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EVOLUTION & DEVELOPMENT
15:6, 466–474 (2013)
DOI: 10.1111/ede.12055
The evo‐devo of multinucleate cells, tissues, and organisms,
and an alternative route to multicellularity
Karl J. Niklas,a,* Edward D. Cobb,a and David R. Crawfordb
a
b
Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA
Department of Philosophy, University of Bristol, Bristol, BS 8 1TB, UK
*Author for correspondence (e‐mail: kjn2@cornell.edu)
SUMMARY Multinucleate cells, tissues, or organisms
occur in 60 families of land plants and in five otherwise
diverse algal lineages (Rhodophyceae, Xanthophyceae,
Chlorophyceae, Ulvophyceae, and Charophyceae). Inspection of a morphospace constructed out of eight developmental
processes reveals a large number of possible variants of
multinucleate cells and organisms that, with two exceptions,
are represented by one or more plant species in one or more
clades. Thus, most of these permutations of developmental
processes exist in nature. Inspection of the morphospace also
shows how the siphonous body plan (a multinucleate cell with
the capacity for indeterminate growth in size) can theoretically
serve as the direct progenitor of a multicellular organism by a
process similar to segregative cell division observed in
siphonocladean algae. Using molecular phylogenies of algal
clades, different evolutionary scenarios are compared to see
how the multicellular condition may have evolved from a
multinucleate unicellular progenitor. We also show that the
siphonous progenitor of a multicellular organism has previously passed through the alignment‐of‐fitness phase (in which
genetic similarity among cells/nuclei minimizes internal
genomic conflict) and the export‐of‐fitness phase (in which
genetically similar cells/nuclei collaborate to achieve a
reproductively integrated multicellular organism). All that is
theoretically required is the evolutionary acquisition of the
capacity to compartmentalize its cytoplasm.
INTRODUCTION
coenocytes (Biao et al. 1988; Ding et al. 1999; Niklas and
Kutschera 2009), i.e., embryophytes are multinucleate supra‐
cellular organisms whose continuous cytoplasm is incompletely
partitioned by a cell wall infrastructure (Niklas and Kaplan 1991).
The appearance of multinucleate cells in 177 land plant
species representing 60 families (Beer and Arber 1919, see
however Burkholder and McVeigh 1941) and in algal clades as
different as the Rhodophyceae (e.g., Griffithsia), Xanthophyceae
(e.g., Vaucheria), Chlorophyceae (e.g., Pediastrum), Ulvophyceae (e.g., Cladophora), and Charophyceae (e.g., Nitella) raises
a number of important but as yet unresolved questions. For
example, are the mechanisms giving rise to multinucleate cells
homologous across different clades? Does this condition provide
an analogue to autopolyploidy without the early negative
consequences of polyvalent chromosomes? Indeed, does it
provide any metabolic or developmental advantage, or does it
simply appear under conditions of neutral or relaxed selection?
Did the siphonous body plan evolve in some cases into a
multicellular body plan, or is it evolutionarily derived from the
latter? These and other questions have been addressed in
different ways depending on the frame of reference of different
authors (e.g., Strasburger 1913; McNaughton and Goff 1990;
Mine et al. 2008). However, all perspectives share a comparative
approach because of the multiple evolutionary origins of
multinucleate cells, tissues, and organisms.
The division of the nucleus is synchronized with the division of
the cytoplasm in the majority of plant and animal cells. However,
many fungi, algae, plants, and animals are composed entirely or
in part of multinucleate cells, e.g., the giant amoeba Chaos chaos
(aka C. carolinensis), the multicellular green alga Cladophora,
and the basal cell of the Pinus embryo. Likewise, there are tissues
and entire organisms that are transiently composed of multinucleate cells, e.g., the free‐nuclear division phase in endosperm
and gymnosperm megagametophyte development. These occurrences demonstrate that karyokinesis is not inextricably coupled
to cytokinesis (as noted by Strasburger 1913), in much the same
way that the duplication of chloroplasts and mitochondria is not
intrinsically coupled to the division of either the nucleus or the
cytoplasm (Imoto et al. 2011). Likewise, there are phylogenetically unrelated organisms that consist of a single multinucleate
cell that can grow indefinitely in size, e.g., the siphonous
(¼ coenocytic) ulvophycean alga Derbesia and the xanthophycean alga Asterosiphon. Some of these organisms are externally
and internally intricate, which shows that multicellularity is not
required to achieve morphological or anatomical complexity
(Fig. 1). Finally, the distributions of plasmodesmata within the
land plants (embryophytes) establish different but interconnecting physiological domains that are functionally analogous to
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Niklas et al.
The evo‐devo of multinucleate cells, tissues, and organisms, and an alternative
467
Fig. 1. A portion of the thallus of the siphonous, holocarpic green
alga Caulerpa cactoides.
The objective of this paper is to explore the developmental
and evolutionary implications of the multinucleate condition and
the siphonous body plan in plants, which are here broadly
defined as photosynthetic eukaryotes to include the algae as well
as the embryophytes. We specifically focus on the possible origin
of a multicellular organism from a siphonous ancestor. In order
to achieve this objective, (1) a previously published morphospace for the body plans of plants elaborated to identify all
possible variants of the multinucleate condition, (2) the existence
of these variants in the different plant clades is assessed, (3) the
phylogenies of different plant clades are examined to determine
whether the siphonous body plan could give rise to a
multicellular organism, and (4) the evolutionary advantages
and disadvantages of multinucleate cells are reviewed and
discussed to determine whether such a transition provides an
evolutionarily expeditious route to multicellularity.
A BODY PLAN MORPHOSPACE
A morphospace is a representation of all theoretically possible
forms of a specific organism or group of organisms
(McGhee 1999). Each axis in a morphospace represents a
variable that describes a phenotypic character (with one or more
character states). Each point in a morphospace represents an
individual with the characters states specified by the variables
identified by intersecting axes. A morphospace for the body
plans of plants was previously constructed using four
developmental features (Niklas 2000; see also Niklas and
Newman 2013): (1) whether or not cytokinesis and karyokinesis
are synchronous, (2) whether or not cells remain aggregated after
they divide, (3) whether or not symplastic continuity is
maintained among the cross walls of neighboring cells, (4)
whether or not individual cells continue to grow indefinitely in
size (Fig. 2). The juxtaposition of these features identifies four
Fig. 2. A morphospace for the four major plant body plans shown in
bold (unicellular, siphonous/coenocytic, colonial, and multicellular)
resulting from the intersection of five developmental processes (e.g.,
karyokinesis and cytokinesis). Note that the siphonous/coenocytic
body plan may evolve from a unicellular or a multicellular
progenitor. The lower panels dealing with the plane of cell division,
localization of cellular division, and symmetry pertain to the
evolution of complex multicellular organisms. Adapted from Niklas
(2000).
major body plans, each of which can be in theory either
uninucleate or multinucleate: (1) the unicellular body plan,
which is characterized by the complete separation of cells after
division coupled with determinate growth in cell size, (2) the
siphonous body plan, which is characterized by the indeterminate growth of a unicellular body plan, (3) the colonial body
plan, which is characterized by the lack of symplastic continuity
among normally aggregated cells, and (4) the multicellular
body plan in which all adjoining cells have the potential to
establish and maintain symplastic continuity. The addition of a
fifth developmental feature –– the orientation of cell division ––
distinguishes among the different tissue constructions of the
multicellular body plan: (1) the unbranched filament, which
results when each cell has the capacity to divide in only one plane
of reference with respect to the body axis, (2) the branched
filament (with or without a pseudoparenchymatous tissue
construction), which requires that each cell has the ability to
divide in two planes of reference, and (3) the parenchymatous
tissue construction, which requires that cells have the ability to
divide in all three planes of reference (Fig. 2).
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Vol. 15, No. 6, November–December 2013
A review of algal cytology and morphology summarized by
Smith (1950), Fritsch (1965), Lee (2008), and Graham et al.
(2009) shows that all but two of the 14 theoretically possible
variants are represented by one or more algal species. For
example, the unicellular multinucleate variant with determinate
growth is represented by the chlorophycean alga Bracteacoccus
and the ulvophycean alga Chlorochytridium; the colonial
multinucleate body plan is represented by the chlorophycean
algae Pediastrum and Hydrodictyon; the siphonous body plan is
represented by the ulvophycean alga Caulerpa and the
xanthophycean alga Vaucheria; and the multicellular multinucleate (siphonocladous) condition is represented by the
rhodophycean alga Griffithsia and the ulvophycean alga
Cladophora (see Graham et al. 2009). Among the siphonocladous variants differing in tissue construction, the unbranched and branched filamentous condition are represented
by the ulvophycean algae Urospora and Acrosiphonia,
respectively; the multicellular body plan with a pseudoparenchymatous tissue construction is represented by species assigned
to the ulvophycean alga Codium. The two variants that are not
represented by any extant or extinct species are the uninucleate
siphonous body plan and the parenchymatous siphonocladous
variants. The absence of the former may be the result of
physiological constraints imposed by the volume of cytoplasm
that a single nucleus can sustain, a hypothesis proposed by Julius
Sachs (1892; see also Baluška et al. 2012). An explanation for
the absence of a parenchymatous siphonocladous body plan is
more problematic. Hommersand and Fredericq (1990) suggest
that morphogenetic constraints imposed by the necessity of
forming cross walls to sequester reproductive cells is responsible
for the lack of parenchymatous tissues in the rhodophytes.
A more detailed rendering of the multinucleate domain within
the plant body plan morphospace is achieved with the addition of
three developmental features, each of which has two character
states: (1) whether or not the adult plant dies after reproducing (i.e.,
holocarpic or non‐holocarpic life cycles), (2) whether or not the
plant produces uninucleate or multinucleate asexual propagules,
and (3) whether or not all cells in a body plan are multinucleate.
The addition of these three developmental features provides a more
diverse landscape for inspection (Fig. 3). Nevertheless, a survey of
the literature once again summarized by Smith (1950), Fritsch
(1965), Lee (2008), and Graham et al. (2009) shows that, with the
aforementioned two exceptions, all of the remaining variants exist
in nature. For example, the siphonous holocarpic variant with
uninucleate propagules is represented by xanthophycean alga
Botrydium and the chlorophycean alga Characiosiphon, whereas
its counterpart with multinucleate propagules is represented by the
xanthophycean alga Vaucheria and the chlorophycean alga
Protosiphon. The presence of uninucleate and multinucleate cells
in the same organism is represented by the external and rhizoidal
cells of the ulvophycean alga Ulva and the apical and sub‐apical
cells of the florideophycean alga Gigartina.
INFERRED CHARACTER POLARITIES
The preceding review permits two conclusions. First, as noted,
almost all of the theoretically possible multinucleate variants are
Fig. 3. An elaboration of the multinucleate condition among the four body plans (see Fig. 2) resulting
from the intersection of three additional developmental processes (e.g., holocarpic life cycle) that
result in 28 possible variants. A survey of the plant
literature shows that all but two of all possible
variants exist in one or more clades.
Niklas et al.
The evo‐devo of multinucleate cells, tissues, and organisms, and an alternative
represented by one or more plant species (i.e., the multinucleate
condition has been extensively evolutionarily explored),
although it is evident that some plant lineages occupy a greater
volume of this morphospace than others. Second, extensive
convergence (or homoplasy) among these variants has occurred,
particularly between the Xanthophyceae and the Ulvophyceae.
This raises a number of questions. For example, the conventional
view concerning the evolutionary origins of multicellularity is
that a unicellular progenitor evolved into a colonial organism
that subsequently evolved multicellularity as a consequence of
passing through an alignment‐of‐fitness phase and an export‐of‐
fitness phase (Grosberg and Strathman 2007; Folse and
Roughgarden 2010), i.e., “unicellular ) colonial ) multicellular” transformation series of body plans. Evidence for this
scenario is found among a number of current phylogenies for the
rhodophytes, stramenopiles, and chlorobionta (Niklas and
Newman 2013). In addition, an “unbranched ) branched )
pesudoparenchymatous ) parenchymatous” tissue transformation series occurs within lineages that have achieved complex
multicellularity (Niklas and Newman 2013).
The evolution and development of the volvocine green algae
provide several cases of the unicellular (uninucleate) ¼>
colonial (uninucleate) transition series (Huxley 1912; Kirk 2005;
Herron and Michod 2008). The ancestral state of volvocines is
unicellular (e.g., Chlamydomonas reinhardtii). Transformation
of the unicellular cell wall into and extracellular matrix (seen in
the Tetrabaenaceae ¼> Goniaceae ¼> Volvocaceae transformation series), incomplete cytokinesis (seen in the Goniaceae
¼> Volvocaceae transformation series), and the appearance of
additional derived traits produce forms ranging from simple
cellular aggregates (e.g., Tetrabaena socialis) to colonies with
complex, asymmetric cell division, to organisms with full germ‐
soma division of labor (e.g., Volvox carteri) (Kirk 2005; Herron
and Michod 2008). Models for these transitions in the volvocines
focus on “cooperation‐conflict‐conflict mediation cycles” that
allowed these algae to achieve both the alignment‐of‐fitness
phase at the cellular level and the export‐of‐fitness phase at the
colony level (Herron and Michod 2008). Evidence for the
transition from colonial to multicellular plant life‐forms is
reviewed by Niklas and Newman (2013).
In contrast, little is known about the transformation series
involving the siphonous/coenocytic body plan, particularly the
possibility that it may serve as the progenitor of a multicellular
body plan. Inspection of the more elaborate multinucleate
morphospace shows that the siphonous body plan can be derived
from a unicellular uni‐ or multinucleate progenitor with the
acquisition of indeterminate growth in cell size (Figs. 2–3).
However, it can also serve as the ancestral condition for a
multicellular organism (by the developmental elaboration of
cross wall formation) just as it may be evolutionarily derived
from a multicellular plant (by the developmental suppression of
cross wall formation). Therefore, the “siphonous ) multicellular” and the “multicellular ) siphonous” body plan transforma-
469
tion series are both theoretically possible. Indeed, the “siphonous
) multicellular” transformation series actually occurs during the
ontogeny of siphonocladean algae by means of a process called
segregative cell division (Fig. 4), which is posited to have
evolved by the co‐option of a wound healing response
mechanism (Børgesen 1905; Le Claire 1982; Graham
et al. 2009) as for example the wound response of the siphonous
green alga Boergesenia forbesii. Analogs of segregative cell
division are seen in endosperm free‐nuclear development
(Schnarf 1931), the early embryology of gymnosperms such
as Welwitschia (Bower 1881), Drosophila embryogenesis
preceding the formation of the blastoderm (Zalokar and
Erk 1976; Foe and Alberts 1983), and zoospore differentiation
of Blastocladiella and other chytrids (Lessie and Lovett 1968).
These and other speculations about the evolution of
multinucleate cells, tissues, or organisms can be evaluated
with parsimony‐based character state reconstructions of the
phylogeny of selected plant lineages. Barring extensive
character state reversals, it should be possible to infer whether
the siphonous body plan is ancestral or derived in one or more
algal lineages containing uni‐ and multinucleate unicellular,
colonial, and multicellular species. Unfortunately, despite great
advances made in algal phylogenetics (e.g., Lewis and
McCourt 2004; Maistro et al. 2007; Cocquyt et al. 2010),
sufficiently detailed parsimony‐based cytological and morphological character state reconstructions of most algal clades are
unavailable. Indeed, detailed yet broad‐scale phylogenies based
on molecular data are rare and difficult to produce, particularly
for the algae, in part because the species used to construct algal
phylogenies are often limited to those that can be cultivated
under laboratory conditions (and may not be representative of
the larger taxa they purportedly represent). Another limitation
arises when one or more lineages within a phylogeny contain
species with diverse body plans, since this can obscure
inferences concerning which among alternative body plans
may have been the progenitor of more evolutionarily derived
variants (Fig. 5).
Nevertheless, it is possible to examine hypothetical character
polarities in light of the distribution of body plans on current
Fig. 4. A schematic for segregative cell division in which the
protoplasm of a multinucleate organism (left) simultaneously
separates into spherical portions (middle) that develop new cell
walls to form a multicellular (siphonocladous) body plan (right).
Among siphonocladean algae, the resulting cells remain
multinucleate.
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Vol. 15, No. 6, November–December 2013
Fig. 5. Possible difficulties in interpreting the character
polarities among variants of different plant body plans (see
insert to right) in a hypothetical plant phylogeny with three
lineages (A – D) when more than one body plan resides on
one or more basal lineages (lineages A – B). Arrows
indicate theoretically possible and competing body plan
transformation series the resolution of which requires
knowing the transformation series within lineages A
and B.
reconstructions of algal phylogeny. For example, among the red
algae, multinucleate cells occur in the multicellular Florideophyceae (e.g., Chondrus), but are unknown among species
assigned to the Bangiophyceae, which most authorities consider
to be ancient within this clade (Cole and Sheath 1990; Goff and
Coleman 1990; Graham et al. 2009). It is reasonable therefore to
suggest that the multinucleate condition is a derived condition
within the red algae. Likewise, using a phylogeny for the
Ulvophyceae based on seven nuclear genes, small subunit
nuclear ribosomal DNA, and two plastid markers, Cocquyt et al.
(2010) considered three hypotheses about the evolution of
multicellularity, among which one posits a “siphonous )
multicellular” transformation series (Cocquyt et al. 2010, their
Fig. 3). All three hypotheses share the assumption that the
ancestral ulvophyte was a unicellular, uninucleate organism
(represented by the prasinophytes), since “early‐branching
lineages are of this type” [of organism] (Cocquyt et al. 2010).
Another feature common to all three hypotheses is that
multicellularity evolved multiple times. Inspection of their
phylogeny shows that the unicellular, colonial, and multicellular
uninucleate body plans are all represented by species in
the Trebouxiophyceae, that the colonial multinucleate and the
siphonocladous variants are represented by species in the
Chlorophyceae, and that the siphonous body plan is represented
in the Trentepohliales and in other phyletically affiliated orders
(Fig. 6). This distribution of body plans is consistent with the
traditional “unicellular (uninucleate) ) colonial (uninucleate)
) multicellular (uninucleate)” evolutionary scenario for the
origin of multicellularity (Fig. 6). Indeed, Cocquyt et al. (2010)
concluded that the siphonous body plan is an evolutionarily
dead‐end body plan that was most likely derived from a
unicellular ancestor.
However, other algal phylogenies provide support for the
evolution of a “siphonous ) multicellular” transformation
series. For example, inspection of a phylogeny for the
Tribonematales (Xanthophyceae) constructed by Maistro et al.
(2007) based on the plastid genes rbcL and psaA shows that the
unicellular uninucleate and the colonial uninucleate body plans
(represented by Chlorellidium tetrabotrys and two species of
Heterococcus) occur in what authorities consider to be ancient
lineages, while the siphonous body plan (represented by
Asterosiphon dichotomus and Vaucheria terrestris) occurs in
species on shorter presumably more recent branches within this
phylogeny. The multicellular uninucleate body plan (represented
by species of Tribonema and Xanthonema) appears on even
shorter branches (Fig. 7). It is therefore not unreasonable to
Fig. 6. Multinucleate body plans (see insert) mapped onto a redacted phylogeny of the Ulvophyceae (based on the molecular phylogeny of
Cocquyt et al. 2010) and the charophycean‐embryophyte (streptophyte) lineages within the chlorobionta (green algae). Note that all of the
body plans known for each branch of this clade are mapped regardless of the particular species used to construct this phylogeny because there is
no a priori assumption that the particular species used to construct the phylogeny are representative of their higher taxon. Theuninucleate
unicellular body plan (represented by the prasinophytes for the entire clade and particularly by the prasinophycean alga Mesostigma for the
streptophytes) is represented by species assigned to the earliest divergent lineages in both portions of this cladogram.
Niklas et al.
The evo‐devo of multinucleate cells, tissues, and organisms, and an alternative
471
Fig. 7. Multinucleate body plans (see insert) mapped
onto a redacted phylogeny of the Tribonematales (based
on the molecular phylogeny of Maistro et al. 2007) in the
Xanthophyceae. Note that all of the body plans known
for each branch of this clade are mapped regardless of
the particular species used to construct the phylogeny
because there is no a priori assumption that the
particular species used are representative of their higher
taxon. The uninucleate unicellular body plan and the
uninucleate colonial body plan (represented by Chlorellidium and species of Heterococcus, respectively)
occur at the bottom of the cladogram. The siphonous
body plan maps on a branch represented by Asterosiphon and Vaucheria that precedes the earliest appearance of the multicellular uninucleate body plan
represented by species of Xanthonema.
suggest that, within the Tribonematales, the “unicellular or
colonial (uninucleate) ) siphonous” transformation series
evolved at least once. This inference is strengthened by the
occurrence of siphonocladous species that achieve their
multicellular condition ontogenetically by means of segregrative
cell division.
THE MULTINUCLEATE CONDITION: HOW AND
WHY
The evolutionary appearance and diversity of the multinucleate
condition in unrelated plant clades raises a number of important
questions, not the least of which is how and why it
evolved multiple times, and whether it is an ancient or derived
condition.
There are two basic ways a multinucleate plant cell can be
formed under normal physiological conditions: (1) as a result of
repeated mitotic nuclear division unattended by cytokinesis
(e.g., during the formation of the Plasmodium schizont stage,
non‐articulated laticifers, endosperm, and Chara internodal
cells), or (2) by the fusion or dissolution of plasma membranes
(e.g., during the formation of syncytia as in the tapetum, the
megagametophytic storage cells of the conifer Pseudotsuga
menziesii, and the development of mammalian musculoskeletal
system). The mechanism responsible for the first of these two
routes to the multinucleate condition appears to differ among
clades (Mine et al. 2008), although some basic commonalities
exist (Baluška et al. 2012). Molecular studies of cytokinesis in
the model embryophyte Arabidopsis reveal a number of genetic
mutations that may account for this form of defective
cytokinesis. For example, the gene products KEULE and
KNOLLE mediate membrane fusion at the cell plate and keule
and knolle mutants are characteristically multinucleate
(reviewed by Assaad 2001). In addition, some of the cells in
keule mutants have incomplete cell wall extensions (Assaad et al.
2001; Lukowitz et al. 2001) that are similar in appearance to the
trabeculae that extend into the cytoplasm of the siphonous green
algae Caulerpa (Fagerberg et al. 2010). Among these and other
mutants, the ontogeny of multinucleate phenotypes indicates that
nuclear division can be completed even when cytokinesis is
incomplete, whereas cytokinesis can only be initiated once the
nuclear cycle is complete (for a review, see Nacry et al. 2000).
However, the mechanisms of cytokinesis are not likely to be
homologous among the different plant clades (see for example
McDonald and Pickett‐Heaps 1976; McNaughton and
Goff 1990; Pickett‐Heaps et al. 1999). For example, embryophyte cytokinesis involves a phragmoplast composed of microtubules and the formation of a new cell plate that starts at the
center of the cell and proceeds centrifugally outward toward the
parental cell wall (phragmoplastic cytokinesis) (Pickett‐Heaps
et al. 1999), a process that involves a complex sequence of
cytoskeletal and membrane dynamics with a vast array of
molecular players (Dhonukske et al. 2006; McMichael and
Bednarek 2013). With the exception of the charophycean algae
and the Trentepohliales, cytokinesis among the various algal
lineages is accomplished by a diaphragm‐like furrowing of the
plasma membrane and associated cell wall layers that develops
as a centripetally growing septum (phycoplastic cytokinesis)
(Graham 1996). A hybrid of these two forms of cytokinesis is
reported for the charophycean (Zygnematales) alga Spirogyra in
which a diaphragm‐like furrow organizes the centripetal in‐
growth of a furrow and a phragmoplastic‐like array of
microtubules is associated with the centrifugal development of
cell plate vesicles (Sawitzky and Grolig 2001). Animal
cytokinesis is based on an actomyosin‐containing contractile
ring and begins at the cell perimeter as a cleavage furrow, which
is drawn toward the derivative nuclei into the dividing cytoplasm
(centripetal cytokinesis). Despite these cytological differences,
cytokinesis appears to involve the participation of the endosomal
protein ESCRT III in the final act of cytokinetic membrane
constriction across the majority of eukaryotes, since endocytosis
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Vol. 15, No. 6, November–December 2013
fails in ESCRT III mutants (Carlton and Martin‐Serrano
2007, 2009).
As to why the multinucleate condition evolved, there are
obvious disadvantages as well as advantages to being
coenocytic. On the one hand, the absence of cross walls allows
for the systemic spread of a pathogen once the cell wall is
breached. It is not surprising therefore that at least six different
rapid‐wound response mechanisms have evolved among the
siphonous algae (Menzel 1988). Yet another disadvantage of the
siphonous body emerges for holocarpic organisms (i.e., those
that completely evacuate their cytoplasm in the act of
reproduction), since the adult must sacrifice itself to reproduce.
On the other hand, there are potential advantages of having
multinucleate cells or a siphonous body plan, e.g., (1) rapid
intracellular mass‐energy exchange when coupled with cytoplasm streaming, (2) a buffer against deleterious mutations as a
consequence of multiple genome copies (or, conversely, a
platform to segregate defective nuclei during the formation of
uninucleate gametes or multinucleate asexual propagules),
(3) higher metabolic and growth rates due to amplified
chromosomal copies of ribosomal RNA cistrons (as an analog
of one of the possible effects of endoreduplication or
polyploidy), and (4) a multinucleate (siphonous) cell has the
potential to occupy diverse microenvironments when coupled
with indeterminate growth (which, for a tubular organism with a
large vacuole, can confer the additional advantage of increasing
the effective surface area with respect to volume for mass and
energy exchange).
Naturally, the null hypothesis is that multinucleate cells,
tissues, and organisms are subject to neutral selection and reflect
homoplasy rather than convergent adaptive evolution. Major
evolutionary innovations are not likely to be retained within a
lineage if they are incompatible with successful reproduction.
However, it is not always the case that every transition requires a
large or even measurable advantage (Grosberg and
Strathmann 2007; Anderson et al. 2011), nor is it the case that
phenotypic responses to selection are invariably in the direction
of an adaptive advantage (Bonduriansky and Day 2009; Gray
et al. 2010; Lynch 2012).
A DIFFERENT EVOLUTIONARY SCENARIO FOR
MULTICELLULARITY?
We have shown that it is theoretically possible for a multicellular
organism to evolve directly from a siphonous/coenocytic
progenitor via a developmental process analogous to segregative
cell division (see Fig. 4). Here, we argue that such a progenitor is
an integrated phenotype that has already passed through both the
alignment‐of‐fitness phase and the export‐of‐fitness phase
(processes reviewed by Folse and Roughgarden 2010; see also
Niklas and Newman 2013), while bypassing the colonial body
plan, which is traditionally postulated in the unicellular to
multicellular transformation series (see also Niklas and
Newman 2013). All that is required to achieve multicellularity
in this scenario is the acquisition of the capacity to partition
cytoplasm into individual cells.
All plant life cycles, including those of all known siphonous
algae, have at least one unicellular “bottleneck” that establishes
genomic uniformity among subsequently produced nuclei. The
bottleneck can take the form of a zygote, an asexual uninucleate
propagule, or an asexual propagule containing genetically
identical nuclei (Niklas and Newman 2013). Further, no
siphonous plant is known to propagate as a result of the somatic
fusion of genetically dissimilar individuals, and most are
haploid. Thus, baring extensive somatic mutations, the nuclei
in a siphonous alga are as genetically similar as the nuclei in
multicellular organism. Consequently, every siphonous organism has passed though an alignment‐of‐fitness phase as a
consequence of its sexual or asexual reproductive cycle.
Traditionally, the export‐of‐fitness phase is said to occur
when cells evolve fitness‐specific tasks to give rise to a
multicellular entity that reproduces similar entities with a
heritable fitness (Folse and Roughgarden 2010). The appearance
of a division of labor between germ‐ and soma‐functionalities
provides evidence that this evolutionary phase has been attained
(Buss 1987). However, obligate sexual reproduction is not
required to override the conflict between the individual organism
and its constituent cells (Michod 1997; Folse and Roughgarden
2010), or to be more precise in the context of this discussion, the
individual organism and its constituent nuclei. All that is
theoretically required is the evolution of one or more multistable
gene regulatory networks (MGRP) capable of producing
different cellular/nuclear functionalities (Laurent and
Kellershohn 1999; Libby and Rainey 2013), e.g., an organism
containing nuclei capable of existing in multiple states of gene
expression. MGRP occur in unicellular bacteria as well as in
uninucleate algae, yeast, and amoebae exhibiting alternative
stable states of gene activity during their life cycles. Further,
mathematical models indicate that cellular/nuclear differentiation can emerge even among genetically identical adjoining
cells as a response to poor compatibility among competing
physiological processes (Ispolatov et al. 2012). Arguably, a
minimum number of different cellular/nuclear functionalities is
required before it becomes necessary to establish methods to
control functional differentiation (Arnellos et al. 2013). However, once again, this condition is achieved by a reproductively
viable siphonous organism.
We therefore argue that the multinucleate unicellular
coenocyte possesses all of the preconditions required for the
evolution of multicellularity in that it has achieved a level of
cooperation among nuclei capable of differential genomic
expression that acheieved delegated functionalities, albeit within
a shared cytoplasm. All that is required is the evolution of the
capacity for cellularization of a siphonous progenitor. In this
context, three features evident among multinucleate plants are
Niklas et al.
The evo‐devo of multinucleate cells, tissues, and organisms, and an alternative
relevant: (1) many siphonous algae achieve elaborate vegetative
morphological features as a result of regional differential
genomic expression patterns (e.g., the ulvophycean algae
Caulerpa; see Fig. 1), (2) many also form temporary cell walls
to sequester “germ” from “somatic” nuclei during their asexual
or sexual life cycles (e.g., the ulvophycean algae Acetabularia),
and (3), as previously noted, siphonocladous algae begin their
life cycles as coenocytes, but subsequently become multicellular
by means of segregative cell division.
The transition to multicellularity via a unicellular multinucleate progenitor has been proposed for account for aspects of
animal evolution (see Hadzi 1953; Hanson 1977), but it is
incompatible with our current understanding of metazoan
phylogenetics. Nevertheless, we believe that this scenario is
consistent with certain aspects of plant evolution. This
proposition can be tested experimentally by detailed analyses
of the phyletic relationships within algal lineages containing
uni‐ and multinucleate cells and siphonous and siphonocladous
organisms. Such analyses require resolution of character state
polarities at the ordinal, familial, and perhaps at the generic level.
However, regardless of its frequency of occurrence or the exact
mechanisms by which it is achieved, the scenario of a unicellular
multinucleate cell evolving into a multicellular organism
represents a theoretically viable hypothesis that requires
consideration when discussing the origins of multicellularity.
Acknowledgements
The authors thank Dr. Linda E. Graham (University of Wisconsin,
Madison), Drs. Dominick J. Paolillo Jr. and Thomas Owens (Cornell
University), and two anonymous reviewers for insightful suggestions
and comments. Funding from the College of Agriculture and Life
Sciences (Cornell University) is gratefully acknowledged. This paper is
dedicated to Dr. Linda E. Graham for her many contributions to
phycology and our understanding of streptophyte evolution.
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