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Cnidarians have long been considered simple animals in spite of the variety of their complex life cycles and developmental patterns. Several cases of developmental conversion are known, leading to the formation of resting stages or to offspring proliferation. Besides their high regenerative and asexual-reproduction potential, a number of cnidarians can undergo ontogeny reversal, or reverse development: one or more stages in the life cycle can reactivate genetic programs specific to earlier stages, leading to back-transformation and morph rejuvenation. The switch is achieved by a variable combination of cellular processes, such as transdifferentiation, programmed cell death, and proliferation of interstitial cells. The potential for ontogeny reversal has limited ecological meaning and is probably just an extreme example of a more general strategy for withstanding unfavourable periods and allowing temporal persistence ofspecies in the environment
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Reverse development in Cnidaria
S. Piraino, D. De Vito, J. Schmich, J. Bouillon, and F. Boero
Abstract: Cnidarians have long been considered simple animals in spite of the variety of their complex life cycles and
developmental patterns. Several cases of developmental conversion are known, leading to the formation of resting
stages or to offspring proliferation. Besides their high regenerative and asexual-reproduction potential, a number of cni
darians can undergo ontogeny reversal, or reverse development: one or more stages in the life cycle can reactivate ge
netic programs specific to earlier stages, leading to back-transformation and morph rejuvenation. The switch is
achieved by a variable combination of cellular processes, such as transdifferentiation, programmed cell death, and pro
liferation of interstitial cells. The potential for ontogeny reversal has limited ecological meaning and is probably just an
extreme example of a more general strategy for withstanding unfavourable periods and allowing temporal persistence of
species in the environment.
Résumé : Depuis longtemps, on considère les cnidaires comme des animaux simples, malgré la variété de leurs cycles
biologiques et de leurs patterns de développement complexes. Il existe plusieurs cas de conversions au cours du déve
loppement qui mènent à la formation de stades de repos ou à la prolifération de rejetons. En plus de leur fort potentiel
de régénération et de reproduction asexuée, plusieurs cnidaires peuvent subir un renversement de leur ontogenèse ou un
développement inversé : un ou plusieurs stades dans le cycle biologique peuvent réactiver des programmes génétiques
spécifiques de stades antérieurs, ce qui donne une rétro-transformation et un rajeunissement des morphes. Le revire
ment est provoqué par une combinaison variable de processus cellulaires, tels que la transdifférentiation, la mort cellu
laire programmée et la prolifération de cellules interstitielles. Le potentiel de renversement ontogénique a une
signification écologique limitée; il s’agit probablement d’un état extrême d’une stratégie plus générale pour survivre
aux périodes défavorables et permettre à l’espèce de se maintenir dans le temps dans son milieu.
[Traduit par la Rédaction] Piraino et al. 1754
The diversity of cnidarian ontogeny
The complexity of hydrozoan life cycles and the
“immortal” jellyfish
The life cycle of the Hydrozoa is typically characterized
by the alternation of three life stages: the planula larva, the
postlarval polyp stage (mainly colonial), and the adult stage,
i.e., the medusa (Boero et al. 2002). The ciliated planula has
been also interpreted as a motile gastrula, and the polyp as
the true larval stage (Bouillon and Boero 2000). The planula
lives only from a few hours to a few days before metamor
phosis, whereas both polyp and medusa stages can have a
much longer life-span (from days to years) (Bouillon 1994).
This life cycle is usually invoked as being paradigmatic for
the Medusozoa group (Hydrozoa, Scyphozoa, Cubozoa, and
Staurozoa; see Marques and Collins 2004). However, side
ways deviations from the norm are common (Fig. 1). Ancestral
taxa (e.g., Actinulidae, Narcomedusae, and Trachymedusae)
lack a polyp stage (Bouillon and Boero 2000); in contrast,
members of derived families of the Hydroidomedusa group
(e.g., Aglaopheniidae, Plumulariidae, and Sertulariidae) re
duced, in part or totally, the medusa stage by paedomor-
phosis (Boero and Bouillon 1987). In many cases, the polyp
becomes the adult stage, and gametes can differentiate either
in the hydranth body column, (e.g., in Hydra spp.) or within
highly reduced medusae (fixed gonophores) retained by
polymorphic polyp colonies. Other species can produce
short-lived, free medusoid morphs characterized by reduced
swimming and (or) feeding potential (e.g., Macrorynchia
philippina (Kirchenpauer, 1872) (Gravier 1970) or Nemale
cium lighti (Hargitt, 1924) (Gravier-Bonnet and Migotto
2000)). These morphs, called swimming gonophores by
Boero and Bouillon (1989), are liberated with already mature
gonads, and their dispersal from the polyp colony is usually
limited (Boero et al. 2002).
In many hydrozoan species, the normal pace of the life
cycle can be modified at some stages. Both planula and
polyp stages can shrink and rest in low-metabolic-cost states
(cysts, dormant hydrorhizae) to survive critical periods, be
ing ready to reactivate cell proliferation and morphogenesis
at the onset of favourable seasons (Boero et al. 1992). Polyp
colonies can last for several years, annually producing large
batches of sexually competent medusae, followed by peri
odic colony shrinkage and recurrent cycles of regenerative
processes, without any obvious sign of senescence (Forrest
1963; Müller 1996). This process, also known as renovation,
is a type of regeneration. In nature, renovation is a normal
process in the hydroid colonies of many Leptomedusae, and
may be repeated several times during their life-span, depend
ing upon intrinsic factors (i.e., age of the colony, health of
the colony, etc.) or sometimes upon the ecological condi
Can. J. Zool. 82: 1748–1754 (2004) doi: 10.1139/Z04-174 © 2004 NRC Canada
Received 28 May 2004. Accepted 23 November 2004.
Published on the NRC Research Press Web site at on 2 February 2005.
S. Piraino,
D. De Vito, J. Schmich, J. Bouillon, and
F. Boero. Dipartimento di Scienze e Tecnologie Biologiche
ed Ambientali, Università di Lecce, via per Monteroni,
73100 Lecce, Italy.
Corresponding author (e-mail:
© 2004 NRC Canada
Piraino et al. 1749
tions they face. Renovation is usually accomplished by
changes in morphology and functional commitment of al
ready specialized cells, a process known as transdifferenti
ation (Schmid 1992). Interstitial cells (I-cells) may partly
contribute to the renovation process, but they are not a fun
damental requisite. In fact, not all those species undergoing
colony or polyp renovation have I-cells (Brien 1941). More
over, cell replacement and differentiation along the body
column, regeneration, and asexual reproduction are equally
active processes in Hydra spp. populations experimentally
deprived of I-cells (Brien and Reniers-Decoen 1955; Diehl
and Bouillon 1966; Marcum and Campbell 1978). Renova
tion is rare, or perhaps less easy to observe, in Antho
medusae polyps, but it is known to occur (e.g., in Tubularia
spp.; Tardent 1963). In marine Hydrozoa, regeneration and
cell replacement occur by activation of epithelial smooth
muscle cells, which then become stem cells by dediffer
entiation (Schmid 1974).
At different levels, both polyp and medusa stages of
Hydroidomedusae can exhibit a combination of budding and
regenerative processes (Boero et al. 2002). It is known that
medusae of several species have the ability to bud (but not
to metamorphose into) polyp structures before or even after
initiation of processes of sex-cell determination (Boero et al.
2002). In addition, direct medusa budding from liberated
medusae is known for several species. Large populations can
be built up in time and space, allowing the species to cross,
by following the currents, deep oceanic waters, where
planulae may have few or no chances to settle. This type of
medusa budding involves transdifferentiation of preexisting
cell types on the manubrium, tentacular bulbs, radial canals,
exumbrellar rim, marginal canal, subumbrellar rim, or even
gonads (for further discussion and a species list see Boero et
al. 2002 and references therein).
An additional potential has been discovered in a few spe
cies whose polyp stage can also be reformed from regressing
tissues of sexual stages (Figs. 1C–1D). Müller (1913) first
described such “reverse ontogeny” in Hydrozoa, having ob
Fig. 1. Models of some hydrozoan life cycles. (A) Hydra spp. have no medusa stage and no planula larva. The gonads originate on the
polyp body column; the new polyp hatches directly from a cuticled embryo. Asexual budding of new polyps is the most frequent mode
of reproduction. (B) Hydractinia echinata (Fleming, 1828) has a highly reduced medusa stage that remains attached to the polyp in the
form of fixed gonophores. Fertilization leads to the formation of a planula larva, which will undergo metamorphosis to develop into a
polyp colony. (C) The life cycle of Hydractinia (Podocoryna) carnea includes a swimming medusa stage and a planula larva. Artificial
detachment of late medusa buds leads to the development of medusae that are complete but reduced in size. In contrast, artificially de
tached early medusa buds are capable of transformation back into polyps. Such reverse transformation is not usually achieved by late
medusa buds or liberated medusae. (D) Turritopsis nutricula has a typical three-stage life cycle: planula, polyp, and medusa. However,
medusae at all stages of development retain the potential for life-cycle reversal; even spent medusae do not die, but transform back
spontaneously into new polyp colonies.
served the formation of stolons and polyps from regressing
medusa buds mechanically detached from the gonozooids of
Hydractinia (Podocoryna) carnea (M. Sars, 1846). Only early
medusa buds could undergo reverse development, whereas
late buds developed into small but fully formed medusae
(Frey 1968; Schmid 1972). Hauenschild (1956) observed the
same potential in Eleutheria dichotoma Quatrefages, 1842
and Kakinuma (1969) reported a comparable process in
Cladonema sp. and Cladonema uchidai Hirai, 1958, with
the formation of hydrorhizal stolons from early medusa buds
experimentally detached from the gonozooids. Also,
Bavestrello et al. (2000) described a complex fragmentation
process in polyp colonies of Hydractinia (Stylactaria)
pruvoti (Motz-Kossovska, 1905) that is induced by strong
water movements: fragmentation of gonozooids bearing
medusa buds led to the early liberation of developing
eumedusoids. As in H. carnea, mature eumedusoids of
H. pruvoti started swimming and spawning, while early
stages underwent a regressive transformation giving rise to
stolons and polyps.
It is now known that the reverse transformation of
H. carnea is due not only to regeneration by proliferation of
I-cells, but also to the occurrence of cell-transdifferentiation
processes (Schmid 1972; Schmid et al. 1982; Schmid and
Alder 1984; Alder and Schmid 1987). Transdifferentiation is
defined as a change in commitment and gene expression of
well-differentiated, non-cycling somatic cells to other cell
types directly or through their reversion to undifferentiated
cells (Okada 1991). In Hydroidomedusae, transdifferenti-
ation might be a common phenomenon in budding and re-
generation, especially where no or few I-cells are located
(Brien 1941). Manubrial budding of secondary medusae in a
few species belonging to different families (Bougainvillidae,
Hydractiniidae, Rathkeidae) originates only from differenti-
ated ectodermal cells, with no aid from the I-cell compart-
ment (Bouillon 1962; see also Boero et al. 2002 and
references therein). All tissues of the newly formed medusae
derive from transdifferentiating ectoderm. However, in all
other cases, the contribution of transdifferentiation processes
is still unstudied.
The fate of developing buds of Sarsia tubulosa (M. Sars,
1835) can be altered by sudden changes in temperature
(Berrill 1953). Medusa buds can develop, depending on wa
ter temperature, either in normal free medusae or in sessile
eumedusoids with rudimentary tentacles and lacking both
mouth and ocelli. Moreover, when rearing of S. tubulosa is
shifted to the temperature range 6–8 °C, medusa buds can be
transformed back into polyp buds (Werner 1963). This pro
cess suggests the involvement of cell transdifferentiation and
programmed cell death, as occurs in H. carnea.
In most cases, ontogeny reversal occurs in incompletely
developed medusa buds with no sign of gonads. The poten
tial for reverse ontogeny is suppressed in late bud stages
with developing gonads, and in liberated medusae. The onset
of sexual reproduction might thus be regarded as the point of
no return in the ontogenetic sequence in any living organ
ism, ultimately leading to aging and death (Stearns 1992). In
cnidarians, as in most other organisms, germ-cell differentia
tion seems to represent a signal for irreversible somatic de
termination, preventing back-transformation of late medusa
buds. However, studies on Turritopsis nutricula Mccrady,
1859 (Anthomedusae, Clavidae) (Fig. 2) demonstrated that
this rule can be broken. Bavestrello et al. (1992) showed that
newly liberated medusae of this species can revert to polyp
stages; later, Piraino et al. (1996) showed that ontogeny re
versal occurs at all stages of medusa growth, including the
adult stage with mature gonads (Fig. 2d). Thus, rejuvenation
of the medusa morph into the polyp stage is always possible
in this species, and is not constrained by gamete differentia
tion. In T. nutricula, rejuvenation involves the contribution
of both transdifferentiation and I-cell-proliferation processes
(Piraino et al. 1996), together with the activation of cell-
death programs (Carlà et al. 2003). These medusae react to
unfavourable conditions (e.g., starvation, mechanical stress,
temperature and salinity changes), starting reverse transfor
mation into the polyp stage: a complete reduction of all
medusa-specific organs and tissues, followed by differentia
tion of new, polyp-specific cell types and the formation of
the polyp morph (Piraino et al. 1996). In T. nutricula, even
senescence (started by the sexual maturation of the gonads)
is a stress factor that consistently induces reverse transfor
mation of medusae. This process would be hardly more re
markable if a butterfly were able to revert to its caterpillar
stage. It must be considered a true metamorphosis, but in the
opposite direction to larval metamorphosis. At the molecular
level, it is reflected in a distinct pattern of stage-specific
gene expressions (Spring et al. 2000; Yanze et al. 2001). Re-
cently, young medusae of T. nutricula and even H. carnea
were shown to undergo reverse transformation and rejuvena-
tion to the polyp stage by exposure to cesium, a chemical
inducer of metamorphosis (J. Schmich, unpublished data).
In addition, reverse development has been recently demon-
strated to occur also in Leptomedusae: young, immature
medusae of Laodicea undulata (Forbes and Goodsir, 1851)
are able to revert to the polyp stage (De Vito et al.
). Steps
leading to back-transformation in L. undulata are compara
ble to those observed in young T. nutricula medusae
(Piraino et al. 1996). The first signals of ontogeny reversal
are thinning of the mesoglea and shortening of the tentacles.
The medusa then becomes unable to swim and settles to the
bottom of the culture vessel. The umbrella is reduced within
a few hours, and the whole medusa is transformed into a
cyst-like rounded mass of poorly differentiated cells.
Periderm-covered hydrorhizae develop soon and the first
“regenerated” polyp appears within 48–72 h of the initiation
of the process. Within a month, new gonothecae are already
reformed from the rejuvenated colony and, from there, sec
ondary medusae are newly budded. Medusae of L. undulata
with mature gonads were not observed and it is still not
known if they retain the potential for ontogeny reversal also
in sexually competent stages, as in T. nutricula.
The formation of stolons by back-transformation was also
observed in mechanically detached medusoids of Cytaeis
schneideri (Motz-Kossowska, 1905) (S. Piraino, unpublished
observations) and from a newly liberated medusa of Clytia
hemisphaerica (L., 1767) (De Vito et al.
). In both cases,
© 2004 NRC Canada
1750 Can. J. Zool. Vol. 82, 2004
D. De Vito, S. Piraino, J. Schmich, J. Bouillon, and F. Boero. Laodicea undulata (Forbes and Goodsir 1851) (Cnidaria, Hydrozoa), a
leptomedusa with the potential for reverse ontogeny. Submitted for publication.
however, stolon formation was not followed at least in
our laboratory experiments by polyp development.
Back-transformation (Rückbildung) in Scyphozoa
In Scyphozoa, the paradigm of the medusozoan life cycle
(planula–polyp–medusa) is retained, but with the distinctive
addition of a pre-adult stage, the ephyra, produced by trans
verse fission of the polyp (strobilation; see Spangenberg
1965, 1968). The medusa phase predominates in the life cy
cle of most scyphozoans, and the polyp stage (scyphistoma)
is in some cases significantly reduced or even completely
suppressed (e.g., in the genera Atolla and Pelagia). Species
of two coronate genera (Nausithoe, Thecoscyphus) lack a
free medusa stage (Jarms 1997) but, unlike many Hydrozoa,
Scyphozoa never completely lose a medusoid stage. Modifi
cations of the basic scyphozoan cycle are the production of
polyp resting stages, called podocysts (known in both
Semeostomeae and Rhizostomeae; for a list of species see
Arai 1997), and of “planula-cysts” (in the genus Cyanea;
Brewer 1976 and references therein). Regeneration can be as
powerful in the Scyphozoa as in the Hydrozoa. Scypho
medusae can regenerate lost organs and tissues, and new
coronate polyp colonies can grow from individually excised
polyps. A striking example of regeneration and asexual re
production by means of “pseudoplanulae” was first discov
ered in Chrysaora sp. by Hérouard (1909), who described
the autotomy of polyp tentacles leading to a ciliated
“planula-like” stage, which was capable of locomotion and
settlement to produce secondary polyps. Afterwards, Lesh-
Laurie and Corriel (1973) demonstrated consistent regenera
tion of complete polyps from isolated tentacles of Aurelia
aurita (L., 1758) scyphistomae. The process of propagule
formation by autotomy of tentacles is also known in Hydro
zoa (e.g., the limnomedusa Armorhydra janowiczi Swedmark
and Teissier, 1958 (Campbell 1974); the hydroidomedusa
H. pruvoti (Bavestrello et al. 2000)).
The first reports of true reverse development in Cnidaria
were given by Hadzi (1909a, 1909b, 1912), who described
back-transformation (Rückbildung) of ephyrae of Chrysaora
hysoscella (L., 1766) to scyphistoma polyps under unfavour
able environmental conditions. Reverse transformation of
ephyrae into scyphopolyps was later observed also in Rhizo
stoma pulmo (Macri, 1778) (Paspaleff 1938) and A. aurita
(Thiel 1963). Comparably, under unfavourable rearing con
ditions, the ephyrae of eight species of Coronatae may un
dergo ontogeny reversal, first regressing to planuloid masses
of cells, and growing into polyps later (from weeks to
months) (reviewed by Jarms 1997). The ability of Nausi
thoidae to produce planuloids is regarded as an ontogenetic
strategy to minimize energy losses and enable survival and
propagation in low-energy habitats, such as caves or deep
seas (Jarms 1997). In this framework, Nausithoe planulo
© 2004 NRC Canada
Piraino et al. 1751
Fig. 2. Reverse development of T. nutricula.(a) Free-living healthy medusa. (b) Transforming medusa, with the everted subumbrellar
muscle layer (at left) and outer manubrium (at right). BrdU staining of DNA replicating nuclei. (c) Ball-like or cyst-like stage of a
transforming medusa. BrdU staining of DNA replicating nuclei. (d ) Butterfly-shaped remnant of an adult medusa of T. nutricula (set
tled on a glass slide) with four mature male gonads (white arrows), producing a hydrorhizal stolon characteristic of the polyp stage
(black arrow). (e) A newly formed polyp from reverse development of a medusa (within 36–48 h at 24 °C). Scale bars: (a)1mm;
(b) 500
m; (c) 300
m; (d and e) 500
phorus (Werner, 1971) shows the highest degree of special
ization by retaining within the polyp peridermal tube all
strobilae, which are eventually transformed into the
planuloid stage, crowling out of the tube and settling a short
distance from the parental polyp. As noted by Jarms (1997),
this apogamic life cycle precludes the benefits of sexual re
combination and should be considered an evolutionary dead-
Reversible metamorphosis in Anthozoa
Anthozoa are considered the ancestral group of Cnidaria
(Bridge et al. 1992; Collins 2002). Their simple life-cycle
pattern consistently lacks a medusa stage, whereas dispersal
is mainly delegated to planula larvae or occurs by fragmen
tation and drift of asexual propagules. Recently, Fautin
(2002) reviewed the modes of cnidarian reproduction: two
main modes of asexual reproduction, scissiparity (either
transverse and longitudinal fission) and budding (sensu
Bouillon 1994) are mainly found in Anthozoa (with the ex
ception of Ceriantharia). Secondary modes of asexual repro
duction are less common, like laceration of the pedal disk in
some Actiniaria, or pinnitomy in some octocorals, whose
tentacular pinnules can autotomize and fall from the parent
colony to give rise to new polyps and, then, new colonies
(Gohar 1940). Comparably, the tentacles of boloceroidid sea
anemones can reconstitute new polyps (Cutress 1979; Pearse
2002). Tentacle or pinnule autotomy is a homologue of the
above-mentioned formation of pseudoplanulae in Scypho-
zoa, with regeneration of complete polyps from autotomized
or isolated tentacles of scyphistomes.
Polyp bail-out (Sammarco 1982) is an adaptive response
to environmental stress, providing a way of escape and adult
dispersal in a pocilloporid coral (also observed in Hydrozoa;
see Gravier-Bonnet 1992). Polyps are able to leave their
hard skeleton and detach from the parent colony. This pro-
cess implies a partial rearrangement of the running genetic
machinery, switching off the progressive assembly of inor
ganic skeletal components and partly reshaping the polyp
column. A further step towards reactivation of early develop
mental programs in Anthozoa is found again within the fam
ily Pocilloporidae. Richmond (1985) described “reversible
metamorphosis” in Pocillopora damicornis (L., 1758), whose
primary polyps may, under unfavourable conditions, aban
don the primary corallites shortly after metamorphosis and
regress to a planula-like stage. Such secondary larvae could
search for appropriate sites of settlement and metamorphose
again. However, nothing is known about such reverse trans
formation at the cellular level, including the potential
contribution from the I-cell compartment or from trans
differentiation processes.
Many metazoans, namely Porifera, Cnidaria, Platyhel
minthes, Placozoa, Nemertea, Rotifera, Nematoda, Acantho
cephala, Arthropoda, Tardigrada, Ectoprocta, and Tunicata,
are able to withstand unfavourable conditions by producing
resting stages through different processes (e.g., encystment,
degrowth or reduction in size, survival budding; see Piraino
et al. 1996 and references therein). These can be envisaged
as developmental conversions along the normal ontogenetic
path. Reverse development, however, seems to be a distinc
tive feature of cnidarians. A growing mass of information
suggests that the potential for ontogeny reversal is more
widespread in Cnidaria than was previously thought.
In most cases, the transformation of body portions into
earlier structures represents a way to produce either resting
or dispersive stages without sexual reproduction. This possi
bility exists in both polyps (which give rise to planula-like
structures) and young medusae (which give rise to polyps).
In the case of T. nutricula, and a small group of other spe
cies, however, a completely different interpretation is called
for. The medusae of T. nutricula, in fact, invariably trans
form into polyps under laboratory conditions (Piraino et al.
1996) and have been called immortal by the nonscientific
press. From each medusa undergoing reverse ontogeny, a
new colony can potentially originate, which in turn will pro
duce new copies of the original medusa, leading to an expo
nential increase in the total number of clonemate offspring.
To date, this potential has been repeatedly demonstrated in
the laboratory with a large number of observations in
T. nutricula (Piraino et al. 1996). By implication, they could
attain immortality. But if this potential for avoiding death
were expressed in the field, these animals would saturate the
world’s oceans! Instead, we see that they suffer mortality,
and population growth is kept under control. It is probable
that such a great potential for ontogeny reversal has limited
meaning and is just an extreme example of a more general
strategy for withstanding unfavourable periods and allowing
temporal persistence of species in the environment.
As already mentioned, the potential for reverse develop-
ment could be present, but hidden, in other cnidarians. In
laboratory experiments the lack of unknown field factors
(e.g., species-specific relationships with marine bacteria) may
obscure possible back-transformation, but the genetic ma-
chinery may remain functional, as is also demonstrated by
the artificial activation of reverse development in adult medu
sae of H. carnea by chemical inducers of metamorphosis.
To date, it seems that only scyphozoan ephyrae, but not
adult medusae, can revert to the polyp stage and, within
Anthozoa, only coral primary polyps can revert to planula
larvae. However, available information on Staurozoa and
Cubozoa is scant and the life cycles of many cnidarians still
need to be elucidated. Therefore, we can reasonably assume
that new cases of reverse development could be discovered.
Other species can retain the potential for transformation, but
(i) it can be transiently expressed only under extraordinary
conditions, or (ii) the genetic program involved in the trans
formation process can be activated, but only few species re
tain the whole signalling cascades needed for the completion
of morph reversal.
As often happens in experimental biology, extreme cases
can become a paradigm for uncovering general, albeit less
extreme, patterns. Boero et al. (1997) theorized that the ge
nome of hydromedusan species with complex life cycles
might be (functionally) divided into two main portions, one
coding for the polyp and one coding for the medusa stage.
The two main stages of the life cycle, in fact, possess differ
ent cell types and organs. As was noted by Boero et al.
(1998), hydrozoan polyps are diploblastic, whereas their
medusae are triploblastic and possibly coelomate, since their
subumbrellar cavity originates by cavitation (i.e., schizo
© 2004 NRC Canada
1752 Can. J. Zool. Vol. 82, 2004
coely) within a third cell layer that, in turn, differentiates
into the striated muscle lining the subumbrella (striated mus
cle is mesodermic in all other Metazoa). With ontogeny re
versal by transdifferentiation, medusa cells transform into
polyp cells, with a total reprogramming of their fate. The
one-way route of developmental programs, always leading
to death, is inverted! In T. nutricula, ontogeny reversal is
caused by both environmental cues (sublethal stress) and se
nescence, activating a trigger that can switch on or restart
the “reading” of the genetic information almost from the
very beginning. As is often the case, epigenetic and genetic
cues concur in defining developmental patterns. The discov
ery of such switching mechanisms is a further step towards
clarifying the mechanisms of senescence and rejuvenation,
and might represent a breakthrough in developmental biol
ogy in general (Boero 1998).
Many thanks are extended to Prof. Volker Schmid (Basel),
who guided us to an understanding of reverse development
and transdifferentiation in Hydrozoa and provided valuable
comments on the manuscript. Financial support was pro
vided by Ministero dell’Istruzione, dell’Università e della
Ricerca (60%, Cofinanziamento progetti di ricerca di inter-
esse nazionale projects and Fondo per gli investimenti dell
ricerca di base), the Administration of the Province of Lecce,
Istituto centrale per la ricerca scientifica e tecnologica
applicata al mare (“Identificazione e distribuzione delle spe-
cie non indigene nel Mediterraneo” project), the European
Union (Marie Curie contract HPMD-CT-2001-00099, and
the Marine Biodiversity and Ecosystem Functioning Net-
work of Excellence), the National Science Foundation of the
USA (Partnerships for Enhancing Expertise in Taxonomy:
NSF DEB-9978131 project on the Hydrozoa).
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... In cnidarians, the borders of sexual and asexual reproduction are rather faint; research continuously adds new insights into these reproductive processes. Asexual reproduction is a field of enormous variation among and even within species, and numerous different forms of asexual reproduction, from mechanical fragmentation to reverse development, to propagation, have been described in cnidarians (reviewed in Fautin, 2002;Piraino et al., 2004). In fact, most ...
... Colony break-up is a common response of cnidarians to a variety of adverse conditions (Babcock, 1991;. Indeed, there are several processes described in cnidarians returning to a mobile individual stage (Piraino et al., 2004), leading to the question: Can polyp bailout be differentiated or distinguished from other similar developmental aspects such as asexual reproduction and propagation mechanisms and reverse developmental processes (Piraino et al., 2004)? In particular, where and how to place polyp bailout in a profound categorization between asexual modes of reproduction or reverse developmental processes is currently proving difficult. ...
... Colony break-up is a common response of cnidarians to a variety of adverse conditions (Babcock, 1991;. Indeed, there are several processes described in cnidarians returning to a mobile individual stage (Piraino et al., 2004), leading to the question: Can polyp bailout be differentiated or distinguished from other similar developmental aspects such as asexual reproduction and propagation mechanisms and reverse developmental processes (Piraino et al., 2004)? In particular, where and how to place polyp bailout in a profound categorization between asexual modes of reproduction or reverse developmental processes is currently proving difficult. ...
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Corals have evolved a variety of stress responses to changing conditions, many of which have been the subject of scientific research. However, polyp bailout has not received widespread scientific attention, despite being described more than 80 years ago. Polyp bailout is a drastic response to acute stress in which coral colonies break down, with individual and patches of polyps detaching from the colony and the calcareous skeleton Polyps retain their symbiotic partners, have dispersal ability, and may undergo secondary settlement and calcification. Polyp bailout has been described worldwide in a variety of anthozoan species, especially in Scleractinia. It can be induced by multiple natural stressors, but also artificially. Little is known about the evolutionary and ecological potential and consequences of breaking down modularity, the dispersal ability, and reattachment of polyps resulting from polyp bailout. It has been shown that polyp bailout can be used as a model system, with promise for implementation in various research topics. To date, there has been no compilation of knowledge on polyp bailout, which prompted us to review this interesting stress response and provide a basis to discuss research topics and priorities for the future.
... At the same time, the medusa stage can be absent in representatives of the Hydroidolina subclass (e.g., in some Leptothecata) [24]. In some species of the Bougainvillidae, Hydractiniidae, and Rathkeidae fami lies, vegetative reproduction can occur both at the polyp and medusa stages [25]. The polyp stage is absent in the life cycle of some Scyphozoa, such as Pelagia [26]. ...
... It is believed that this process is caused by stress, such as starvation or drastic changes in the envi ronment. Reverse development has been observed in sev eral Hydrozoa species at the medusa stage [25]. One of the most well known experiments is the induced regres sion of a mature medusa of the immortal jellyfish Turritopsis spp. ...
A unique set of features and characteristics of species of the Cnidaria phylum is the one reason that makes them a model for a various studies. The plasticity of a life cycle and the processes of cell differentiation and development of an integral multicellular organism associated with it are of a specific scientific interest. A new stage of development of molecular genetic methods, including methods for high-throughput genome, transcriptome, and epigenome sequencing, both at the level of the whole organism and at the level of individual cells, makes it possible to obtain a detailed picture of the development of these animals. This review examines some modern approaches and advances in the reconstruction of the processes of ontogenesis of cnidarians by studying the regulatory signal transduction pathways and their interactions.
... For example, a settled, calcified polyp may build back its radially compartmented body plan, reverse metamorphosis to become a mobile secondary larva, disperse with the currents and reattach elsewhere (Richmond 1985). Reverse development may also affect the colony: through ontogenetic reversal, genetic programs specific to earlier stages are reactivated, leading to back- 'rejuvenation') resulting in resting developmental stages with inert metabolic functions (Piraino et al. 2004). Polyp detachment, including polyp expulsion and polyp bail-out, is another form of reverse development, where a sessile polyp abandons its initial structure and becomes mobile again, maintaining its biological organization. ...
... Polyp dropout differs from other reported forms of reverse development confined to stressed shallow-water colonial scleractinians in tropical, subtropical and temperate environments in a number of ways (Table 1). In contrast to (i) reversible metamorphosis (Richmond 1985) and (ii) ontogeny reversal (Piraino et al. 1996(Piraino et al. , 2004, polyp dropout is not accompanied by fundamental changes in the body plan. Polyp dropout also differs from (iii) polyp expulsion (Kramarski-Winter et al. 1997) and (iv) polyp bail-out (Sammarco 1982;Kružić 2007;Capel et al. 2014;Serrano et al. 2018). ...
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Scleractinian corals feature both sessile and mobile stages and diverse modes of development. In some cases, development can be reversed. Examples include polyp detachment in response to environmental stress (bail-out or polyp expulsion) and reverse metamorphosis, where juveniles detach from the primary skeleton and revert to the mobile stage. Here, we provide aquaria and field evidence of a new form of reverse development: polyp dropout in the solitary cold-water coral Caryophyllia huinayensis. It features tissue retraction and detachment of an entire adult polyp from the skeleton in the putative absence of a stressor. The dropout polyp remains viable and continues to live for many weeks, albeit in a rather collapsed state lacking a well-developed hydroskeleton. We carried out a long-term (37 months) rearing experiment under constant aquaria conditions and found polyp dropout in four out of 83 individuals. Detachment was accompanied by the extrusion of mesenterial filaments through perforations in the body wall. We believe this resulted in the loss of the hydroskeleton, which prevented the dropouts to subsequently resettle or form a new skeleton. As opposed to other known forms of reverse development, the new form is not accompanied by reversible metamorphosis, abandonment of the colonial way of life, nor is it a survival or asexual reproduction strategy. We found field indications of polyp dropout in Patagonian field populations of C. huinayensis , where 1.4 ± 0.8% (mean ± SD, N = 9322) of the polyps of the natural population showed partial detachment indicative of imminent dropout in the putative absence of external impact. Polyp dropout is the first record of polyp detachment in a solitary CWC with possible repercussions for adult coral mobility, evolution and Stanley’s (2003) ‘naked coral’ hypothesis.
... Many cnidarians, for instance, display remarkable abilities to transdifferentiate, seemingly including converting somatic cells into germ cells (Gold and Jacobs, 2013). Medusozoan cnidarians are even capable of "degrowing" gonadal structures or reverting to asexuality (Hamner and Jenssen, 1974;Piraino et al., 2004). Similarly, plants do not segregate germlines from somatic lineages, but rather derive germ cells from somatic lineages (Kawashima and Berger, 2014). ...
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A small number of extraordinary "Major Evolutionary Transitions" (METs) have attracted attention among biologists. They comprise novel forms of individuality and information, and are defined in relation to organismal complexity, irrespective of broader ecosystem-level effects. This divorce between evolutionary and ecological consequences qualifies unicellular eukaryotes, for example, as a MET although they alone failed to significantly alter ecosystems. Additionally, this definition excludes revolutionary innovations not fitting into either MET type (e.g., photosynthesis). We recombine evolution with ecology to explore how and why entire ecosystems were newly created or radically altered-as Major System Transitions (MSTs). In doing so, we highlight important morphological adaptations that spread through populations because of their immediate, direct-fitness advantages for individuals. These are Major Competitive Transitions, or MCTs. We argue that often multiple METs and MCTs must be present to produce MSTs. For example, sexually-reproducing, multicellular eukaryotes (METs) with anisogamy and exoskeletons (MCTs) significantly altered ecosystems during the Cambrian. Therefore, we introduce the concepts of Facilitating Evolutionary Transitions (FETs) and Catalysts as key events or agents that are insufficient themselves to set a MST into motion, but are essential parts of synergies that do. We further elucidate the role of information in MSTs as transitions across five levels: (I) Encoded; (II) Epigenomic; (III) Learned; (IV) Inscribed; and (V) Dark Information. The latter is 'authored' by abiotic entities rather than biological organisms. Level IV has arguably allowed humans to produce a MST, and V perhaps makes us a FET for a future transition that melds biotic and abiotic life into one entity. Understanding the interactive processes involved in past major transitions will illuminate both current events and the surprising possibilities that abiotically-created information may produce.
... tion of endoparasitic myxozoans and further radiations within this clade, including the vermiform ceratomyxids. These traits include exceptional capacities for developmental plasticity, regeneration and transdifferentiation(Bosch, 2008;Leclère & Röttinger, 2017;Piraino et al., 2004), a relatively simple body plan based on epithelial sheets (ectoderm and endoderm), and the principal cnidarian building block (epitheliomuscular cells). Developmental plasticity and the diploblast body plan may have predisposed the evolution of endoparasitism and miniaturisation associated with endoparasitism in the Myxozoa(Okamura et al., 2015b). ...
Metazoans with worm-like morphologies across diverse and disparate groups typically demonstrate motility generated by hydrostatic skeletons involving tissue layers (muscles and epithelia). Here we present representative morphological, behavioural and molecular data for parasitic cnidarians (myxozoans) that demonstrate unprecedented variation in form and function, developing as cellular hydrostats. Motile elongate plasmodia characterise a remarkable radiation of species in the genus Ceratomyxa. The vermiform plasmodia inhabit gall bladders of a range of South American freshwater fish and exhibit undulatory motility reminiscent of nematodes but achieved at the cellular level. Collective insights from ultrastructure, confocal and light microscopy along with videos depicting movements highlight key features that we propose explain the unique motility of the plasmodia. These features include cytoskeletal elements (net forming microfilaments and microtubules), a large internal vacuole, a relatively rigid outer glycocalyx and peripherally arranged mitochondria. These constituents provide collective evidence for repurposing of the cnidarian epitheliomuscular cell to support worm-like motility at the cellular level. The apparent restriction of vermiform ceratomyxids to South American freshwaters suggests an origination via Cretaceous or Miocene marine transgressions and subsequent radiation.
... Classical in vitro experiments have also shown that isolated muscle from the medusae umbrella can reconstruct de novo organs under the special culture conditions [16]. Furthermore, in some jellyfish, including the "immortal jellyfish", Turritopsis dohrnii, adult medusae can transform into cysts after injury or starvation and eventually return to polyps, a phenomenon known as "reverse development" [17,18]. These observations indicate that the medusa stage exhibits a high regenerative capacity, which likely varies across different species. ...
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Medusozoans, the Cnidarian subphylum, have multiple life stages including sessile polyps and free-swimming medusae or jellyfish, which are typically bell-shaped gelatinous zooplanktons that exhibit diverse morphologies. Despite having a relatively complex body structure with well-developed muscles and nervous systems, the adult medusa stage maintains a high regenerative ability that enables organ regeneration as well as whole body reconstitution from the part of the body. This remarkable regeneration potential of jellyfish has long been acknowledged in different species; however, recent studies have begun dissecting the exact processes underpinning regeneration events. In this article, we introduce the current understanding of regeneration mechanisms in medusae, particularly focusing on cellular behaviors during regeneration such as wound healing, blastema formation by stem/progenitor cells or cell fate plasticity, and the organism-level patterning that restores radial symmetry. We also discuss putative molecular mechanisms involved in regeneration processes and introduce a variety of novel model jellyfish species in the effort to understand common principles and diverse mechanisms underlying the regeneration of complex organs and the entire body.
During this PhD project, I studied a natural transdifferentiation event naturally occurring in vivo in a single cell using the nematode worm Caenorhabditis elegans as a model organism. This cell, called Y, transdifferentiates from a rectal identity into a moto-neuron identity called PDA. This system has contributed key insights on the transition and cellular steps involved in transdifferentiation and the identification of conserved nuclear factors crucial to the initiation of the process, or the relative importance and roles of transcription factors versus histone modifying factors for the dynamics and robustness of the conversion. Those evidences suggest that many genes are switched ON or OFF. However, the transcriptional dynamics of the transition remains unknown. This transdifferentiation event cannot be studied in vitro. I therefore need to use entire animals to understand how this process functions, in a single cell. During the development of my PhD work, I setup new ways to use a methodology called DamID, which I implemented on whole animals. DNA adenine methyltransferase identification (DamID) uses a fusion between a protein of interest, in our case an RNA polymerase subunit and a bacterial adenine methyltransferases (Dam). Binding of the RNA polymerase to transcribed genes leads to DNA methylation of their genomic locus, which can be subsequently identified using molecular techniques. In order to restrict expression of the dam::fusions to the transdifferentiating cell, I used different methodologies including in vivo recombination systems and fluorescence activated cell sorting. This PhD work have produced a collection of Y specific genes that can help to get a better understanding of how Y-to-PDA transdifferentiation initiates and what molecular key players are regulating the beginning of this natural transdifferentiation event in the Caenorhabditis elegans. This PhD work also generated a new DamID pipeline using Oxford Nanopore Technologies that will be extremely useful to carry molecular biology studies using this nematode or other model organisms
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Adult stem cells (ASCs) in vertebrates and model invertebrates (e.g. Drosophila melanogaster) are typically long-lived, lineage-restricted, clonogenic and quiescent cells with somatic descendants and tissue/organ-restricted activities. Such ASCs are mostly rare, morphologically undifferentiated, and undergo asymmetric cell division. Characterized by 'stemness' gene expression, they can regulate tissue/organ homeostasis, repair and regeneration. By contrast, analysis of other animal phyla shows that ASCs emerge at different life stages, present both differentiated and undifferentiated phenotypes, and may possess amoeboid movement. Usually pluri/totipotent, they may express germ-cell markers, but often lack germ-line sequestering, and typically do not reside in discrete niches. ASCs may constitute up to 40% of animal cells, and participate in a range of biological phenomena, from whole-body regeneration, dormancy, and agametic asexual reproduction, to indeterminate growth. They are considered legitimate units of selection. Conceptualizing this divergence, we present an alternative stemness metaphor to the Waddington landscape: the 'wobbling Penrose' landscape. Here, totipotent ASCs adopt ascending/descending courses of an 'Escherian stairwell', in a lifelong totipotency pathway. ASCs may also travel along lower stemness echelons to reach fully differentiated states. However, from any starting state, cells can change their stemness status, underscoring their dynamic cellular potencies. Thus, vertebrate ASCs may reflect just one metazoan ASC archetype.
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: Based on live specimens of Nemalecium lighti collected in the coasts of La Reunion (Indian Ocean) and Sao Sebastiao (Southeastern coast of Brazil) and kept in the laboratory, we observed the release of short-lived medusoids. The gonangia pass through six developmental phases: growing, ripening, migrating, stripping, liberating and spawning. The medusoids are tall, lack tentacles, bulbs, circular and radial canals, and the sexual products are packed around the eccentric manubrium; they are provided with a velum and with a subumbrellar ectoderm rich in transverse striated muscle fibers. There are refringent and isotropic corpuscles within vacuolated and ciliated large cells located around the aperture of the medusoid, which possibly function as statoliths. The corpuscles are similar to those already described for the families Plumulariidae and Aglaopheniidae. The gametes are liberated shortly after the release of the medusoid from the gonotheca. The female medusoid spawned 40-62 ova; spermatozoa exhibited a semicircular nucleus, and planulae were formed c. twelve hours after fertilization. Colonies with medusoids of only one sex or with both male and female medusoids.
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A cladistic analysis of 87 morphological and life history characters of medusozoan cnidarians, rooted with Anthozoa, results in the phylogenetic hypothesis (Anthozoa (Hydrozoa (Scyphozoa (Staurozoa, Cubozoa)))). Staurozoa is a new class of Cnidaria consisting of Stauromedusae and the fossil group Conulatae. Scyphozoa is redefined as including those medusozoans characterized by strobilation and ephyrae (Coronatae, Semaeostomeae, and Rhizostomeae). Within Hydrozoa, Limnomedusae is identified as either the earliest diverging hydrozoan lineage or as the basal group of either Trachylina (Actinulida (Trachymedusae (Narcomedusae, Laingiomedusae))) or Hydroidolina (Leptothecata (Siphonophorae, Anthoathecata)). Cladistic results are highly congruent with recently published phylogenetic analyses based on 18S molecular characters. We propose a phylogenetic classification of Medusozoa that is consistent with phylogenetic hypotheses based on our cladistic results, as well as those derived from 18S analyses. Optimization of the characters presented in this analysis are used to discuss evolutionary scenarios. The ancestral cnidarian probably had a sessile biradial polyp as an adult form. The medusa is inferred to be a synapomorphy of Medusozoa. However, the ancestral process (metamorphosis of the apical region of the polyp or lateral budding involving an entocodon) could not be inferred unequivocally. Similarly, character states for sense organs and nervous systems could not be inferred for the ancestral medusoid of Medusozoa.
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Die Hydromeduse Eleutheria dichotoma pflanzt sich normalerweise sowohl geschlechtlich als auch vegetativ fort. In Klonkulturen treten jedoch als Ausnahmen sprunghaft asexuelle Medusen auf, welche die Fähigkeit zur Keimzellenbildung eingebüßt haben und sich nur noch vegetativ fortpflanzen; auch von den am Polypen entstehenden Primärmedusen ist nicht selten ein kleiner Prozentsatz bereits asexuell. In beiden Fällen erscheinen in der vegetativen Nachkommenschaft der geschlechtslosen Medusen, auch bei jahrelanger Zucht, keine sexuell differenzierten Exemplare mehr. Durch Zerstückelung und Aufzucht der Regenerate sowie durch Röntgenbestrahlung ließ sich ein derartiger Verlust der Sexualität z. T. künstlich herbeiführen. Asexuelle Individuen konnten nur durch Implantation von Normalmedusen-Gewebe wieder zur Keimzellenbildung veranlaßt werden; dabei waren die an I-Zellen besonders reichen Implantate am wirksamsten. Dagegen war eine entsprechende Einpflanzung von Polypengewebe stets erfolglos.
The behavior of the planula of Cyanea capillata (Linneaus) is studied in the laboratory to determine if it responds to environmental cues in a way which may account for the distribution of its sedentary scyphistoma stage in the field.The planulae react to gravity, water chemistry, surface texture, and possibly to light. They exhibit an initial geopositive response in well-aerated sea water, but become active and geonegative under conditions associated with local depletion of oxygen. Their attachment follows, and is usually upside-down on a horizontal surface. They attach with greatest frequency on substrates that are rough, and give evidence of discriminating among surfaces of different rugosity. The planulae possibly show a weak photonegative response at the time of attachment; confirmation of this photic response requires further work. These sequential responses shown in the laboratory result in an orientation at the time of attachment which is in agreement with the position usually occupied by the scyp...