Integrative and Comparative Biology, volume 50, number 5, pp. 734–743
doi:10.1093/icb/icq096
SYMPOSIUM
The Invention of the Pilidium Larva in an Otherwise Perfectly
Good Spiralian Phylum Nemertea
Svetlana A. Maslakova1
Oregon Institute of Marine Biology, University of Oregon, Charleston, OR 97420, USA
From the symposium ‘‘Spiralian Development: Conservation and Innovation’’ presented at the annual meeting of the
Society for Integrative and Comparative Biology, January 3–7, 2010, at Seattle, Washington.
1
E-mail: [email protected]
Synopsis One of the most remarkable larval types among spiralians, and invertebrates in general, is the planktotrophic
pilidium. The pilidium is found in a single clade of nemerteans, called the Pilidiophora, and appears to be an innovation
of this group. All other nemerteans have either planktotrophic or lecithotrophic juvenile-like planuliform larvae or have
direct development. The invention of the pilidium larva is associated with the formation of an extensive blastocoel that
supports the delicate larval frame and elaborate ciliary band. Perhaps the most striking characteristic of the pilidium is
the way the juvenile worm develops inside the larva from a series of isolated rudiments, called the imaginal discs. The
paired cephalic discs, cerebral organ discs, and trunk discs originate as invaginations of larval epidermis and subsequently
grow and fuse around the larval gut to form the juvenile. The fully formed juvenile ruptures the larval body and, more
often than not, devours the larva during catastrophic metamorphosis. This review is an attempt to examine the pilidium
in the context of recent data on development of non-pilidiophoran nemerteans, and speculate about the evolution of
pilidial larval development. The author emphasizes the difference between the planuliform larvae of Palaeonemerteans
and Hoplonemerteans, and suggest a new name for the hoplonemertean larvae—the decidula.
Nemerteans are good spiralians
The nemerteans, commonly referred to as ribbon
worms, constitute a separate phylum of marine invertebrates with 1275 formally recognized species
(Kajihara et al. 2008). The vast majority of nemerteans are benthic marine predators, which attack their
prey using a unique eversible proboscis. The proboscis is housed dorsal to the gut in a fluid-filled cavity,
called the rhynchocoel. Other characteristics of
nemerteans include a brain that encircles the rhynchocoel, instead of the foregut, as in canonical protostome invertebrates, and the two main lateral blood
vessels (compared to the dorsal and ventral).
Historically grouped with flatworms as acoelomates,
nemerteans are now widely considered to be closely
related to coelomate protostomes, such as annelids
and mollusks (Turbeville 2002; Jenner 2004). The
coelomate affinities of nemerteans were initially suggested by the characters of microscopic anatomy,
e.g., the presence of continuous endothelial lining
in the rhynchocoel and the two main lateral blood
vessels (which are thus homologized with the coelomic cavities), gliointerstitial system (Turbeville and
Ruppert 1985; Turbeville 1991), and schizocoelous
formation of nemertean blood vessels (Turbeville
1986). Additional support comes from many independent molecular and total-evidence phylogenetic
studies (Turbeville et al. 1992; Winnepenninckx
et al. 1995; Giribet et al. 2000; Peterson and
Eernissee 2001).
Recent phylogenies based on mitochondrial gene
arrangement and EST data sets firmly place nemerteans in the Lophotrochozoa (arguably synonymous
with Spiralia) and suggest close ties to coelomate
taxa, although the nemertean sister group is yet to
be identified (Turbeville and Smith 2007; Dunn et al.
2008; Bourlat et al. 2008, Chen et al. 2009,
Podsiadlowski et al. 2009). Nemerteans display stereotypical equal spiral cleavage (Delsman 1915;
Hammarsten 1918; Maslakova et al. 2004a) and
a large degree of conservation of classical spiralian
cell fates, including ectomesoderm derived from
Advanced Access publication July 19, 2010
ß The Author 2010. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
735
Larval development in nemerteans
3a and 3b cells, and endomesoderm derived from the
4d cell (Henry and Martindale 1998).
Aside from the spiral cleavage itself, many spiralians posses a trochophore larva, in the sense of the
word used by Rouse (1999), and broadly defined as a
larva with a preoral ring of large ciliated cells, called
the prototroch. The prototroch is primarily used for
larval locomotion, and sometimes for feeding.
Critically, the prototroch arises from particular embryonic progenitor cells in a spiralian embryo, called
the trochoblasts. Many spiralians have variously
modified larvae that deviate from the generalized
trochophore body plan, e.g., molluscan veligers, the
sipunculid pelagosphaera, uniformly ciliated larvae,
endolarvae, or the mitraria larva of annelids.
However, many of these still go through a brief
trochophore-like stage. At the very least, other representatives of these phyla possess trochophore
larvae. Until recently, however, no nemertean was
known to possess a trochophore larva, and it was
not clear how to relate nemertean larvae to the classical spiralian trochophores. Descriptive and
cell-lineage studies in the palaeonemertean
Carinoma, however, revealed clear vestiges of the
trochophore (Maslakova et al 2004a, 2004b). This
means that the origin of the pilidium larva should
be interpreted in the context of classical spiralian
developmental program, including the stereotypic
behavior of the trochoblast lineage.
Larval diversity in nemerteans
Nemertean larvae can be classified by shape and development into pilidium larvae (Fig. 1A) and planuliform larvae (Fig. 1B). The two correspond to
the traditionally recognized categories of ‘‘indirect’’
(pilidial) and ‘‘direct’’ (non-pilidial) development in
nemerteans (Henry and Martindale 1997; Norenburg
and Stricker 2002). The terms ‘‘direct’’ and ‘‘indirect’’ are somewhat misleading because many of the
‘‘direct-developing’’ nemerteans nevertheless have
long-lived feeding planktonic juvenile-like larvae.
‘‘Direct’’ in this case refers to a developmental trajectory without a distinct larval body plan, or an
overt metamorphosis, rather then to the lack of a
swimming or feeding planktonic stage in the life
cycle.
The long-lived transparent planktotrophic pilidium
larva is found only in the monophyletic clade
Pilidiophora (Fig. 2), which comprises the Heteronemertea and the formerly palaeonemertean family
Hubrechtidae (Thollesson and Norenburg 2003),
with a total of 450 species (Kajihara et al. 2008).
Fig. 1 The two easily distinguished types of nemertean larvae: the pilidium and the planuliform larva. Apical plate and tuft (ap), which
identifies larval anterior end, is up. (A) Pilidium larva of the pilidiophoran Lineus flavescens with a fully developed juvenile inside. The
antero-posterior (AP) axis of the larva is nearly perpendicular to that of the juvenile. Juvenile anterior (to the left) is identified by the
two eye spots. The pilidial ciliated band, which spans the lappets, is marked by the dotted line. Scale 200 mm. (B) Uniformly ciliated
planuliform larva of the hoplonemertean Pantinonemertes californiensis. The AP axis of the planuliform larva coincides with that of the
adult. Scale 55 mm.
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Fig. 2 The distribution of the major larval types (the pilidium and
the planuliform larva) across nemertean taxa. Phylogeny modified
after Thollesson and Norenburg (2003). The only group with
pilidium larva is the Pilidiophora (light gray box), which includes
the traditional order Heteronemertea and the formerly
palaeonemertean family Hubrechtidae. The traditional order
Hoplonemertea is monophyletic, has planuliform larvae, and is
the sister clade to the Pilidiophora. The traditional order
Palaeonemertea (dark gray box) forms a basal paraphyletic
assemblage, and has planuliform larvae.
The pilidium stands out because of its characteristic
morphology, and the unusual development of the
juvenile via imaginal discs (Salensky 1912; Dawydoff
1940; S. A. Maslakova and L. S. Hiebert, manuscript
in preparation). Its development culminates in dramatic metamorphosis, in which the juvenile emerges
from the larva by rupturing the larval epidermis,
and, in most cases, devours the larval body (Cantell
1966a, 1969; Maslakova and Hiebert, manuscript in
preparation). Pilidial development is so unlike any
other, that it is difficult to relate it to the development of other spiralians.
Planuliform larvae, found in the non-pilidiophoran
nemerteans, the monophyletic Hoplonemertea, and
the basal paraphyletic Palaeonemertea, are uniformly
ciliated, non-transparent, and resemble cnidarian
planulae, hence the name. In contrast to the pilidium, the juvenile body is largely prefigured by the
larva. Development of a planuliform larva is gradual,
and does not involve a conspicuous metamorphosis,
i.e., a dramatic change in body plan between the
larval and the juvenile stages. Although all nemertean
planuliform larvae look superficially similar to each
other, and have been traditionally lumped together
as ‘‘direct developers’’, it is clearly a heterogeneous
group (Maslakova and von Döhren 2009).
The most obvious, but frequently overlooked, distinction between the palaeonemertean and the
hoplonemertean planuliform larvae lies in their
ecology. Most of the studied palaeonemertean
S. A. Maslakova
planuliform larvae are planktotrophic (Smith 1935;
Iwata 1960; Jägersten 1972; Norenburg and Stricker
2002; Maslakova et al. 2004a, 2004b; S. A.
Maslakova, personal observations). Relatively small
eggs (100 mm) are free-spawned and, within a few
days, develop into simple planula-like larvae with a
conspicuous mouth (derived directly from the blastopore), which leads into a blind gut with a distinct
lumen. These larvae apparently require food to grow
and develop juvenile structures such as the proboscis,
the cerebral ganglia, and the lateral nerve cords.
Unlike the pilidium larvae, which are equipped
with a ciliated band with which they can capture
unicellular algae, palaeonemertean larvae do not
seem to be able to collect microscopic particles.
Laboratory observations show that they are capable
of swallowing larger particles, including isolated
sea urchin blastomeres and bivalve veligers
(S. A. Maslakova, personal observations), dinoflagellate-size microplankton (Norenburg and Stricker
2002), and even pilidium larvae (Jägersten 1972).
However, no one to this day has identified the preferred food for any given species, or succeeded in
rearing a palaeonemertean larva to the point of developing juvenile structures. Advanced stages, which
are clearly feeding and growing, are found in plankton samples (Jägersten 1972; Norenburg and Stricker
2002; S. A. Maslakova, personal observations).
In contrast to palaeonemerteans, the hoplonemerteans have lecithotrophic (non-feeding) development
(Norenburg and Stricker 2002). In many studied
hoplonemertean species that free-spawn small eggs
(100–200 mm) the larva develops the proboscis
and the juvenile nervous system without feeding.
This is correlated with a rather complex morphogenesis of the hoplonemertean digestive system. The
blastopore closes, and the mouth and foregut develop later via a secondary invagination, which eventually fuses with the midgut (Friedrich 1979;
Maslakova and von Döhren 2009). Thus, unlike the
palaeonemertean larvae, the hoplonemertean larvae
are simply not equipped to feed. In some species,
settlement is observed soon after the juvenile structures, which include the proboscis, the brain, and the
complete gut develop (Maslakova and von Döhren
2009). In others, larvae likely remain in the plankton
as feeding juveniles (S. A. Maslakova, personal observations). Many hoplonemertean species with
larger eggs (200–500 mm) deposit egg cocoons, and
the development is entirely encapsulated, i.e., a complete juvenile emerges from the egg envelopes
(Hickman 1963; Norenburg 1986, Maslakova and
Malakhov 1999; Maslakova and von Döhren 2009).
A few hoplonemertean species bear live young
Larval development in nemerteans
(Coe 1904; Norenburg 1986; Maslakova and
Norenburg 2008).
Several pilidiophoran species are known to exhibit
encapsulated development (e.g., see Schmidt 1964),
or possess an ovoid non-feeding uniformly ciliated
planktonic larva that superficially resembles planuliform larvae of hoplonemerteans and palaeonemerteans (Iwata 1958; Fig. 3D). Furthermore, Schwartz
and Norenburg (2005) described a transverse equatorial ciliary band in an otherwise planula-like larva
of the pilidiophoran Micrura rubramaculosa.
Nevertheless, in each case the juvenile develops via
imaginal discs, indicating that these larvae and encapsulated pilidiophoran embryos (called Desor’s
and Schmidt’s larvae) represent secondary modifications of pilidial development.
Pilidial development
A typical pilidium larva looks like a deerstalker cap
(the kind worn by Sherlock Holmes)—with ear flaps
pulled down (Figs. 1A, 3A and 5A). The external
shape of pilidium varies by species (Dawydoff 1940;
Cantell 1969; Norenburg and Stricker 2002; Lacalli
2005; Fig. 3), but almost uniformly these are transparent larvae with a blind gut and an unusually extensive blastocoel supporting a delicate larval muscle
frame (Fig. 5A). The pilidium is equipped with a
long-apical tuft, which can be partially retracted
into the dome by a special muscle. The mouth is
located inside the cap, between the ear flaps. The
surface of the dome is uniformly covered by short
cilia. A band of longer cilia spans the margins of
larval lappets (Figs. 1A, 3A and B) and produces
737
the feeding current. The pilidium spends weeks to
months in the plankton feeding on microscopic
particles.
Analysis of lineage contributions to the larval body
of the pilidiophoran Cerebratulus lacteus (Henry and
Martindale 1998) revealed both conserved and novel
features. Among the classical spiralian lineage traits is
the dual source of mesoderm. Pilidial larval muscles
are derived from the 3a and 3b cells, and the rest of
the mesoderm (and a portion of the gut) is derived
from the 4d cell, the spiralian mesentoblast. Among
the unusual characteristics is the relatively large contribution of the first quartet micromeres (1q) to the
larval body—the entire external surface of the pilidium is produced by the first-quartet micromeres.
Because the pilidium is derived within nemerteans,
and larvae of the basal members of the phylum are
uniformly ciliated (i.e., lack distinct-ciliated bands),
the ciliated band in the pilidium larva is not homologous to the prototroch of the trochophore larvae of
other spiralians as a ring of differentially ciliated cells
employed in locomotion and feeding. Unlike the
classical spiralian prototroch which is composed of
24–40 relatively large cleavage-arrested cells (Damen
and Dictus 1994) derived as a rule from the first and
second quartet micromeres (Henry et al. 2007), the
pilidial ciliated band consists of numerous, perhaps
hundreds, of very small ciliated cells and includes a
contribution of the first-quartet, second-quartet, and
also the third-quartet micromeres 3c and 3d (Henry
and Martindale 1998). The sheer number and size of
cells in the pilidial ciliated band suggests that even
though they are partially derived from the spiralian
Fig. 3 The diversity of form among pilidium larvae. (A) Pilidium of Micrura alaskensis with three pairs of imaginal discs—cephalic discs
(cd), trunk discs (td), and cerebral organ discs (cod). Only one of each pair is in focus. The large dark shape (magenta in the online
colored version) inside is the gut. Scale 100 mm. (B) A pilidium larva of auriculatum type from Coos Bay, OR plankton, which, according
to 16S rDNA sequence data, belongs to the hubrechtid pilidiophoran Hubrechtella juliae (S. A. Maslakova, unpublished data). Scale
100 mm. (C) A pilidium larva of recurvum type from Coos Bay, OR plankton, which belongs to an unidentified pilidiophoran species.
Scale 100 mm. (D) A uniformly ciliated planula-like larva of an unidentified pilidiophoran, from Coos Bay, OR plankton. Scale 50 mm.
738
trochoblast lineage, they must escape the cleavage
arrest and continue to divide to form the elaborated
and ever expanding ciliated band of the pilidium
larva. Although this behavior of the trochoblast
lineage is likely a derived condition for nemerteans
(see below), it is certainly not unique. Prototrochs of
several other kinds of spiralian larvae seem to have
converged upon the same solution to the problem of
making an extensive larval ciliated band, e.g., many
gastropod and bivalve veligers, the mitraria larva of
the polychaete Owenia (Smart and von Dassow
2009), and the endolarva of the polychaete
Polygordius (Woltereck 1902).
The most remarkable thing about the pilidium is
the development of the juvenile inside the larva from
a series of isolated rudiments, called imaginal discs.
The larval body plan is carved out according to the
spiralian cell lineage, but formation of the juvenile is
largely disconnected from larval development. This
type of development is unique among spiralians.
Although, of course, the pilidial imaginal discs are
not homologous to the identically-named rudiments
in the development of holometabolous insects such
as Drosophila, it is not inconceivable that similar developmental processes and mechanistic solutions
are utilized in both groups to address analogous
challenges.
A typical pilidium has three pairs of imaginal
discs, which develop as invaginations of larval epidermis (Fig. 3A). The cephalic imaginal discs, which
give rise to the head of the juvenile, appear first. The
second pair is the trunk discs, which form the major
portion of the juvenile body. The third pair is the
cerebral organ discs, which give rise to a pair of
chemosensory organs (unique to nemerteans) in
the head of the juvenile (Salensky 1912; S. A.
Maslakova and L. S. Hiebert, manuscript in preparation). The cephalic discs in the pilidium larva are
derived from the first quartet micromeres (Henry
and Martindale 1998). The formation of the other
imaginal discs is nutrition-dependent and takes a
much longer time (weeks) than the injected fluorescent dextrans can be detected. Until more persistent
lineage markers are developed for nemerteans, one
can only guess which lineages give rise to the other
imaginal discs based on their position in the larva.
Both the trunk discs and the cerebral organ discs
invaginate below the ciliated band (Salensky 1912;
Maslakova and Hiebert, manuscript in preparation),
which suggests that they are derived from the second
or third micromere quartets.
Although many textbooks suggest that all discs
form as invaginations, this is incorrect. There
are at least two additional juvenile rudiments,
S. A. Maslakova
which do not develop as invaginations of larval
epidermis, but instead appear to be mesenchymal
in origin (S. A. Maslakova and L. S. Hiebert, manuscript in preparation). Both are unpaired and located
in the plane of bilateral symmetry. The proboscis
rudiment is first evident as a small cluster of mesenchymal cells between the cephalic discs and larval
epidermis. It fuses with the cephalic discs, and the
proboscis forms at the junction. Since the proboscis
of the adult worm is clearly an epithelial derivative,
while the rhynchocoel (a coelom-like sack which
houses the proboscis) is likely of mesenchymal
origin, one might hypothesize that the unpaired mesenchymal rudiment gives rise to the rhynchocoel,
and instructs the tissue of the cephalic discs to
form the proboscis proper. The other mesenchymal
rudiment is the so-called dorsal disc, which appears
between the gut and the larval epidermis and later
fuses with the trunk discs (Salensky 1912; S. A.
Maslakova and L. S. Hiebert, manuscript in preparation). The lineage of these two unpaired mesenchymal rudiments is unknown. However, it is perhaps
not unreasonable to suggest that they are derived
from the progeny of the spiralian mesentoblast
(4d), which produces scattered populations of
mesenchymal cells in the blastocoel of a young
pilidium larva (Henry and Martindale 1998).
Imaginal discs fuse with each other to form the
juvenile worm around the larval gut. The body plan
of the planktonic pilidium larva and the benthic juvenile are dramatically different, and the transition
between the two stages is rapid (minutes) and catastrophic. Because the larva and the juvenile share the
gut, they are physically connected around the mouth.
During metamorphosis, the juvenile ruptures the
larval epidermis, and emerges from the larva while
swallowing the larval tissues, until the entire pilidium
is ingested (Cantell 1966a, 1969; Maslakova and
Hiebert, manuscript in preparation).
The pilidium represents a striking example of spatial and temporal segregation of larval and juvenile
morphogenesis. Development of the larval body is
completed long before any but the first pair of juvenile rudiments appears. The formation and growth of
imaginal discs is dependent on nutrient uptake (feeding) by the larva. In the absence of food, the larva
can survive for many weeks, without developing juvenile structures (S. A. Maslakova, personal observations). Related to this is the apparent dissociation of
the larval and juvenile body axes. In all planuliform
larvae, the larval and juvenile body axes are one and
the same (Fig. 4A). In a typical pilidium, in contrast,
the antero-posterior (AP) axis of the juvenile is perpendicular to the AP axis of the larva (Figs. 1A and
739
Larval development in nemerteans
Comparative embryonic and larval development
in nemerteans
Fig. 4 Relative orientation of larval (black arrows) and juvenile
(gray arrows) antero-posterior (AP) in a planuliform larva (A)
and different types of pilidia (B–D). (A) Planuliform larva of
non-pilidiophoran nemerteans prefigures the adult, including the
body axes. (B) In a typical pilidium, the larval AP axis is nearly
perpendicular to that of the juvenile. (C) In pilidium larvae of
recurvum type, the direction of the larval and the juvenile AP axes
coincide. (D) In the pilidiophoran Micrura akkeshiensis, which has
modified pilidial development (Iwata 1958), the direction of the
juvenile AP axis is reversed compared to the larval AP axis.
4B). In the types of larvae called Pilidium recurvum
(Dawydoff 1940; S. A. Maslakova, personal observations) and Pilidium recurvatum (Cantell 1966b), as
well as in the recently described larva of M. rubramaculosa (Schwartz and Norenburg 2005) the AP
axis of the juvenile coincides with that of the larva
(Fig. 4C), while in Micrura akkeshiensis (Iwata 1958),
the AP axes of the larva and the juvenile are reversed
(Fig. 4D). This diversity suggests that the evolution
of pilidial development was accompanied by the dissociation of the mechanisms responsible for patterning the larval and the juvenile body axes.
An incidental observation of abnormal development in one cohort of pilidia of M. alaskensis
(S. A. Maslakova, personal observations) suggests
that the individual juvenile rudiments develop largely
independently from each other. While the larvae
looked normal and were actively feeding, a large proportion of pilidia in this culture exhibited various
abnormalities of the imaginal discs. For example,
some were missing one or both of the cephalic
discs, one or both of the cerebral organ discs, or
the proboscis rudiment, or failed to fuse the discs
properly. Remarkably, the absence of one or several
rudiments did not visibly affect the development of
other rudiments. This observation suggests that individual discs must be more than simply bags of proliferating cells; they are capable of extensive pattern
formation and differentiation even before the whole
body is assembled.
Hyman (1951, p. 514) wrote that ‘‘. . . the chief difference between the direct and the larval [pilidial]
types of development [in nemerteans] consists in
the replacement in the latter of the larval ectoderm
by the invaginated ectoderm. . .’’. She was referring
to the origin of the definitive epidermis from
the invaginating imaginal discs, and the pilidial
metamorphosis, in which the pilidial body is consumed by the emerging juvenile. However, nonpilidiophoran nemerteans may have an equivalent
developmental process in which the larval epidermis
is replaced by the definitive epidermis.
Several species of hoplonemerteans with planktonic larvae or encapsulated development have been reported to possess a transitory embryonic or
larval epidermis, which is replaced by the definitive
epidermis during development (Delsman 1915;
Hammarsten 1918; Reinhardt 1941; Hickman 1963;
Maslakova and Malakhov 1999)—a process possibly
homologous to pilidial metamorphosis (Jägersten
1972; Maslakova and Malakhov 1999). Recent studies
of hoplonemertean larval development added more
species to the list, suggesting that presence of the
transitory epidermis, which is shed or resorbed
during development, is likely the rule for hoplonemerteans (Maslakova and von Döhren 2009; Hiebert
et al. 2010).
One earlier study showed that the larva of the
palaeonemertean Tubulanus punctatus may also possess some sort of a transitory epidermis (Iwata 1960).
Although this report has never been independently
confirmed, it led to the hypothesis that the metamorphic type of life history, as found in pilidiophorans, may be ancestral for the phylum (Jägersten 1972;
Maslakova and Malakhov 1999). With the idea of
testing this hypothesis, the author set out to examine
the larval development of the palaeonemertean
Carinoma tremaphoros, looking for transitory larval
epidermis, and a possible homology to pilidial metamorphosis. Instead, we discovered, by tracing the
epidermal cell outlines and the cell lineage, that
what appeared at first as a transitory larval epidermis, was in fact, a vestigial prototroch, composed of
40 cells derived from the classical spiralian trochoblast lineage (Maslakova et al. 2004a, 2004b). This
prototroch is inconspicuous because Carinoma’s planuliform larva is uniformly ciliated, but the cells of
the prototroch are distinguished by their large size,
arrangement in a discrete pre-oral ring, cleavage
arrest, and ultimate degenerative fate (Fig. 5C). The
presence of a ‘‘hidden trochophore’’ in a basal
740
S. A. Maslakova
Fig. 5 The three representative types of nemertean larvae. All three images are confocal projections of larvae stained with fluorescent
phalloidin to show the muscles (A) and the outlines of surface cells (B and C). (A) Side view of a 4-week-old pilidium of the
pilidiophoran M. alaskensis. Brightly labeled apical plate is on the upper right. Epithelial cell microvilli in the gut (to the right) are also
brightly labeled. A prominent muscular strand underlies the ciliated band that spans the lappets. Microvillar collars of presumed sensory
cells punctuate the larval ciliated band. Scale 50 mm. (B) Ventral view of a 5-day-old decidula of the hoplonemertean Paranemertes
peregrina. Scale 50 mm. Note the small cells of the definitive epidermis intercalated between the larger cells of the transitory epidermis.
(C) Ventro-lateral view of a 30-h-old hidden trochophore of the palaeonemertean Carinoma tremaphoros. The oblique subequatorial
band of brightly labeled large cells is the prototroch. Epidermal cells in the pre-trochal (upper right) and post-trochal (lower left)
regions, which form the definitive epidermis, are conspicuously smaller. Reproduced with permission from Maslakova et al. (2004b;
Fig. 4A). Scale 25 mm.
nemertean supports the notion that pilidial development is derived in nemerteans, and provides a useful
reference point when comparing nemertean larvae to
the larvae of other spiralians.
It remains to be tested (e.g., by cell lineage
analysis) whether the transitory epidermis of the
hoplonemertean planuliform larvae is homologous
to the prototroch in Carinoma and other spiralians,
or whether it may be homologous to the pilidial
larval body. Morphologically, this transitory or ‘‘deciduous’’ epidermis is different from the vestigial
prototroch in Carinoma in several ways. First of all,
more cells (80–90) are participating in the formation
of the hoplonemertean transitory epidermis, than
in the hidden prototroch of Carinoma. Second, the
cells of the hoplonemertean transitory epidermis
become separated from each other by the intercalating cells of the definitive epidermis (Fig. 5B), as
opposed to histolysing as a contiguous domain (Fig.
5C) in Carinoma (Maslakova et al. 2004a, 2004b;
Maslakova and von Döhren 2009; Hiebert et al.
2010). To emphasize the difference between the
palaeonemertean and the hoplonemertean larvae,
the author proposes a new name for the hoplonemertean planuliform larva—the decidula (Fig. 5B), from
the Latin deciduus, meaning ‘‘to shed’’.
The most characteristic feature of pilidial development, the imaginal discs, might also have a counterpart in planuliform development. Invaginated
rudiments of one kind or another have been described
in development of almost every non-pilidiophoran
nemertean species. At the very least, two lateral transitory invaginations are observed at the anterior end
on each side of the apical plate. These invaginations,
found in both palaeonemerteans and hoplonemerteans, have been variously interpreted as the
rudiments of the nervous system, the cerebral
organs, or other structures (Maslakova and von
Döhren 2009 and references therein). In the hoplonemertean Pantinonemertes californiensis, in addition
to the anterior invaginations, there is a pair of
transitory postero-lateral invaginations (Fig. 6;
Hiebert et al. 2010), which resemble the imaginal
discs of encapsulated Desor’s and Schmidt’s larvae
of the pilidiophorans Lineus viridis and L. ruber
(Schmidt 1964).
Hoplonemertean development is of particular interest to the origin of the pilidium larva, because the
hoplonemerteans represent a sister group to the
Pilidiophora (Thollesson and Norenburg 2003), and
the hoplonemertean decidula larva is clearly different
from the hidden trochophore larva of basal
741
Larval development in nemerteans
Funding
Friday Harbor Laboratories postdoctoral fellowship to S.A.M; the Society for Integrative and
Comparative Biology and the Society for Developmental
Biology
(Symposium
on
Spiralian
Development).
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I thank the researchers and staff of the Friday Harbor
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