The German biologist Fritz Müller wrote a famous book in 1863 that provided Darwin with crucial early support. Müller’s
book deals almost entirely with the anatomy of crustaceans, but bears the general title
Für Darwin (For Darwin).
Müller cited
Sacculina
, and its undoubted relationship with free-living barnacles, as a primary example of “retrogressive metamorphosis” in evolution. He referred to this genus as “these
ne plus ultras
in the series of retrogressively metamorphosed Crustacea,” and he wrote of their
limited activity:
The only manifestations of life which persist . . . are powerful contractions of the roots and an alternate expansion and contraction of the body, in consequence of which water flows into the brood-cavity, and is again expelled through a wide orifice.
E. Ray Lankester (1847–1929), later director of the Natural History Division of the British Museum, published a famous essay
in 1880 titled
Degeneration: A Chapter in Darwinism.
He defined degeneration as “a loss of organization making the descendant far simpler or lower in structure than its ancestor,” using
Sacculina
as a primary example. Lankester described the barnacle parasite as “a mere sac, absorbing nourishment and laying eggs.”
Yves Delage (1854–1920), one of France’s finest natural historians and a patriotic
Lamarckian, published a major empirical study on
Sacculina
in 1884. He referred to the genus as “this singular parasite, reduced to a sac containing the genital organs.”
“Sacculina,”
he added, “seems to be one of those beings made to chill adventurous imaginations” (
faits pour refroidir les imaginations aventureuses
).
Thus, all major authors and experts used the Rhizocephala as primary illustrations
of degeneration in the evolution of parasites (or, at least, of simplification if we wish to avoid the taint of moral opprobrium). I will not challenge this assertion for a restricted view of the adult as an external sac attached to internal roots. But I do wish to oppose the myopia of such a restriction. From a properly expanded viewpoint—and for three major reasons that I shall discuss in
sequence—rhizocephalans are remarkably intricate animals, as bizarre in their elaborate uniquenesses as any creature on earth. In this expanded perspective, however, they remain as wonderfully provocative as ever—as superbly illustrative of the meaning of evolution as when Europe’s greatest zoologists falsely appointed them as chief exemplars of Darwinian degeneration.
1. T
HE FULL LIFE CYCLE
OF THE
R
HIZOCEPHALA.
How did we ever discern the barnacle ancestry of
Sacculina?
We could now gain this information by sequencing DNA, but early-nineteenth-century zoologists correctly identified the affinity of rhizocephalans. How did they know, especially when studies of the adult externa and interna could not provide the slightest clue?
Observations of the complex life cycle in female rhizocephalans
solved this zoological puzzle. (I shall discuss the growth of males later, as my third argument.) The first two phases of growth differ very little from the development of ordinary barnacles, and therefore seal the identification. The larvae exit from the externa’s brood pouch as a conventional dispersal stage, common in many crustaceans, called the
nauplius.
The rhizocephalan nauplius passes
through as many as four instars (molting stages) and, except for the absence of all feeding structures, looks like an ordinary crustacean nauplius, right down to the most distinctive feature of a single median eye.
I am trying to suppress my usual lateral excursions in this essay—if only because I find the main line of the story so exciting—but I cannot resist one digression for its striking
illustration of science’s human face. Yves Delage’s 1884 monograph on
Sacculina
, undoubtedly the most important early study of rhizocephalans, runs to more than three hundred pages of dry anatomical description, devoted mainly to these early stages of the life cycle. But at several points he vents his anger at a German colleague, R. Kossmann. Delage took particular delight in exposing Kossmann’s
error in identifying two larval eyes. Early in his monograph, this French patriot admits the source of his venom and consequent pleasure in Kossmann’s mistakes. Kossmann had previously skewered a Frenchman, a certain Monsieur Hesse, for errors in interpreting the life cycle of
Sacculina.
Delage took offense for two reasons. First of all, poor Hesse was a dedicated amateur who only took up the
study of marine zoology in retirement, “at an age when so many others, in Germany as elsewhere, are only seeking to enjoy the inactivity of repose merited by their long service.” Kossmann should have been more generous. But second, and impossible to forgive, Kossmann had explicitly attacked Hesse
as a Frenchman
in clear violation of the norms of science as a cooperative and international enterprise.
Delage then speculated about Kossmann’s motives and recalled his own bitter feelings at the defeat of his country in the Franco-Prussian War of 1872:
What I cannot excuse is that this gentleman [Mr. Kossmann] expressed pleasure in seeing a scientist fall into error because that scientist is a Frenchman. This illustrates the workings of a narrow mind, and such thinking will quickly destroy the
characteristic nobility of scientific discussion. But Mr. Kossmann has an excuse. Note that he wrote in 1872, at a moment when Germany was still tipsy from its recent military successes, and he just didn’t have enough fortitude to resist the temptation to give the proverbial kick in the behind to the defeated.
The one-eyed nauplius only identifies rhizocephalans as crustaceans, but the next
phase, the cyprid larva, occurs only in barnacles and thus specifies the ancestry of the root-heads. If the nauplius acts as a waterborne dispersal phase, the subsequent cyprid explores the substrate by crawling about on a pair of frontal appendages called antennules, securing a good spot for attachment, and then secreting cement for permanent fastening. This cement fixes most barnacles to rocks,
but some species attach to whales or turtles, and one species sinks deep into whale skin to live as a near parasite. Thus, we can easily envisage the evolutionary transition from fastening to rock, to external attachment upon another animal, to internal burrowing for protection, and finally to true internal parasitism. In any case, the rhizocephalan cyprid functions like its barnacle counterpart
and searches for an appropriate site of attachment upon a crustacean host. (Favored sites vary from species to species; some settle on the gills, others on the limbs.)
We now reach the crux of the argument in considering the curious uniqueness of rhizocephalans as defined by newly evolved stages in an intricate life cycle. How does the cyprid, now attached to an external part of the host, manage
to get inside the host’s body to become an adult root-head? The rhizocephalan life cycle proceeds from taxonomic generality to uniqueness. The initial nauplius identified the creature as a crustacean; the subsequent cyprid proves barnacle affinities within the Crustacea. But the next phase belongs to root-heads alone.
The female cyprid, now attached to the host by its antennules, metamorphoses
to a phase unique to the rhizocephalan life cycle, as discovered by Delage in 1884 and named the
kentrogon
(meaning “dart larva”). The kentrogon, smaller and simpler than the cyprid, develops a crucial and special organ—Delage’s “dart” (now generally called an “injection stylet”). The kentrogon’s dart functions as a hypodermic needle to inject the precursors of the adult stage into the body of
the host!
This delivery system for the adult’s primordium shows great diversity across the two hundred or so species of rhizocephalans. In one group, the kentrogon cements its entire ventral surface to the host. The dart then pierces the host through this ventral surface, requiring a passage through three layers—the kentrogon’s cuticle, the attaching cement, and the host’s cuticle. In another
group, the kentrogon’s ventral surface does not cement, and antennules continue to function as attachments to the host. In these forms, including the genus
Sacculina
itself, the injecting dart goes right through one of the antennules, and thence into the body of the host! A third group skips the kentrogon stage entirely; the cyprid’s antennule penetrates the host and transfers the primordial cells
of the adult parasite.
Yves Delage, who discovered the kentrogon and its injecting device in 1884, could not hide his amazement. He wrote:
All these facts are so remarkable, so unexpected, so strange compared with anything known either in barnacles or anywhere in the entire animal kingdom, that readers will excuse me for providing such a thorough factual documentation.
But the next observation
strikes me as even more amazing—the high-point of rhizocephalan oddity, and a near invitation to disbelief (if the data were not so firm). What constitutes the primordium of the adult parasite? What can be injected through the narrow opening of the dart’s hypodermic device?
Delage, who discovered the mechanism, concluded that several cells, maintaining some organization as precursors to different
tissues of the adult, entered the host. He could hardly come to grips with the concept of this much reduction separating larval and adult life. Imagine going through such complexity as nauplius, cyprid, and kentrogon—and then paring yourself down to just a few cells for a quick and hazardous transition to the adult stage. What a minimal bridge at such a crucial transition! “The
Sacculina
,” Delage
wrote, “has been led to make something of a tabula rasa [blank slate] of its immediate past.” Delage then groped for analogies, and could only come up with a balloonist jettisoning all conceivable excess weight upon springing a leak.
All can be explained by the necessity for the parasite to make itself very small in order to pass more easily through the narrow canal, whose dimensions are set
by the orifice of the dart. [The transferred cells] are in the same condition as an aeronaut whose balloon has lost part of its gas, and who, needing to rise again at all cost, lightens his load by throwing out everything not absolutely indispensable to the integrity of his machine.
Well, Monsieur Delage, the actual situation far exceeds your own source of amazement. You were quite right; many
species do transfer several cells through the dart. But other species have achieved the ultimate reduction to a single cell! The dart injects
just one cell
into the host’s interior, and the two parts of the life cycle maintain their indispensable continuity by an absolutely minimal connection—as though,
within
the rhizocephalan life cycle, nature has inserted a stage analogous to the fertilized
egg that establishes minimal connection
between
generations in ordinary sexual organisms.
The evidence for transfer of a single cell has been provided in recent articles by our leading contemporary student of rhizocephalans, Jens T. Høeg of the zoological institute of the University of Copenhagen. (I read about a dozen of Høeg’s fascinating papers in preparing this essay, and thank him for so
much information and stimulation.) In a 1985 article on the species
Lernaeodiscus porcellanae
, published in
Acta Zoologica
, Høeg documented the settlement of cyprids, formation of kentrogons, and injection of only a single cell, recognizable within the kentrogon, into the host. Høeg writes of the tenuous bridge within the kentrogon: “Because of its size and apparent lack of specialization the
invasion cell stands out conspicuously against the surrounding epithelial, nerve and gland cells.”
The September 14, 1995, issue of
Nature
, my original inspiration for this essay, reports an even more remarkable discovery: “A new motile, multicellular stage involved in host invasion by parasitic barnacles (Rhizocephala),” by Henrik Glenner and Jens T. Høeg. The authors found that the kentrogon
of
Loxothylacus panopaei
injects a previously unknown structure into the host: a wormlike body containing several cells enclosed in an acellular sheath. This “worm” breaks up within the host’s body, and the individual cells, about twenty-five in number, then disperse separately “by alternating flexure and rotating movements.” Apparently, each cell maintains the potential to develop into an entire
adult parasite, though only one usually succeeds (a few crabs develop multiple externa with independent root systems inside the body).
This minimal transition helps to explain why the adult root-head shows no sign of barnacle affinities. If the adult parasite develops anew from a single transferred cell, then all architectural constraints of building an adult from parts of a taxonomically recognizable
larva have been shed. In any case, the primordial cell or cells then migrate from the site of injection, through the circulatory spaces of the host, find a site for settlement, build an internal root system, and finally emerge through the host’s abdomen as a new structure bearing the charming name of “virgin externa.”
Take all this—nauplius; cyprid; kentrogon; injected passage into the host’s
body, sometimes by a single cell; migration to a permanent site; reproduction of the rooted interna; and emergence of the externa. Stack up these stages against our own lives, even through all the Sturm und Drang of our teenage years, and which life cycle would you label as more “complex”?
2. M
ANIPULATING AND COMMANDEERING THE HOST.
The adult parasite may look like a rooted blob, but just as
the most unprepossessing humans often hide immense power beneath their ordinary appearance (as many a Hollywood “toughie” has discovered to his great hurt and sorrow), beware of equating ugly wartiness with benign simplicity. The adult rhizocephalan parasite has more tricks up its nonexistent sleeve than externa appearance would suggest.
Consider the following problem in logic as an indication
of the physiological and behavioral sophistication that adult parasites must possess. We know that crabs fight back when the cyprid larvae try to settle, for potential hosts use their cleaning and grooming behaviors to remove the settling cyprids—and the great majority of potential parasites are thereby destroyed. In fact, the rapid transformation of exploring cyprid to cementing kentrogon (accomplished
within ten minutes in some species), the low and hunkering shape of the kentrogon, and its firm cementation to the host in many species have all been interpreted—quite correctly in my view—as active adaptations by the parasite to vigorous counterattacks by potential hosts.