The larval lifestyle may seem alien to us terrestrial bipeds,
but it comes quite naturally to most creatures
especially inhabitants of the worlds oceans.
By Gregory A. Wray
A tiny larva, not much larger than a speck of dust, swims through the swirling soup of plankton in the cool waters of Puget Sound. Rows of minute cilia along the sides of its body pulsate continuously, pulling single-celled algae near before flicking them into its mouth. Fifty feet below the larva, an adult of the same species creeps across the rocky seafloor in search of a meal. Looking nothing like the larva and colossal by comparison (weighing about a million times more), this animala Pisaster ochraceus sea star, or starfishis an active predator, searching out clams and mussels to pry open with its powerful arms. The larva and the adult lead lives that differ in almost every conceivable way: what they eat, how they move, what predators they must avoid, and the physical world they must negotiate.
From a human perspective, this may seem an odd arrangement. Even as embryos, we possess many anatomical features of our future adult bodies, albeit often in rudimentary form. Furthermore, only a few temporary structures appear during human development, most notably the transient gill slits that close when we are still early embryos, the placenta that feeds us in the womb, and the baby teeth that erupt soon after birth. Human development is quite direct, involving a fairly steady progression toward adult form.
Not so for most animals. The vast majority begin life as larvae that differ drastically from the corresponding adults. Many familiar animals have a larval form: caterpillars turn into butterflies, and tadpoles into frogs. But it is among the oceans marine invertebrates that the larval lifestyle is most dramatically displayed. By one estimate, about 170,000 species of marine invertebrates exist worldwide, including not only sea stars but also sea urchins, sea cucumbers, sea slugs, and sea lilies, as well as corals, clams, barnacles, and feather-duster worms. These animals typically spend days, weeks, or even months in larval form, mostly swimming in the top ten to twenty feet of water in the company of myriad other creatures. (One bucketful of seawater might contain the larvae of a dozen or so species of marine invertebrates.) At the end of the larval stage, the animals drop down to the seafloor and metamorphose into adults. There they live, grow, and eventually reproduce, releasing sperm and eggs into the water and beginning the cycle again.
The marine invertebrate larvae are so small that their discovery came only in the late 1700s, with the development of good microscopes. Samples of seawater examined through these new instruments revealed a world teeming with unfamiliar organisms. Early observers believed that these tiny creatures must be the adults of previously unknown species, and they named them according to the animals often bizarre shapessuch as pilidium (from the Greek word for hat) or auricularia (from the Latin for ear).
Barnacle larvae found crawling on adults, for instance, were thought to be parasitesa misconception not corrected until the 1820s, when Irish surgeon and amateur naturalist John Vaughn Thompson observed them metamorphosing into immature barnacles. Zoologists initially responded to his findings with disbelief; for centuries, many people had believed that goose barnacles were the young of real geese (hence the barnacles common name), and zoologists were understandably wary of this new and seemingly equally fantastic claim.
Two decades after the publication of Thompsons findings, German physiologist Johannes Müller accidentally discovered a second example while studying a microscopic creature to which he had earlier given the scientific name Pluteus paradoxus, or strange easelan apt name for a creature whose triangular profile and projecting legs gave it the general appearance of an artists easel, albeit a nearly transparent one flecked with bright red spots. Müller was surprised to observe a miniature brittle star (a slender relative of sea stars) growing inside the body of this minute animal. His continuing patient observations revealed that the two creatures were in fact one and the same: the adult develops inside the swimming larva, whose body is cast away when the adult takes up residence on the seabed.
One by one, nearly all the creatures in the peculiar microscopic bestiary of ocean water were found to be the larval stages of familiar animals. By the beginning of the twentieth century, scientists could confidently assert that a complex life cycle with an extended larval detour is in fact the most common method of development in the animal kingdom. This newly discovered complexity raised several questions: Why is the larval stage such a widespread feature of animal life, and if it is advantageous, why dont all animals go through one? And why do larvae look so bizarre?
One key insight into these questions came during the 1920s from Walter Garstang, an English embryologist and amateur poet. Garstang was among the first to argue that larvae are intricately adapted to their planktonic world, a world so different from the seafloor habitat of adults that few features of anatomy could serve a useful purpose in both locations. Take, for example, cone snails (or cone shells, as they are known to collectors): the adults crawl about the seabed, while the larvae are swept along by currents near the oceans surface; the adults are active predators, armed with potent neurotoxins, while the larvae are herbivores that capture single-celled algae with the aid of microscopic cilia; and the adults are preyed upon by octopuses, while small jellyfishes and a great variety of other tiny predators feed on the larvae. The contrasts are enormous.
Pointing to transient larval organs that form no part of the adult, Garstang argued that the rigors of life among the plankton drove the evolution of numerous and seemingly bizarre adaptations in the early part of the life cycle: the highly convoluted tracts of cilia on the larvae of clams and acorn worms, used for swimming and feeding; the long spines on some annelid worm larvae that flare in response to the slightest touch; and the specialized, suckerlike organs used by the larvae of sea squirts and sea stars to adhere to rocks or shells during metamorphosis.
Although Garstangs observations and conclusions may now seem almost obvious, they went against the then-prevailing view. Just half a century earlier, the German comparative anatomist Ernst Haeckel had forcefully argued that embryonic development retraces the course of evolutionary history. Haeckel, who interpreted larvae as vestiges of ancestral adults, remained influential well into the twentieth century. In arguing that its anatomy specifically adapts a larva for planktonic life, Garstang challenged Haeckels paradigm and, indeed, played an important role in its eventual demise as a general principle. (Garstangs poetry remains popular among biologists today, in large part because it venomously satirizes Haeckel and other intellectual opponents.)
But why would young need a body plan and habitat different from those of adults? In Garstangs view, the answer was dispersal. Local habitatswhether a suitable rock, a chunk of coral reef, or a bit of sandy sea bottominevitably suffer periodic disruptions from silt deposition, unusually violent storms, disease outbreaks, and the like. Setting great numbers of offspring adrift in the ocean increases the chance that at least some will survive and be delivered to suitable locations, a strategy that contemporary ecologists call bet hedging.
Larvaes ability to drift long distances also provides a mechanism for genetic mixing. Many adult marine invertebrates have only a limited ability to move, and some, such as corals and barnacles, do not move at all. Inbreeding is a real danger for creatures that are (quite literally, in some cases) stuck in one place. Widespread dispersal helps ensure that when larvae do settle down, their neighborsand potential mateswill be unrelated.
Although dispersal provides tangible benefits, the cost is high. Among the plankton are numerous diminutive but voracious carnivores, including small jellyfishes and comb jellies, saber-toothed creatures called arrowworms or chaetognaths, and a host of crustaceans and small fishes. Larvae that are not eaten are still prey to the ocean currents, which can sweep them away from suitable habitats. And when suitable habitat means a coral reef in the Pacific Oceanseparated from the next reef by perhaps a thousand miles of open oceanalmost any current is likelier to move a larva away from safety than toward it.
Yet the broad geographical distribution of many species of marine invertebrates across the South Pacific is proof that larvae do sometimes successfully drift from reef to reef, crossing over abyssal depths that adults could never negotiate. Just how far from its birthplace a larva may drift became clear in the 1970s, when oceanographers, using fine-mesh nets similar to those invented by Thompson a century and a half earlier, began a systematic sampling of plankton in the middle of oceans. These plankton hauls often included the larvae of clams, sea stars, and other invertebrates whose adults live only in the relatively shallow water of continental shelves. We now know that the Gulf Stream sweeps countless larvae out of the Caribbean Sea and into the North Atlantic, where most perish and perhaps a tiny fraction survive long enough to ride the entire gyre to Europe and back across to the Caribbean.
All these hazards take a heavy toll. Estimates of larval death rates range from 10 to 20 percent per day. Even at the lower rate, barely one-fifth of a brood will survive two weeks among the plankton, and only a few percent will last a month. (Most larvae must feed for weeks or months before they grow large enough to undergo metamorphosis.) Such heavy mortality suggests that natural selection will favor the evolution of well-defended larvae that eat efficiently, grow quickly, drop out of the plankton community in short order, and soon undergo metamorphosisjust as Garstang and others suggested nearly a hundred years ago. The idea has only recently been tested in detail, however.
Using time-lapse microscopy, Michael Hart, an evolutionary biologist at Dalhousie University, has observed echinoderm larvae capturing food particles and then quantified their feeding rates. Comparing the rates of sea urchin and sea star larvae, he found that those of sea urchins were higher and that these larvae reached metamorphosis sooner. Anatomically the two kinds of larvae are quite similar, and both use the cilia along the sides of their bodies to sweep algae toward their mouths, but the sea urchin larvae also develop long projections lined with hundreds of cilia, which help the larvae pull in even more food. Specializations for feeding abound among immature marine invertebrates. The cilia on the larvae of acorn worms capture algae; strings of mucus serve as fishing lines for some sponge larvae; and the larvae of lobsters and shrimp use powerful claws to grab unwary prey.
Well-fed or not, larvae face the problem of predation. The larvae of many groups defend themselves with spines and spikes, which can be impressive. Some shrimp larvae sport sharp spines extending more than five times their body length. Other defensive strategies include toxicity (some sea squirt larvae) and concealment (larval snails that hide in their shells). And nearly all marine invertebrate larvae enjoy the advantage of transparency.
To study how larvae defend themselves from predators, Steve Rumrill and Tim Pennington, then graduate students at the University of Alberta, set up aquariums with different combinations of predators (adult jellyfish and juvenile fish, for example) and prey (sea urchin embryos and larvae in various stages). They found that the embryos and younger larvae were especially vulnerable because they had not yet developed their feeding projections, inside of which are spiny spicules capable of deterring some predators, such as jellyfish. But nothing stopped the fish, whose mouths opened wide enough to swallow even late-stage urchin larvae whole.
Even if a larva manages to get enough to eat and to escape being eaten, it confronts the challenge of finding an appropriate place to settle and undergo metamorphosis. Those fortunate enough to drift near the right habitat at the right time must still select exactly the right site. Settling near a hungry snail could be disastrous for a peanut worm, and landing too far from kelp would doom a sea urchin to starvation. As the time for metamorphosis approaches, most larvae become acutely sensitive to chemical cues that signal the presence of food, conspecific adults, and potential hazards. The importance of finding a good place to land is underscored by the fact that the decision, once made, is often final: many larvae bear specialized structures that glue them to their chosen spot.
Metamorphosis itself must coincide with settlement on the seafloor, an environment so different from the surface that no larva would long survive unchangedjust as no adult could handle life in a planktonic world. Metamorphosis can be dramatic and literally gut-wrenching. Almost immediately after attaching to a rock or a blade of kelp, for instance, the larva of a bryozoan begins a violent rearrangement of its internal organs and external appearance. Pockets of sticky cells evert, securing the animal in place; other cells evert to form the outside of the adult; still others secrete a tough shell; and muscles quickly fold the former larval body wall inside the newly forming adult, where it is resorbed. In many ribbon worms and echinoderms, metamorphosis is remarkably rapid, with the major changes from larval to adult body form taking less than half an hour.
And then there are larvae that have no need to feed at allincluding those of some clams, snails, sea stars, and annelid worms. Nonfeeding larvae are generally much simpler anatomically than the feeding larvae of related species, having jettisoned useless feeding structures and significantly accelerated the events leading to metamorphosis. In these species, eggs are provisioned with enough protein and fat to fuel development all the way through metamorphosis. This shift to dependence on maternally provided food reserves has evolved within most groups of animals and at many junctures in the history of life. In the most extreme cases, a distinct larval stage is lost altogether, and embryos develop directly into miniature versions of adults. This evolutionary shift, too, has occurred many timesgroups as diverse as squids, roundworms, and most vertebrates develop without the benefit of larvae.
Why dont all species adopt this trick of minimizing or even bypassing the larval stage? Because neither having nor lacking a larva is inherently superior. Each has costs and benefits, and the balance shifts among groups of animals and across the myriad habitats of the marine realm. Species with feeding larvae, for example, produce small eggs and consequently can afford to have much larger broods, whereas species with nonfeeding larvae or direct development tend to produce larger eggs or to have placentas and therefore much smaller brood sizes. Predators may also affect the duration of larval development: species heavily preyed on as small juveniles may be better off prolonging their time among the plankton, but others may do better to settle on the seafloor as quickly as possible and thus avoid planktonic predators. Understanding the particular ecological contexts that favor the evolutionary retention, reduction, or loss of larvae represents one of the outstanding challenges facing biologists today. For now, however, we can say that although larvae dont offer the only road to adulthood, for most animals they provide a good way to get there.
An associate professor of biology at Duke University, Gregory A. Wray wrote on sea stars and other echinoderms in the December 1998January 1999 issue of Natural History. That article ("Body Builders of the Sea"), coauthored with Rudolf A. Raff, prompted our editors to put together the present set of articles on marine invertebrates. Wray continues to study the evolution of developmental mechanisms in echinoderms (as well as in ants). The peculiar anatomy of marine larvae was what first sparked his interest in asking how natural selection shapes the way an animal develops, a question that led in turn to his current research on the evolution of gene networks in embryos and larvae.
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