Origin of Asexual Reproduction in Hydra
Introduction
Hydra's buds develop through the integrated activity of two different types of cells:
- a) Epithelial (aka epithelial-muscular) cells forming the didermic
body wall (with extension into tentacles, hypostome, and foot) and
b) Interstitial cells (aka amoeboid or basal cells) differentiating as cnidocytes (aka nematocytes, the cells that make cnidocysts, aka nematocysts), nerve, gland, and sex cells [1-3].
Over the years, I consolidated some ideas and data into a theory
about how these different kinds of cells came to cooperate in budding
[4-8]. I proposed that early in the Neoproterozoic Era a primitive two
layered epithelial mat (resembling contemporary Placozoa [9-10]), was
infected by amoeboid cells already equipped with an extrusion apparatus.
The epithelia's attempt to reject the foreign cells failed but a
symbiogenic relationship evolved and the duel system found a selective
advantage in modified ejection. Ultimately, a mechanism for removing
excess amoeboid cells was adapted for the production of buds. The
adaptation hinged on three conditions:
- i. Amoeboid cells equipped with an extrusion apparatus were the ancestors of hydra's interstitial cells.
ii. Hydra routinely produced excess cells that moved toward and accumulate in the budding region.
iii. Excess cells form discrete modules that erupt as buds and are then "ejected."
a) Amoeboid cells equipped with an extrusion apparatus were the
ancestors of hydra’s interstitial cells. I am hardly the first to point
to the presence of stinging apparatuses in protozoans and to
similarities between protozoan "cnidocysts" and cnidarian cnidocysts:
the "peduncle," "rhizoid," and "perforator" cnidocysts of
dinoflagellates [11-14], the trichocysts of trypanosomes [15],
zooflagellates [16] and mastigophorans [17], the "apicoplasts" (apical
complexes) of "Sporozoa," the "polaroplast," of microsporidians [18],
and the "polar capsules" of myxosporidians [19-25]. Jiri Lom, the
distinguished Czech protozoologist and parasitologist, suggested that
these "homologies [were] perhaps too close to be considered only a
convergency phenomenon" [26], and Pierre Tardent, the renowned Swiss
coelenterologist commented "The wheel didn't have to reinvent itself"
[27], i.e., cnidrians didn’t have to invent cnidocysts. It is a small
step to extend Lynn Margulis' hypothesis of endosymbiosis [28] from
mitochondria and chloroplasts to cnidocysts. Ancient eukaryotic amoeba
could have been infected by monerans (presumably bacteria) already
equipped with an eversion apparatus. The "guest” would then introduce
genes to the "host" through unilateral horizontal gene transfer, and a
permanent extrusion apparatus (a cnidocyst) would have evolved in the
amoeba. What followed was a different sort of symbiosis -symbiogeny -
the merging and mutual evolution of eukaryotes [5-6]. In the case of
cnidarians, at some point in the evolution of multicellular eukaryotic
life, probably prior to the Vendian Period 700 million years ago, an
amoeboid protoctistan (to use Margulis' term [29], aka protozoan)
already equipped with an extrusion apparatus gained access to a
primitive didermic metazoan mat either by invading or being ingested. I
suggest that, at the time, mechanisms for isolating different forms of
metazoan life were not as restrictive as they became since and the
efforts of the epithelia to reject the amoeba were feeble.
Thus, the protoctistan wound up sequestered in the primitive
epithelium, and the two entered a symbiogenic relationship in which each
symbiont evolved to mutual advantage. Inevitably, cooperation gave rise
to the rudiments of the phylum Cnidaria. "Are cnidarians composite
metazoans... metazoan chimeras" [30]? Did what begin as a protoctistan
equipped with a cnidocyst - whether trespasser, guest, foreigner,
invader, colonizer, or ingested prey - become Cnidaria’s interstitial
cells, while the epithelial mat -host, victim, or predator -evolved into
the cnidarian epithelia Had that happened, interactions between the two
could have led to the further evolution of nerve and gland cells from
amoeboid descendants, while the cellular mat could have evolved into the
cnidarian body wall's epidermis and gastrodermis, tentacles with
epithelial battery cells, hypostome, peduncle, and adhesive foot.
b) Hydra routinely produces excess cells that move toward and
accumulate in the budding region. One of Hydra's attraction to
biologists is that under optimal laboratory conditions, hydra cultures
expand exponentially. The cell populations also expand exponentially
[31-34]. Since the density of hydra’s cell populations is constant,
except for transient increases in the budding region, hydras would seem
to produce and get rid of excess cells. Rather than treating these cells
as waste, however, symbiogeny capitalized on them by adapting them for
asexual reproduction through budding. The movement of cells toward the
budding region is well documented. Richard Campbell [31-35] calculated,
that in H. littoralis, under optimal laboratory conditions,
85-86% of hydra's structural cells produced throughout the body cylinder
(gastric, budding, and upper peduncle regions) migrate to the budding
region. Similarly, in H. viridis, about 800 of a thousand parental gastrodermal [digestive] cells move to the budding region per day [34].
Likewise, interstitial cells and their differentiation intermediates
make up more than half of all the cells in the adult animal moving to
the budding region [36]. The remainder of a hydra's daily cellular
production is lost at the animal's extremities, tentacles and foot. All
the excess cells dedicated to budding are produced along the length of
hydra’s body wall [31-37] in species- specific patterns of cell
division. Paul Brien discovered "La zone de croissance sous
hypostomiale" (Brien’s sub-hypostomal growth zone) in Hydra fusca [38],
and Allison Burnett extended Brien's growth zone in H. viridis and H. pseudoligactis (H. canadensis) to the gastric and budding regions [39] where a high frequency of mitotic figures is also found. Campbell showed that in H. littoralis,
a distal zone of elevated mitotic activity appears among epidermal
epitheliomuscular cells (a.k.a. "Ectodermal epithelial cells") and
gastrodermal gland cells (a.k.a. "Endodermal gland cells"), but cell
proliferation peaks in the budding region for interstitial cells
("Ectodermal interstitial cells," a.k.a. basal cells, amoeboid cells)
and gastrodermal epitheliomuscular cells (a.k.a. "Endodermal epithelial
cells") [33, 35, 40-42].
Measured in mitotic figures and in the incorporation of tritiated
thymidine, the epidermis supports a higher rate of cell division than
the gastrodermis [33]and labeled epidermal epitheliomuscular cells move
toward the budding region faster than gastrodermal digestive cells
[32-34]. Whatever the cell type, and wherever along the body column
cells are produced (i.e., both above and below the budding region) they
converge on the budding region [33-35,40-43]. The mesoglea situated
between the epidermis and gastrodermis is a substratum for cell movement
rather than a glue holding the two epithelial layers together.
Epithelial-muscle cells, with longitudinal muscle extensions seem to
actively crawl on the mesoglea with the help of their muscle processes
[44] and are seen to migrate over experimentally denuded mesoglea [45].
In contrast, the gastrodermal epithelial-muscle (digestive) cells with
circular muscle extensions seem to become compressed and crowded into
the budding region [46].
c) Excess cells form discrete modules that erupt as buds and are then
"ejected." Neither the budding region nor buds are distinctive
fountains of proliferating cells, meristems, or blastemata. Likewise, in
H. viridis, the frequencies of mitotic figures in early buds
lacking tentacles (stage I) and buds with tentacle rudiments (stage II)
"could not be distinguished." Given the absence of mitotic figures in
the hypostome, the "number of mitotic figures on the bud proper at the
later stage" (stage III) is below that on the parent [32]. Moreover,
cell divisions proceed at the same rate in freshly detached buds, during
the initial growth period, and in budding animals [32,34,47-51]. The
distinguishing characteristic of the budding region is the local
production of new mesogleal components [52-54]. Indeed, "[a]t sites of
tissue evagination... the mesoglea was dramatically remodeled and
epithelial cells moved relative to the mesoglea" [43].
Thus, "no loss of ECM [i.e., extracellular material of the mesoglea]
occurs before the time of bud emergence. Rather, the ECM is continuous
at the sites of bud formation and what occurs is simply an increase in
the expression of. [mesogleal components] as evagination of the bud
progresses.. Before evagination of the bud occurs. upregulation of at
least. [one mesogleal components] has already occurred. High expression
of both basement membrane and interstitial matrix components occurs
throughout all stages of bud formation" [54].
Hydra's excess cells funneled into the budding region form discrete
bud modules that break with parental symmetry, jut outward, form a
hypostome, tentacles, body cylinder, and feet, and ultimately detach as
buds [8, 30-35]. In transgenic H. vulgaris [43] and grafted H. viridis
[55], cells are literally seen moving out onto buds. "[C]ells located
near the evaginating centre will end up in the oral/distal part of the
bud; those located more distantly will move to a more aboral/proximal
part of the bud" [46]. The further "[e] longation of the early bud is
driven by recruitment of epithelial tissue from the mother polyp into
the newly forming protrusion" [46]. Interstitial cells may play a
special role in bud modules, since hydras partially or fully (?)
deprived of interstitial cells, so-called "epithelial animals," have
difficulty budding. Hydras’ interstitial cell population is reduced or
eliminated in a variety of ways: treatment with colchicine, nitrogen
mustard (NM), hydroxyurea, urethane, and lowered temperature [56-62].
Treated hydras suffer addition losses beyond interstitial cells:
Specialized nerve and gland cells disappear, and the hydras neither
move, capture prey, or ingest them. They do not restore the missing
cells either. If they survive the initial treatment, "epithelial
animals" frequently die from bacterial infections of slowly healing
wounds inadvertently inflicted during forced feeding and evacuation.
Surviving hydras (one in twenty) may enlarge, especially in their
peduncle, and add thin supernumerary tentacles [56].
Photographs of "epithelial animals" show bloated hydras with stubby
tentacles [56,58]. Like starved animals [63-66], "epithelial animals"
bud initially, and they are capable of regenerating thin tentacles
lacking cnidocysts, but without feeding the animals shrink in size [58].
Interstitial cell populations can be restored, however, in "epithelial
animals" [67] and in clones of reaggregated cells from NM-treated hydras
[68-70] through grafting with normal tissue. Along with the missing
interstitial cells and cell linages [70], including eggs [71] and sperm
[72], the hydras re-acquire normal morphology and behavior.
Under optimal laboratory conditions, hydras reach an equilibrium (a
steady state) at which body size is constant and the rate of cell
production is balanced by the rate of cell loss through budding
(everything else being equal such as cell loss on tentacles and foot).
At equilibrium, excess cells move to the budding region, join bud
modules, and move off the parental body column into developing buds
[30-41]. In contrast, starved hydras and "epithelial animals," deprived
of interstitial cells and their products only produce buds initially
while shrinking [64-66] and then cease budding. A residue of bud modules
would seem to be fully determined at the initiation of starvation and
interstitial cell destruction (albeit foot cells involved in detachment
may be defective in "epithelial animals"). But starved animals resume
budding when feeding is resumed, and "epithelial animals" resume budding
when interstitial cells are reintroduced [67-72].
The failure of starved animals to continue budding is easily
explained by the failure of these animals to fill bud modules, but the
absence of budding in "epithelial animals" (deprived of interstitial
cells and their products) suggests that epithelia alone are incapable of
rejecting cells in buds. Thus, hydra's epithelia need a dose of
interstitial cells to reject cells in buds. Interstitial cells would
seem to provide an essential component of bud modules required for cell
rejection or a trigger for the eruption of a bud from its module. The
premise that budding evolved from a primitive epithelia's attempt to
reject foreign amoeboid cells is consistent with these observations.
Symbiogeny's constructive and creative roles in evolution might have
modified cellular rejection into budding given budding's selective
advantage [3-8]. "Natural selection... is not [after all] the only force
governing evolution, nor had Darwin ever suggested that it was" [75].
The evolution of eukaryotes following the capture of mitochondria and
chloroplasts certainly justifies Lynn Margulis’ claims for the creative
consequences of endosymbiosis [28-29]. Likewise, the creative power of
symbiogeny, is implicit in the comparison between pond amoeba and
blood-borne magakaryocytes. The evolution of budding from the rejection
of amoeboid cells by a primordial epithelial mat at the beginning of
hydra's evolutionary history would seem another example of how
creativity is captured by natural selection [5,73-74].
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