostic character (synapomorphy) establishing its bangiacean affinity is
the fourfold radially symmetrical arrangement of wedge-shaped cells that constitute
most multiseriate filaments; this habit records
389
MESOPROTEROZOIC SEX AND MULTICELLULARITY
TABLE 1. Characteristics of Bangiomorpha, Bangia, and filamentous Ulotrichales, Prasiolales (Chlorophyta), and Stigonematales (Cyanobacteria).
Multiseriate filaments with fourfold
radial symmetry
Radially oriented longitudinal
intercalary division
Nonbranching filaments
At least two spore types (on separate
plants)
Diffuse transverse intercalary division
Basipetal maturation
Ratio of multiseriate to uniseriate
diameters 1–2
Uniseriate filament diameter
15–45 mm
Multiseriate filament diameter
30–70 mm
Centripetal cytokinesis
Filaments uniseriate, multiseriate,
and/or combined
Uniseriate filaments of uniformly
disk-shaped cells
Thin, discrete walls defining
individual cells
Thick outer wall/sheath defining
whole filament
Vertical orientation
Preference for hard substrates
Intertidal habitat
Differentiated multicellular holdfast
Bangiomorpha
Bangia
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
monoecious
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
rhizoids
X
X
X
X
rhizoids
X
X
X
X
rhizoids
X
X
X
X
X
the unique pattern of longitudinal intercalary
cell division that is otherwise known only in
modern Bangia. Likewise, the hierarchical
pairing of cells in uniseriate filaments documents the bangiacean habit of diffuse growth
whereby all vegetative cells contribute to initial filament elongation through transverse intercalary cell division (vs. the apical growth of
most other algae and filamentous cyanobacteria).
Despite these marked similarities, the first
issue must be taxonomic. Can Bangiomorpha be
assigned unambiguously to the bangiacean
red algae? Among cyanobacteria, the default
assignment for Proterozoic microfossils, the
only reasonable comparison is with the filamentous Stigonematales. Most Stigonematales
differentiate a comparably thick external
sheath, and many are multiseriate. They are
also, however, characterized by true branching, apical growth, and differentiated heterocysts and akinetes (Martin and Wyatt 1974;
Anagnostidis and Komárek 1990), none of
which is found in Bangiomorpha. Furthermore,
Ulotrichales
Prasiolales
Stigonematales
transient
no stigonematalean, or indeed any known cyanobacterium, exhibits the regular radial intercalary cell division seen in Bangia/Bangiomorpha (Table 1). This latter feature likewise
rules out comparison with various eukaryotic
filaments, e.g., species of the green algal family Schizomeridaceae (filamentous Ulotrichales) (Table 1) or more primitive filamentous
bangiophyceans belonging to the Porphyridiales (e.g., Goniotrichum) or Erythropeltidales
(Erythrotrichia). Intercalary radial division has
been observed in the modern prasiolalean
chlorophyte Rosenvingiella; however, it does
not show the regular fourfold symmetry of filamentous bangiaceans (Table 1) (Scagel 1966:
Plate 13D). More importantly, the radial cells
of Rosenvingiella are decidedly transient as
they proceed to divide in three planes producing the solid parenchymatous spheres
characteristic of the genus.
The fossils differ from modern Bangia in a
number of ways, the most obvious being the
possession of a multicellular holdfast structure; by contrast, modern Bangia typically has
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NICHOLAS J. BUTTERFIELD
elongated, nonseptate rhizoids descending
from a number of basal vegetative cells (Sommerfeld and Nichols 1970: Fig. 3). Geesink
(1973), however, has reported holdfast structures in Bangia that are limited to the basal
cell, and other filamentous bangiophytes,
though not Bangiales, do have multicellular
holdfasts closely comparable to those of Bangiomorpha (e.g., Erythrotrichia [Garbary et al.
1980: Fig. 4n]). Insofar as holdfasts are related
critically to the local turbulence and substrate
conditions, their particular form might be
considered relatively plastic (though this is
not always the case [C. Pueschel personal
communication 1999]). Accessory, but less
compelling, reasons for separating Bangiomorpha from Bangia are the 1.2-billion-year difference in their ages and the relative timing of
holdfast initiation (see below).
Enzien (1990) has described a short uniseriate filament fragment with evidence of transverse intercalary cell division (paired diskshaped cells within an outer sheath) from the
Narssârssuk Formation, northwestern Greenland, and Kah and Knoll (1996) have mentioned similar material from the Society Cliffs
Formation on adjacent Baffin Island. Both of
these units are at least broadly correlative
with the Hunting Formation (Kah et al. 1999)
and represent similar peritidal carbonate environments. The possibility that the Narssârssuk and Society Cliffs fossils are also Bangiomorpha is intriguing, but in the absence of the
diagnostic multiseriate filaments or a holdfast
structure they cannot be distinguished unambiguously from a Johannesbaptistia-like cyanobacterium. Sheathed multiseriate filaments comparable in size to Bangiomorpha are
characteristic of Palaeomicrocystis schopfii Maithy, 1975 from the Neoproterozoic Bushimay
System of Zaire/Congo; however, the flattened nature of these compression fossils prevents analysis of the cell shape and division
patterns, and therefore their higher-order taxonomy.
Bangiomorpha pubescens n. sp. (Figs. 2–6)
Etymology. With reference to its pubescent
or hairlike form, as well as the connotations of
having achieved sexual maturity.
Holotype. HUPC 62912, Figure 5E, Slide
HUST-1A, England Finder coordinates: O-35.
Type Locality. Lower Hunting Formation,
Somerset Island, arctic Canada. Field locality
87-HUST; 73835.5‘N,94846‘W.
Diagnosis. A species of Bangiomorpha with
uniseriate portions of filaments less than 50
mm wide.
Description. Vertically oriented uniseriate
and multiseriate unbranched filaments up to
2 mm long; isolated or gregarious in clusters
of up to 15 individuals; commonly colonizing
localized firm substrates. Uniseriate forms 15–
45 mm wide (x̄ 5 25.4 6 6.0 mm; n 5 500) with
disk-shaped cells hierarchically paired and/
or with a circumferential furrow recording incipient centripetal division. Multiseriate
forms 30–67 mm wide (x̄ 5 45.7 6 8.6 mm; n
5 27), usually with four to eight radially arranged wedge-shaped cells present in transverse cross-section. Multiseriate filaments occasionally constructed of four spheroidal cells
isolated by translucent outer wall material or,
rarely, of many close-packed spheroidal cells
with no intervening matrix. Some filaments
with intervals of both the uniseriate and multiseriate habits, the ratio of multiseriate to uniseriate filament diameter ranging from 1.0 to
2.1 (x̄ 5 1.5 6 0.3; n 5 13). All filaments surrounded by a prominent but relatively translucent outer wall. Lobate multicellular holdfast structure connected to remainder of filament via a single cell.
Material. Chert/carbonate sample 87-HUST1 (20 thin-sections, 10001 specimens); 87HUST-2 (2 thin-sections); 87-HUST-5 (5 thinsections); 87-HUST-7 (3 thin-sections); 87-HUST-8 (2 thin-sections).
Paratypes. Thin-section number and England Finder coordinates in parentheses.
HUPC 62995, Figure 3B (HUST-1Q, O-45);
HUPC 62996, Figure 4E (HUST-1E, J-25);
HUPC 62997, Figure 4F (HUST-1A, N-40);
HUPC 62998, Figure 5C (HUST-1R, M-17);
HUPC 62999, Figure 5E (HUST-1A, O-34);
HUPC 62919, Figure 5H (HUST-1B, M-42);
HUPC 62910, Figure 5I (HUST-1A, O-37);
HUPC 63011, Figure 6A (HUST-1C, N-38).
Discussion. Most multicellular organisms
undergo an ontogenetic development originating from a single cell. This certainly was
MESOPROTEROZOIC SEX AND MULTICELLULARITY
the case with Bangiomorpha pubescens n. gen.,
n. sp., and the large populations in the Hunting Formation allow a nearly complete reconstruction of its ontogeny (Figs. 3–5). Although
diagnosed on its multicellular habit, the initial
single-celled (Fig. 4A) and double-celled (Fig.
4B) stages of Bangiomorpha can be identified by
the specific character of their cell walls, in particular the relatively dark, pointillistically textured inner cell wall surrounded by a relatively translucent outer wall. Filament growth
was initiated by the first cell division, oriented
parallel to the substrate. By the four-celled
stage (Fig. 4C), the characteristic pairing of
cells reveals the transverse intercalary nature
of cell division in uniseriate filaments; centripetal cytokinesis is documented by the
common occurrence of prominent circumferential furrows (e.g., Fig. 3B). The basal holdfast is first seen to differentiate at the ca. 12–
16 cell stage (Fig. 4F,G) and typically develops
as a multilobed (usually two, but sometimes
four or more) multicellular structure connected to the rest of the filament via a single cell
(Fig. 6).
At some, presumably relatively mature,
stage the cells of some Bangiomorpha filaments
underwent longitudinal (with respect to the
filament) intercalary division giving rise to
multiseriate filaments. There are, however, at
least three variations to the general pattern:
Type 1: In most instances the intercalary division was oriented radially resulting in four
or eight wedge-shaped cells arranged around
a central space (Fig. 5E). The mean diameter
of all such filaments is 46.2 6 7.4 mm (n 5 23).
In specimens with both uniseriate and multiseriate portions (n 5 9), the mean multiseriate
diameter is 42.0 6 5.5 mm and the adjacent uniseriate diameter 30.6 6 6.4 mm; the ratio of
uniseriate to multiseriate diameter ranges
from unity to 1.8 (x̄ 5 1.4 6 0.3). Type 2: In a
few instances, longitudinal intercalary division gave rise to relatively few spheroidal cells
separated from one another by translucent
outer wall material (Fig. 5A,D). Mean filament
diameter is 40.0 6 9.1 mm (n 5 4). In specimens with both uniseriate and multiseriate
portions (n 5 3), the mean multiseriate diameter is 36.7 6 8.0 mm and the adjacent uniseriate diameter 24.0 6 7.0 mm; the ratio of
391
FIGURE 3. Bangiomorpha pubescens n. gen. n. sp. Thinsection identification and England Finder coordinates
appear in parentheses. A, HUPC 63000 (HUST-1P, M32). B, HUPC 62995 (HUST-1Q, O-45), paratype; note
the hierarchically paired cells reflecting diffuse transverse intercalary cell division. C, HUPC 63001 (HUST1Q, P-25); note the multiseriate portions of the filament,
unaccompanied by filament expansion; scale as for A.
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NICHOLAS J. BUTTERFIELD
FIGURE 4. Early ontogeny of Bangiomorpha pubescens n. gen. n. sp. Thin-section identification and England Finder
coordinates appear in parentheses. A, HUPC 63002 (HUST-1N, W-67); single cell with characteristic dark inner cell
wall and translucent outer wall. B, HUPC 63003 (HUST-1D, P-33); two cells. C, HUPC 63004 (HUST-1C, O-20); four
cells. D, HUPC 63005 (HUST-1A, J-22); eight cells. E, HUPC 62996 (HUST-1E, J-25), paratype; ca. 16 cells. F, HUPC
62997 (HUST-1A, N-40), paratype; ca. 16-celled filament with an incipient basal holdfast structure. G, HUPC 63006
(HUST-1D, O-34); ca. 12-celled filament with clearly differentiated basal cells. Scale for A–D, F, G as for E.
uniseriate to multiseriate diameter ranges
from 1.2 to 2.1 (x̄ 5 1.6 6 0.4). Type 3: In a single specimen, the multiseriate portion of a filament is composed of many close-packed
spheroids with translucent outer-wall material limited to the margins of the filament (Fig.
5H); it is 63 mm in diameter and the adjacent
uniseriate portion 30 mm, for a ratio of 2.1.
This specimen also includes a basal holdfast,
thus revealing the basipetal maturation of
Bangiomorpha.
Clearly there is a wide range of variation in
the multicellular habit of Bangiomorpha. In
some instances, for example, the shift to the
multiseriate condition was accompanied by
considerable filament expansion (Fig. 5A–
C,H), and in others none (Fig. 3C). Although
most multiseriate filaments are associated
with relatively large-diameter uniseriate filaments, this is not always the case (e.g., Fig.
5A). There is also an indication (not statistically significant) that Type 2 multiseriate filaments were narrower and derived from
somewhat smaller-diameter uniseriate filaments than the other two types. In any event,
with uniseriate filaments up to 45 mm diameter and multiseriate filaments as narrow as 30
mm, it is clear that maturation in Bangiomorpha
MESOPROTEROZOIC SEX AND MULTICELLULARITY
393
FIGURE 5. Bangiomorpha pubescens n. gen. n. sp. Thin-section identification and England Finder coordinates appear
in parentheses. A, HUPC 63007 (HUST-1L, L-49); Type 2. B, HUPC 63008 (HUST-1L, L-49); Type 1. C, HUPC 62998
(HUST-1R, M-17), paratype; Type 1. D, HUPC 62999 (HUST-1A, O-34), paratype; Type 2 transverse section. E,
HUPC 62912 (HUST-1A, O-35), holotype; Type 1, transverse section. F, HUPC 63009 (HUST-1A, O-35); Type 1,
oblique section. G, HUPC 63010 (HUST-1A, O-34); uniseriate filament, transverse section. H, HUPC 62919 (HUST1B, M-42), paratype; Type 3. I, HUPC 62910 (HUST-1A, O-37), paratype; Type 2. All to scale in H.
394
NICHOLAS J. BUTTERFIELD
FIGURE 6. Bangiomorpha pubescens n. gen. n. sp. showing range of differentiated holdfast structures. Thin-section
identification and England Finder coordinates appear in parentheses. A, HUPC 63011 (HUST-1C, N-38), paratype;
typical bilobed basal holdfast. B, HUPC 63012 (HUST-1D, L-58); uniseriate filament with bilobed basal holdfast;
note brittle breakage, suggestive of very early, probably primary, silicification. C, HUPC 62920 (HUST-1A, O-36);
filament with multilobed, multicellular basal holdfast. D, HUPC 63013 (HUST-1G(a), R-45); pronounced bilobed
holdfast. E, HUPC 63014 (HUST-1L, M-49); higher magnification view of a multicellular basal structure, surrounded
by outer wall. F, HUPC 63015 (HUST-1C, N-36); clustered uniseriate filaments with basal holdfasts. G, HUPC 63016
(HUST-1C, M-43). Scale for A–D, G as for F.
was not simply a matter of size. With ecophenotypic effects limited by the close proximity of all these filaments (all types occur in
a single hand sample), it is clear that Bangiomorpha had at least two, possibly more, distinct
ontogenetic fates.
Comparison with Modern Bangia. In most
details of its morphology and ontogeny, Bangiomorpha n. gen. compares closely with the
haploid phase of the modern red alga Bangia,
a Recent cosmopolitan seaweed that colonizes
shallow-water, often emergent, hard substrates in both marine and freshwater settings
(Geesink 1973; Sheath and Cole 1980, 1984;
Sheath et al. 1985). Modern Bangia has a biphasic life cycle with a macroscopic, haploid,
gametophytic generation—the ‘‘bangia’’ phase—
alternating with a microscopic, diploid, sporophytic ‘‘conchocelis’’ phase. Bangia-phase
filaments are unbranched and, when immature, composed of a single (uniseriate) row of
stacked, disk-shaped cells. The polysaccharide cell walls are distinctly biphasic, with a
conspicuous inner wall that defines individual
cells and an outer wall enveloping the whole
organism (Cole et al. 1985); the translucent
MESOPROTEROZOIC SEX AND MULTICELLULARITY
FIGURE 7. Modern mature (multiseriate) Bangia atropurpurea in transverse cross-section. A–C, Asexual/vegetative filament showing the radially arranged wedgeshaped cells. D, Portion of female plant showing the 8–
16 fertilized carpospores produced by each wedgeshaped cell. E, Portion of male plant showing the ca. 128
spermatia produced by each wedge-shaped cell. Redrawn from Garbary et al. 1980.
material that constitutes this outer wall may
also occupy the central part of more mature
multiseriate filaments (Fig. 7). A submicronthick ‘‘cuticle’’ gives the filament a sharply delineated outer wall.
Gametophytic Bangia is notable in having
three reproductive types—asexual, male, and
female—which can be distinguished on the
basis of cellular morphology. Female Bangia
filaments tend to be the largest diameter,
males intermediate and asexual filaments the
narrowest, although absolute dimensions vary
between habitats and regions. For example,
populations of asexual filaments have a mean
maximum diameter of 75.3 6 0.9 mm in the
Great Lakes, but 157 6 3.2 mm in the Pacific
Ocean; males range from 86.2 6 4.1 mm in the
Atlantic to 124 6 7.6 mm in the Pacific; and females from 127 6 4.0 mm in the Atlantic to 171
6 8.1 mm in the Pacific (Sheath and Cole 1984).
Germlings, however, are considerably narrower, 11.1–20.8 mm diameter (Sheath and
Cole 1984), and Geesink (1973) has reported
filaments from the Netherlands up to 15 cm
long that measure just ca. 20 mm diameter at
the (uniseriate) base and 20–80 mm at the
(multiseriate) apex.
Growth of a Bangia filament from a germinating asexual monospore (or a conchocelis-
395
derived conchospore) begins with the differentiation of a basal attachment structure followed by cell division parallel to the substrate
(Sommerfeld and Nichols 1970) (unlike in
Bangiomorpha, where holdfast differentiation is
initiated only at the 12–16 cell stage). Except
for this basal cell, all cells then divide in the
same plane (diffuse intercalary cell division)
to produce an unbranched uniseriate filament.
Uniseriate Bangia filaments are induced to
become multiseriate by specific light and temperature conditions (Sommerfeld and Nichols
1973), a process that begins at the apex and
proceeds basipetally. The first stage involves
a longitudinal intercalary cell division of a
distal uniserial cell, resulting in 4, 8, or 16
wedge-shaped cells arranged radially around
a central space (Fig. 7A–C). Depending on the
filament type, the diameter of multiserial portions of filaments may be either several times
that of uniserial portions or much the same
(Sommerfeld and Nichols 1970). In either case,
the resultant daughter cells typically retain
their positions and thereby reflect the original
uniserial arrangement of the mother cells.
Subsequent maturation involves the production of reproductive spores, which can be
recognized by (1) further intercalary division,
(2) a spatial separation of the constituent cells,
and/or (3) the acquisition of spheroidal cell
shape. It is at this stage that it is possible to
distinguish, on the basis of morphology, asexual, male, and female filaments. In asexual
Bangia, individual vegetative cells are transformed directly into asexual reproductive
spores without intervening division (Garbary
et al. 1980; but see Cole et al. 1985: Fig. 11 for
a possible exception); thus a single uniserial
cell, having divided radially to produce 4–16
vegetative wedge-shaped cells, will produce
4–16 monospores. In male Bangia, each of the
wedge-shaped cells undergoes repeated divisions to produce up to 128 small, colorless
spermatia; thus an original uniserial cell
might yield up to 2048 spermatia (Fig. 7E). In
female Bangia, the wedge-shaped cells transform directly into carpogonia, which, following fertilization, divide to form 8–16 carpospores (Fig. 7D); thus an original uniserial cell
typically yields 4–16 carpogonia, but 32–256
carpospores.
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NICHOLAS J. BUTTERFIELD
Released carpospores germinate to produce
the diploid conchocelis phase of the Bangia life
cycle. The conchocelis differs conspicuously
from the bangia phase, having a microscopic,
branching, uniseriate thallus that grows endolithically within carbonate substrates (Cole
and Conway 1980). Following meiotic reduction, the conchocelis produces haploid conchospores, which complete the life cycle by
germinating bangia-phase filaments. The bangiophyte conchocelis is thought to be of particular evolutionary importance in that it expresses a variety of characteristics typical of
the florideophyte red algae, e.g., apical
growth, plugged pit connections, multiple ribbon-shaped chloroplasts, peripherally positioned chloroplasts, and a central vacuole
(Cole and Conway 1975). The implication is
that the florideophytes may have arisen as a
consequence of sexual reproduction in bangiophytes.
Given the compelling case for identifying
Bangiomorpha as a bangiacean red alga, it is
worth considering the marked variation in
(multiseriate) form as reflecting different reproductive types, as it does in modern Bangia.
It is the mature, spore-bearing filaments (i.e.,
those bearing differentiated spheroidal cells)
that provide the most convincing evidence:
whereas Type 2 filaments (Fig. 5A,D) appear
to have derived just a single spore from each
of four vegetative, wedge-shaped cells, Type 3
filaments (Fig. 5H) clearly underwent significant tertiary division such that each wedgeshaped cell produced many spores. By comparison with Bangia, the former would appear
to represent asexual monospores or unfertilized carpogonia, and the latter fertilized carpospores or spermatia (compare with Fig. 7)
(Garbary et al. 1980). By the same token, Type
1 filaments are identified as vegetative plants
that have yet to differentiate identifiable spore
or gamete types. Although imperfect preservation frustrates exact identification of particular reproductive types in Bangiomorpha, the
marked differences in ontogenetic pattern
make a convincing case for the presence of differing reproductive types and therefore sexual
reproduction. Positive identification of sex in
the Proterozoic is of course significant in that
it has been regularly invoked (Schopf et al.
1973; Stanley 1975; Knoll 1992), but rarely
documented (see Zhang and Yuan 1996), as a
key innovation in early eukaryotic evolution.
Bangiomorpha is the earliest direct evidence for
such a habit.
There is no direct evidence for a conchocelis
phase—the expected consequence of bangiophyte sexual reproduction—in the Hunting assemblages. This is not entirely unexpected given the distinct habits (and accompanying taphonomies) of the two phases. The
oldest, indeed the only, reported fossil conchocelis occurs in Late Silurian rocks from Poland (Campbell 1980) and is not associated
with a haploid phase. It may be, of course, that
a conchocelis does occur in the Hunting assemblages but has simply not being recognized as such; certainly there is no necessity
that the entire life cycle of Bangiomorpha mirror that of modern Bangia. In any event, absence of a recognized conchocelis in no way
implies that Bangiomorpha was asexual (see below).
The Early Fossil Record of Eukaryotes
With a well-constrained age of ca. 1200 million years, Bangiomorpha is the oldest taxonomically resolved eukaryote yet reported
and thus represents a key (minimum) datum
point for constraining eukaryote evolution.
Certainly there are older eukaryotic fossils,
but a dearth of preserved characters precludes
any satisfactory taxonomic placement. Macroscopic coiled filaments from the Paleoproterozoic Negaunee Iron Formation, Michigan,
for example, have been compared with large
coenocytic chlorophytes (Han and Runnegar
1992), but realistically cannot be distinguished from numerous other groups, including colonial prokaryotes. The same is true for
the diverse macrofossils reported from the ca.
1700-Ma Chuanlinggou and Tuanshanzi Formation s (Changcheng System), Jixian, China
(Zhu and Chen 1995; Yan 1995; Yan and Liu
1997); an exception here is Qingshania (Chuanlinggou Fm.), a relatively large-diameter filament which is at least convincingly eukaryotic
(Yan 1989). Early eukaryotes are also recognized among the acritarchs beginning around
1850 Ma (Zhang 1997). Although of unknown
taxonomic affinity, relatively large acritarchs
MESOPROTEROZOIC SEX AND MULTICELLULARITY
(.50 mm diameter) are generally accepted as
representing a eukaryotic grade of organization. Eukaryotic biomarker molecules are now
recognized as far back as the late Archean (2.7
Ga [Brocks et al. 1999]).
Eukaryote diversity remains conspicuously
low through most of the Mesoproterozoic
(1600–1000 Ma). Larger acritarchs, although
widespread, are represented by simple sphaeromorphs (Knoll 1994). The coiled macrofossil
Grypania, reasonably interpreted as an individual eukaryote and broadly distributed by
ca. 1400 Ma (Walter et al. 1990; Kumar 1995),
appears to be unaccompanied by other multicellular/macroscopic fossils (with the possible exception of problematic ‘‘string of
beads’’ imprints from Montana and Australia
[Horodyski 1993]). It is only toward the end of
the Mesoproterozoic that diversity is seen to
increase, most notably perhaps with the appearance of Bangiomorpha (Rhodophyta) and
other possible eukaryotes in the Hunting Formation (Butterfield in press). In the terminal
Mesoproterozoic and/or earliest Neoproterozoic, diversity rises further with the introduction of increasingly diverse ornamented acritarchs (Knoll 1992, 1994; Xiao et al. 1997) and,
in the ca. 1000-Ma Lakhanda Formation of Siberia, the first appearance of a fossil stramenopile, Palaeovaucheria (Hermann 1981; Woods
et al. 1998). Diversity and taxonomic resolution continue to rise through the early–middle
Neoproterozoic with the identification of possible dinoflagellates (alveolates) in the ca. 850Ma Wynniatt Formation, arctic Canada (Butterfield and Rainbird 1998) and of several taxa
of green algae (chlorophytes) in the ca. 750-Ma
Svanbergfjellet Formation, Spitsbergen (Butterfield et al. 1994). Possible ‘‘phylloid’’ algae
are also reported from the early Neoproterozoic Pahrump Group of California (Horodyski
and Mankiewicz 1990); ‘‘scale microfossils’’
from the middle Neoproterozoic Tindir
Group, Alaska, are reminiscent of certain
chrysophyte or diatom elements (Allison and
Hilgert 1986; Kaufman et al. 1992); and vaseshaped microfossils found through much of
the Neoproterozoic are interpreted as testate
amoebae (Porter and Knoll, this issue). Thus,
by the middle of the Neoproterozoic there is
397
good fossil evidence for the divergence of
most of the major algal/protistan clades.
Despite the early appearance of these sundry groups, it is important to recognize that
the data are exceedingly sparse, typically single occurrences that precede the next appearance in the fossil record by hundreds of millions of years. Taken individually they are unlikely to offer even a crude approximation of
actual first appearances. Collectively, however, there does appear to be a genuine signal,
with the interval between 1200 and 700 Ma
conspicuously more diverse than the preceding 500 million years. The reality of this pattern—to the extent of documenting a major
Meso/Neoproterozoic radiation of eukaryotes
(Knoll 1992)—is bolstered by the accompanying diversity increase among the much better sampled acritarchs (Knoll 1994), as well as
molecular analyses suggesting a ‘‘big bang’’
origination of the principal eukaryotic lineages (Knoll 1992; Philippe and Adoutte 1998;
Philippe et al. in press). Such an interpretation
accords with the pulsed pattern of diversification expected during adaptive radiation,
though there is no evidence that this proceeded at a rate comparable to, say, the ‘‘Cambrian
explosion’’; indeed, evidence from the acritarch record points to a fundamentally slower
evolutionary turnover among Proterozoic eukaryotes compared to their Phanerozoic counterparts (Knoll 1994).
The Red Algae in Early Eukaryotic
Evolution
The red algae have been shunted widely
about in eukaryotic phylogenies. Beginning in
the mid–nineteenth century (see Ragan and
Gutell 1995), they were considered among the
most ancient eukaryotes because of their universal lack of flagella, basal bodies and centrioles and their conspicuously cyanobacterialike chloroplasts (e.g., phycobilin pigments
and unstacked thylakoids). This basal positioning acquired some support from early
molecular phylogenetic analyses based on 5S
rRNA (Hori and Osawa 1987). Subsequent
work, however, using the larger and presumably more reliable SSU rRNA (Bhattacharya et
al. 1990; Hendriks et al. 1991; Kumar and
Rzhetsky 1996) and LSU rRNA (Perasso et al.
398
NICHOLAS J. BUTTERFIELD
1989), positioned them relatively late in eukaryotic evolution, arising more or less coincidentally with other major eukaryotic clades;
e.g., the alveolates, stramenopiles, chlorophytes, fungi, and metazoans. Within these
‘‘crown eukaryotes’’ the red algae have been
considered a sister group of the chlorophytes
(Ragan and Gutell 1995) or of a more basal
plant/animal/fungi clade (Kumar and Rzhetsky (1996), despite the widespread recognition that rRNA offers limited phylogenetic
resolution at this level (Ragan and Gutell 1995;
Delwiche and Palmer 1997; Hirt et al. 1999;
Phillippe et al. in press).
Most other molecules that have been applied to eukaryotic phylogeny (e.g., elongation
factors, tubulins, hsp70, GAPDH) yield similarly tenuous results (Delwiche and Palmer
1997). By contrast, RPB1, the gene encoding
the largest subunit of RNA polymerase II, provides strong statistical support for the divergence of the Rhodophyta diverging before the
last common ancestor of an unresolved
‘‘crown’’ (Stiller and Hall 1997), indeed one of
the few instances of statistical support for any
relationship at this taxonomic level (Delwiche
and Palmer 1997; but see Moreira et al. 2000).
Insofar as many, perhaps all (Philippe et al. in
press) of the purportedly ancient eukaryotic
groups that occupy the ‘‘stem’’ of SSU rRNA–
based trees are now recognized as derived
constituents of the ‘‘crown’’ (Hirt et al. 1999;
Stiller and Hall 1999; Philippe et al. in press),
the red algae might once again be considered
an early-diverging lineage. By extension, their
lack of flagella and related structures might
thus reflect the ancestral eukaryotic condition.
Within the red algae, molecular analyses
have contributed more clearly to phylogenetic
resolution. The two rhodophyte classes (Bangiophyceae and Florideophyceae) are separated on the basis of both SSU rRNA (Ragan et
al. 1994) and plastid rbcL (Freshwater et al.
1994), with the bangiophytes consistently occupying the most basal branches. Unlike the
clearly monophyletic florideophytes, the bangiophytes are highly divergent, to the extent
that they are likely to be ‘‘polyphyletic’’ (5
paraphyletic [Ragan et al. 1994]). Within the
Bangiophyceae, the order Bangiales appears
to be relatively derived and monophyletic,
though notably divergent, as with the red algae as a whole (Ragan et al. 1994).
Multicellularity
By introducing large size, complex morphology, and thereby increasingly complex
ecology, the introduction of eukaryotic multicellularity represents a critical threshold in
the history of life. Such organization is first
documented convincingly by the simple cellular filaments of ca. 1700-Ma Qingshania, followed by the macroscopic, possibly coenocytic Grypania at ca. 1400 Ma. Although not the
oldest multicellular eukaryote, Bangiomorpha
nevertheless holds special status as the first on
record to exhibit true cellular differentiation
and specialization. Unlike any of its predecessors, Bangiomorpha had, for example, a differentiated holdfast, multiple cycles of cell division, differentiated spores, and sexually differentiated whole plants.
In one sense, multicellularity is nothing
more than the substitution of somatic for reproductive mitosis (Kondrashov 1997). In the
simplest case this will result in a multicellular
mass of identical cells. Differing local environments might then lead to differing fates for
particular cell lineages and so to the emergence of (multicellular) organism-level characteristics. In the first instance this likely involved little more than intercellular attachment or arrangement, e.g., acquisition of a filamentous habit and/or vertical orientation.
More profound organism-level characteristics
would have arisen with the introduction of
asymmetric cell division, where the differing
fates of sister cells give rise to specialization
and an intraorganismal division of labor (see
Horvitz and Herskowitz 1992; Maynard Smith
and Szathmáry 1995; Kirk 1998). Combined
with the eukaryotic potential for large size
and sophisticated development, such novelty
would have opened up fundamental new areas of morphospace.
As with any evolutionary innovation, ecology assuredly played a critical role in the origin of eukaryotic multicellularity. Large size
and complexity present a variety of otherwise
unavailable habits conferring selective advantage, including predator evasion and an enhanced uptake and storage of essential nutri-
MESOPROTEROZOIC SEX AND MULTICELLULARITY
ents (Kirk 1998). In the case of Bangiomorpha,
and perhaps other early metaphytes, multicellularity also introduced a novel approach
to benthic photosynthesis: with a differentiated basal attachment structure imparting
current and wave resistance, multicellular filaments could now compete effectively for
light and nutrients by growing vertically (Fig.
2). Vertical orientation in turn introduces a
substantial new aspect to shallow-water environments, affecting bottom-water currents,
sediment transport and trapping characteristics, chemical exchange, and a host of biological interactions (Carpenter and Williams
1993); indeed, vertically oriented turf-forming
algae are recognized today as the basis of a
distinct benthic community (Hay 1981). Insofar as modern algal turfs also contribute importantly to environmental patchiness and
overall benthic heterogeneity (Airoldi and
Virgilio 1998), it would also appear that the
early evolution of vertical orientation—tiering—would have contributed importantly to
the diversification of Proterozoic environments, just as it has in the Phanerozoic (e.g.,
Bottjer and Ausich 1986). Differential effects
on sedimentation and sedimentary fabric no
doubt played a further role in the mid-Mesoproterozoic diversification and early Neoproterozoic decline of stromatolites (see Grotzinger and Knoll 1999). More generally, by breaking the hegemony of horizontally oriented microbial mats, vertically oriented algal turfs
might well have triggered a mutual feedback
system of diversification (see Stanley 1973),
broadly expressed as the Mesoproterozoic/
Neoproterozoic radiation.
Other Mesoproterozoic organisms may also
have contributed to this effect. Various bacteria and cyanobacteria are known to grow vertically, and simple vertically oriented filaments have previously been reported from
late Mesoproterozoic microbial mat assemblages (Knoll and Sergeev 1995: Fig. 3). These,
however, are on a much smaller scale than that
seen with Bangiomorpha, and are limited fundamentally by their prokaryotic organization
(see below). Mesoproterozoic Grypania has
also been interpreted as a benthic macrophyte,
presumably with the axis of its coiled filament
oriented vertically (Walter et al. 1990; Runne-
399
gar 1994; Kumar 1995). It does not, however,
show any evidence of a terminal holdfast or
indeed any cellular or morphological differentiation.
Sexuality
The appearance of sexual reproduction—
i.e., syngamy, genetic recombination and meiosis—has long been considered a major evolutionary threshold, giving rise to a fundamental increase in variation (Schopf et al.
1973), a novel ability to remove deleterious
mutations (Muller 1964), and indeed ‘‘true’’
species and speciation (Stanley 1975). The
presence of at least two distinct spore-producing phases in Bangiomorpha, and their close
comparison to sexual phases in modern Bangia, presents a convincing case for eukaryotic
sex by at least ca. 1200 Ma.
Sex appears to be plesiomorphic, if not necessarily monophyletic (Ruvinsky 1997), for all
eukaryotes with a differentiated multicellular
grade of organization (Bell 1982; Buss 1987;
Grosberg and Strathman 1998; Dacks and
Roger 1999), and there is a compelling case for
considering sex to be a prerequisite for eukaryotic multicellularity. At one level, it would
appear that the intercellular recognition and
coordination critical to sexual reproduction
are very much the same kinds of processes involved in the development of a multicellular
organism. Thus, appearance of sex, for whatever reason, might have introduced a collateral capacity for multicellularity.
At another level, sex—in particular, obligate
sex (Dacks and Roger 1999)—would appear to
be necessary for the evolution of multicellularity simply to override the inherent conflict
between the individual and its constituent
cells (Buss 1987; Michod 1997). Differentiated,
functionally specialized somatic cells are of
obvious selective advantage to the whole organism but, by diminishing their individual
reproductive capacity, are at a severe competitive disadvantage next to any cell retaining,
or capable of reverting to, its original totipotent condition. In asexual lineages there is no
way of excising such ‘‘somatic cell parasites’’
(Muller’s ratchet), and any potential multicellular organism will, so it is argued, eventually
reduce to a mass of undifferentiated cells. Sex-
400
NICHOLAS J. BUTTERFIELD
ual reproduction, by contrast, allows for the
periodic removal of these ‘‘parasites,’’ allowing the selective forces on the multicellular individual to take precedence over that of its
cells (Buss 1987). It is a powerful argument
(despite the existence of cellularly differentiated prokaryotes, e.g., heterocystous cyanobacteria) and, insofar as Bangiomorpha features
differentiated vegetative cells (e.g., the basal
holdfast), corroborates its status as an early
sexually reproducing organism. By contrast,
neither Qingshania nor Grypania shows any evidence of the cellular differentiation that
would suggest sexuality.
True somatic differentiation in Bangiomorpha was limited to its basal holdfast structure;
apart from the differentiated spores/gametes,
all other cells were effectively identical, underwent regular mitosis and contributed
equally to plant elongation (i.e., diffuse intercalary division). This pattern is entirely distinct from the apical meristem–type growth of
most (but not all [Table 1]) other metaphytes
and would appear to represent a particularly
primitive grade of multicellularity (progressive loss of cellular totipotency being the logical consequence of evolving multicellular lineages [see Buss 1987]). Indeed, the present fossil material might be interpreted as evidence
for such a gradient even within the Bangiaceae: whereas holdfast differentiation in Bangiomorpha was not initiated, i.e., totipotency
not abandoned, until the 12–16 cell stage (Fig.
4F,G), modern Bangia differentiates its basal
cell following the first cell division.
Sexual reproduction results in a haploiddiploid alternation of generations, which itself
offers a rich source of evolutionary novelty
(Mable and Otto 1998). In the case of the red
algae, the sexually derived diploid conchocelis
phase of the Bangiales appears to be the link
between the basal Bangiophyceae and the derived Florideophyceae (Cole and Conway
1975). The presence of sexually reproducing
bangiophytes at ca. 1200 Ma thus suggests an
early initiation of the florideophyte grade of
organization, if not necessarily its cladogenetic independence. The first fossils reasonably
interpreted as florideophytes follow the Hunting bangiophytes by some 600 million years;
i.e., phosphatized cellular thalli of Paramecia
and Thallophyca in the terminal Neoproterozoic Doushantuo Formation of South China
(Zhang et al. 1998).
Evolutionary Implications
Bangiomorpha is the oldest taxonomically resolved eukaryote on record. As such it provides a key datum point for resolving/constraining protistan phylogeny, particularly
molecular clock hypotheses (e.g., Kumar and
Rzhetsky 1996). The precise taxonomic assignment of this fossil—to the family level—is
based on detailed comparison with the living
rhodophyte Bangia. Neither the morphology
nor ontogeny of this lineage has changed appreciably for some 1200 million years. Such
‘‘living fossil’’-type longevity might be ascribed to a variety of factors but is most likely
related to the unusually harsh conditions of
the upper intertidal habitat; like Bangia, Bangiomorpha would have been regularly exposed
to highly variable salinities and intervals of
complete desiccation. It is interesting to note
here that other early multicellular fossils also
exhibit pronounced morphological stasis and
likewise have modern counterparts with
broad salinity tolerances; e.g., both Vaucheria
(cf. ca. 1000-Ma Palaeovaucheria Hermann 1981)
and Cladophora (cf. ca. 750-Ma Proterocladus
Butterfield 1994) range from marine to freshwater and even subaerial environments
(Fritsch 1935).
With its clear differentiation of sexual
morphs Bangiomorpha is the oldest confirmed
example of eukaryotic sex. There is of course,
a much more ancient record of eukaryotes
(Brocks et al. 1999), as well as a good case for
sex representing the plesiomorphic condition
among exant eukaryotes (Dacks and Roger
1999). This is not to suggest, however, that
sexual reproduction was coincident with the
origin of the eukaryotic cell (though it might
well be implicated in the much later radiation
of crown-group eukaryotes [i.e., the last common ancestor of extant groups plus all its descendants]). On the other hand, there is a
strong case to be made for a near-synchronous
appearance of sexual reproduction and complex multicellularity: in addition to sex being
necessary for a differentiated multicellular
grade of organization (through its ability to
MESOPROTEROZOIC SEX AND MULTICELLULARITY
shed somatic cell parasites), the clear ecological advantages of eukaryotic multicellularity
virtually assure its immediate succession. If
this were the case, then the most reliable proxy
for the appearance of sexual reproduction
would be the first appearance of complex multicellularity. Bangiomorpha in the ca. 1200-Ma
Hunting Formation is the oldest confirmed example of complex multicellularity.
The existence of numerous entirely unicellular eukaryotic clades suggests that complex
multicellularity was not the primary impetus
for the evolution of sex (see Bell 1982). Rather,
sex introduced the opportunity of multicellularity, which was then exploited in various
lineages and in various ways as selective advantages were discovered. Although limited
initially, such opportunities would have expanded as accumulating morphology created
novel environments and increasingly complex
ecologies. Intriguingly, Stiller and Hall (1998)
have presented molecular evidence for the
particularly primitive nature of multicellularity in the red algae.
Both the fossil and molecular records point
to an early but ecologically inconspicuous history of eukaryotic life, followed by a major radiation somewhere in the vicinity of the Mesoproterozoic/Neoproterozoic boundary (1
Ga). What was responsible for this ‘‘big bang
of eukaryotic evolution’’? Or, alternatively,
how was it that eukaryotes appeared so early
but took so long to diversify (or indeed to
make a significant contribution to the biogeochemical record [Summons et al. 1999])? Brasier and Lindsay (1998) argue that much of
this time was occupied simply assembling the
various components of the modern eukaryotic
cell. The mitochondrion, however, is probably
more closely tied to the Archean origin of eukaryotes (Martin and Müller 1998), and the
chloroplast to their Paleoproterozoic appearance in the body-fossil record (Knoll 1992). Alternatively, delayed evolution/acquisition of
the eukaryotic flagellar apparatus might be
invoked, particularly in light of arguments for
the aflagellate red algae representing the ancestral eukaryotic condition (see above).
The more common explanation for the Mesoproterozoic/Neoproterozoic radiation is
that it followed from the appearance of sexual
401
reproduction (Schopf et al. 1973; Knoll 1992).
This, I think, is surely correct, but not for the
reasons usually proffered. True, sex would
have greatly enhanced the genetic flexibility of
eukaryotes, but this alone cannot explain their
expansion into a biosphere already monopolized by highly adaptable prokaryotes. Without recourse to mass extinction, the displacement of such incumbents requires clear-cut
ecological superiority. The one, perhaps only,
field in which eukaryotes categorically outpace the Bacteria and Archaea is in their capacity for morphological differentiation, multicellularity, and large size. The reason sex was
critical in eukaryotic evolution was that it introduced organismal morphology as a significant evolutionary factor, a new way to play
the game that was simply beyond the means
of the prokaryotic grade of organization.
At one level this alone is sufficient—after
all, complex multicellularity constitutes much
of the phenomenon we are seeking to explain.
The more fundamental consequence of multicellularity, however, has to do with the revolutionary effects of morphology on Proterozoic ecology. Whereas the developmental/
morphological simplicity of prokaryotes condemns them forever to operate in a simplistic
physical environment, multicellular eukaryotes invented a biological environment, in
particular, one with a virtually unlimited capacity for morphological complexity and size.
With such conditions, of course, comes a host
of complex ecological interactions, including
powerful feedback effects on environment
(ecological engineering, sensu Jones et al.
1997), organismal coevolution, adaptive reciprocity, and ‘‘progress’’ (indeed, these are an
underlying assumption of logistic models of
diversification for the Phanerozoic [e.g., Sepkoski 1978]). The new world order was a product of multicellular eukaryotes, which in turn
was a consequence of sexual reproduction.
The Mesoproterozoic/Neoproterozoic radiation of eukaryotes might have begun quite
trivially—perhaps tiering on a scale somewhat larger than possible with prokaryotes or
asexual eukaryotes—but the discovery of progressive morphological adaptation was to
lead, perhaps inevitably, to the modern world
of large, complex organisms.
402
NICHOLAS J. BUTTERFIELD
Acknowledgments
I thank R. Buick, J. Stiller, H. Philippe, and
S. Conway Morris for useful discussion, and
A. Knoll and C. Pueschel for very constructive
reviews. Cambridge Earth Science Contribution 5841.
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