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Some of the simplest animals in the sea enjoy a sex life unimaginable to Darwin, but fascinating for what it says about his famous legacy.

In the button-down world of university research, Don Levitan has a very sexy job. The marine ecologist has spent the better part of his career delving into the sex lives of animals who, to put it mildly, just don't get around much.

Levitan is an expert in the spawning habits of sea urchins and corals. At first blush, probing the mating playbook of these sedentary sea creatures may seem insufferably bland. There are no courtship displays or barroom brawls to determine who takes home the girl. No bucks locking antlers or male fiddler crabs making female crabs swoon with a come-hither wave of an oversized claw. No wink and a nod from the sexy sea urchin across the reef.

Even Charles Darwin was unfazed. The pre-eminent English naturalist posited that sexual competition didn't occur among species that fertilize eggs externally, in other words, without copulating. "In the lower division of the animal kingdom," he wrote, "sexual selection seems to have done nothing…(these animals') perspective and intellectual faculties are not sufficiently advanced to allow feelings of love and jealousy or the exertion of choice."

Levitan says this view, coming as it did from such an eminent authority, put a damper on early research into marine invertebrates' mating habits.

"Because naturalists did not realize there were sex differences in these organisms and because no one knew how to measure fertilization in the sea, this remained a largely unexplored topic."

So, pity the poor sea urchin or coral, the conventional thinking went. Too low on the Darwinian totem pole to pick a mate, too dumb to care.

But in recent years, Levitan says research has profoundly changed that thinking. Scientists have discovered that despite what Darwin thought, marine invertebrates such as urchins and corals have a robust—if complicated—sex life that is far beyond anything the father of evolution could have imagined.

Sex and the Single Sea Urchin

Levitan says the best part of his research is how he approaches it. He says he is the only biologist specializing in the reproductive habits of marine organisms who combines field experiments with molecular studies. From coral reefs of the Caribbean, in Panama and in Belize to the frigid coasts of western Canada, since 1989 he has observed firsthand one of nature's most intriguing phenomena—the annual spawning rites of some of the world's most colorful reef-bound marine creatures.

In the brisk waters off the west coast of Vancouver Island, for example, Levitan and his graduate students brave 45-degree waters to study the red sea urchin (Strongylocentrotus franciscanus). These small, spiky, globular creatures are members of the phylum Echinodermata, which also includes sea stars, sea cucumbers and brittle stars.

Analogous to wind-aided pollination of plants on land, sea urchin mating is a free-floating affair. Both male and female urchins look for environmental cues to tell them when to release their gametes—their eggs and sperm—into the open water. Levitan said this spawning activity seems to be triggered by a combination of phytoplankton and sperm. When phytoplankton concentrations are sufficiently high, a few males will start to spawn, in turn triggering other males and eventually females to join them.

In a single spawning event, male urchins can release anywhere from 10 billion to 100 billion milky white sperm cells, Levitan said. Females, by comparison, release only a million or so eggs.

How successful this co-mingling of eggs and sperm is—in terms of producing fertilized eggs—can vary widely, Levitan said. Many physical factors come into play, such as currents, wave action, water temperature, salinity and chemistry. Once fertilized, eggs spend about six weeks floating around before settling to the ocean floor and metamorphosing into an adult urchin.

But a major factor in determining the success of an urchin spawning event is a phenomenon well beyond the ken of even the sharpest scientist of Darwin's day. Both the eggs and the sperm cells are coated with layers of special proteins that attract each other, but at different rates. Surprisingly, there are plenty of fireworks in urchin sex—it's just that all the competition between the sexes takes place at the molecular level.

Large protein molecules attached to the surface of urchin eggs and sperm are literally the matchmakers of urchin mating, the key to the animals' existence and their evolutionary history. These critically important molecules determine the compatibility between suitor—sperm cells—and the pursued—the eggs.

Levitan is the first researcher to show how these proteins and other reproductive traits perform in the ocean and influence fertilization in both urchins and corals. In fact, he was the first biologist to measure patterns of sexual selection in an externally fertilizing organism, period. The body of his research represents a book of clues to the evolution of animals that don't need physical contact to reproduce.

Understanding how and under what conditions marine invertebrates successfully reproduce is important both commercially and ecologically. The research aids fisheries managers in determining sustainable harvests for oysters, abalones, mussels, clams and sea urchins, for example, and in designing marine reserves.

Sperm Wars: The Battle for the Prize Egg

But what Levitan and others have come to understand in ever-clearer detail is the importance of the availability of free-swimming sperm, especially to sessile (stationary) animals literally cemented to their homes for life. The relative levels of sperm density during spawning control both the reproductive success and evolution of these animals more than any other factor, said Levitan.

Too many sperm can be as bad—if not worse—than too few. Levitan's research has shed much light on why this is, and what it means.

When a free-swimming urchin (or coral) sperm cell chances upon an egg whose surface proteins find it compatible, the two gametes quickly fuse—"tie the knot," in a manner of speaking. When this happens, the egg immediately erects a cellular barrier to prevent access by other sperm. But if sperm cells happen to be overly abundant, additional sperm can sneak in before the egg gets a chance to erect a defense.

Biologists call this condition polyspermy, and it is lethal to eggs.

When sperm are at a normal density level, on the other hand, that's generally a plus for a successful spawning event. Polyspermy is kept at a minimum, and thus, compatible proteins are the "winners" in the competition for mates and become more common in the genetic pool.

But that's not the whole story. When sperm are abundant, eggs can rapidly evolve new surface proteins that fight polyspermy. Such eggs become pickier about their choice of mates-deliberately making themselves less compatible to the sperm hordes. Not to be outdone, spurned sperm can start making—evolving—newer and more enticing varieties of proteins, too, and fast. Eventually, the eggs find themselves right back where they started when vast numbers of sperm show up—vulnerable to multiple invasions of sperm (polyspermy) and thus death.

So, sperm are constantly under pressure to provide the best match possible with whatever eggs they encounter, while eggs faced with high sperm densities are constantly evolving mechanisms to repel multiple suitors. When sperm evolve to become a close match, the egg evolves to become a poor match, the male catches up by producing more compatible proteins, and the female once again is "chased away," so to speak.

Still, as a whole, urchins as a species benefit from this evolutionary arms race, Levitan said. Females with highly compatible eggs risk far higher chance of death from polyspermy when sperm are prolific.

Ultimately, females producing less compatible eggs are more successful at having their genes passed on to the next generation. Males do best when the fertilization rate is high and females are more successful when the fertilization rate is lower, resulting in conflict between males and females over the optimal fertilization rate—a tit-for-tat in the sexual game that perhaps even humans can relate to on some subliminal level.

Did Darwin have it all wrong?

Darwin was the first scientist to describe in any detail the dynamics of sexual competition and conquest among species—an elaborately cunning process he called the theory of sexual selection.

In most vertebrate animals, evidence is anywhere one cares to look that his idea—150 years old this year—is rock—solid. To keep themselves from going extinct, animals develop outlandish behaviors and physical accoutrements—from flashy tails to bright red appendages to deep-throated mating calls—in fierce competition to find a suitable mate. The whole elaborate song-and-dance explains how certain evolutionary traits get passed down through the generations, and, if necessary, modified over the eons.

Sexual selection at work is easy to see in a strutting peacock, but all but impossible to notice—with the unaided eye—in an invertebrate life-form that never moves or makes a sound. Darwin was dead-on when he posited that most species survive and evolve on the premises of sexual selection. What he didn't know was that his theory works at the molecular level.

"He was both right and wrong," says Levitan, "in that the act of sexual selection, instead of operating (strictly) on morphological traits, is operating on gamete traits and spawning behavior."

In other words, proteins on the surface of eggs and the number of individuals competing for mates—not physical traits such as body size, fighting appendages or plumage-determine who ends up with whom. And here's the kicker: This system works in humans, too.

"The same sorts of proteins are found on human and mammal eggs," he said. When it comes to picking a husband, women may be picky about the height, weight—and even smell—of whom they choose to marry. Playing silently behind this often unconscious sorting process in mate-picking is a molecular orchestra that modern biology is only now beginning to understand.

"The basic idea is that we need a thorough understanding of gamete (egg and sperm) availability," Levitan said. "In the end, this will provide a basic understanding of egg and sperm compatibility and perhaps provide insight into human fertility."

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