Alarming Butterflies and Go-Getter Fish.

Overlooked ways to invent new species

There's a trick at the top of evolutionary biologist James Mallet's Web page, where five pairs of tropical Heliconius butterflies pose in a double row.

Each pair flashes a distinctive pattern of colored bands across dark wings. Read the caption closely. Partners in the pairs may look alike, but they don't belong to the same species. Instead, the five butterflies with blatantly mismatched colors in the top row do belong to the same species. The bottom five, equally mismatched ones belong to a single other species.

So, what's going on?

Butterfly enthusiasts may shrug off the question as just another case of Nature taunting any poor soul with a field guide. Mallet of University College London and his colleagues, however, look to these butterflies for hints about where species come from. Mallet muses over one of the big questions of biodiversity: Why do some variations lead to new species when others don't?

That question may be old, but these are tumultuous times for such matters. Within the past few years, biologists have observed species splits with what appear to be the wrong geography, wrong time frame, and wrong driving force. In response, some researchers have proposed new types of origins for butterflies, fish, flies, and other animals.

Mallet describes "a fundamental divide" now opening between biologists concocting these new scenarios and those working with older approaches.

To give a rough sense of the philosophical split between the camps, Mallet describes the different types of events that these groups have enthroned as the main force that cleaves one species into two. The older scenarios typically invoke radical changes in landscape or huge catastrophes, Mallet says. They make up the major-motion-picture school of speciation, with volcanoes spurting, continents cracking, and glaciers grinding over the horizon.

In contrast, scientists whom Mallet has whimsically called "prophets of the new ways" look more to small-scale accommodations of everyday life. Some researchers call this approach "ecological speciation." Their hypotheses hinge on an animal finding a new fruit to eat, shallower water for laying eggs, or a better dodge to foil attackers.

The debate over the splitting of species, Mallet says, "is really about whether we need a deus ex machina or whether life itself can create the instabilities."

Before plunging too deeply into the mechanisms of life, let's smash some illusions about theories of evolution.

First, there's the matter of just what a species is. Believe it or not, that's still an open question among biologists. Ask most reasonably diligent high school students, and chances run high that they will say that a species is a group of organisms sharing many characteristics and breeding among themselves but not with members of another species. Versions of that formulation dominated biology for decades. Ask modern evolutionary biologists, however, and there'll be no consensus. Voices rise and dueling graphs appear.

For just a sample of the fray, consider the puzzle of hybrids. Hundreds of species do interbreed to some extent where their ranges overlap, and plenty of their offspring reproduce and mix up parentage even more. For example, although North American warblers mate mainly with others of their species, they break the rules on interbreeding often enough to frustrate dedicated bird watchers.

Such uncertainty, however, doesn't bother Dolph Schluter of the University of British Columbia in Vancouver, who is one of those taking a new look at how species form. "Speciation is more interesting than `species,'" he says. When asked for a rough working definition of species, he gives a minor variation on the familiar theme: Members of a species share some distinctive look or make-up and don't breed a lot with outsiders.

Another illusion is that Darwin's explanation of natural selection settled the question of where new species come from. Darwin created a grand outline, but his intellectual heirs still struggle with just how certain parts of his theory work.

Natural selection, Darwin said, shaped species because the fittest survived and reproduced, passing along the genes that worked well to the next generation. That can explain how a branch of the family tree of life might bend toward, say, a capability to withstand drought or to reproduce earlier in the year. However, how in the world did that branch fork into two species?

Some butterflies, for instance, might happen to grow wings with colors that birds hesitate to eat. Those genes could spread quickly, since an unusually large proportion of their bearers would survive to reproduce. However, this shift doesn't create a new species. It just changes the old one.

What would actually divide one species into two? The scenario that dominated most of the 20th century came from the Harvard University ornithologist Ernst Mayr, who began formulating evolutionary theory in the 1930s. To split a species, Mayr called for a geographic barrier. A mountain or a glacier might do, for instance, for a butterfly.

Once some physical separation kept one part of the species from mating with the other, the two populations could diverge. Their genomes might drift apart randomly, or the change might be driven by the animals' adaptation to life on different sides of a glacier. Eventually, Mayr predicted, they'd differ so much, they couldn't breed even if the glacier melted. Mayr called this idea "allopatric speciation."

One of Mayr's students, Guy Bush, started a string of experiments during the 1960s that suggested an alternative to Mayr's theory. Bush worked with a fly species that he contends is splitting into two species without the drama of a glacier or a mountain. Instead, Bush says, the split comes from a lifestyle change.

Last year, former Bush student Jeffrey L. Feder of Notre Dame University in Indiana and his coworkers published the latest support for the fly's offbeat story.

Before the 18th century, the widespread New World fly Rhagoletis pomonella laid x its eggs and fed its young only in the small fruits, or haws, of hawthorn trees. As European apple trees multiplied in the United States, however, some of the flies did a little colonizing of their own. The flies that sampled apples laid their eggs there, and the next generation returned to apples instead of haws to mate.

In lab experiments, Bush and like-minded biologists have demonstrated genetic differences between the flies with the two fruit preferences. They argue that a new apple-loving species is branching off R. pomonella.

In the Oct. 12, 2000 NATURE, Feder and his coworkers reported on another difference that could be splitting the species. The chosen apple varieties ripen earlier than hawthorn haws, and this gap has advanced the apple-loving flies' lives by 3 to 4 weeks.

Such a leap forward brings mortal peril at the end of the season. A fly that goes into the ground early for its winter resting period might get confused by Indian summer and emerge just in time to freeze to death. However, Feder's tests show that early-to-bed, apple-eating flies prove less likely than the haw residents to snap out of their hibernation-like diapause during a burst of warm weather. Again, a genetic difference underlies the flies' new lifestyle.

Science may have caught another species in the act of doing an unconventional split, suggests Andrew Hendry of the University of Massachusetts in Amherst. He and his colleagues turned to Cedar River, a major tributary of Lake Washington in Washington. Some 100,000 to 350,000 sockeye salmon breed in the river, but the researchers realized that an offshoot of the river salmon around 1957 seems to have taken a hankering to breeding in the shallows of the lake.

In the 13 generations or so since then --barely a clock tick in evolutionary time--distinctive protein markers have shown up in each population, Hendry and his colleagues reported in the Oct. 20, 2000 SCIENCE.

Each sockeye group has its own look. More-petite females thrive in the lake, whereas the river females remain hefty enough to dig deep nests that withstand floods and other riverine mishaps.

The reverse seems to be true with males. The river males maintain a slim physique as befits creatures that battle currents. Life along the beach, however, seems to permit more flexibility in body shape. Researchers report that males in the lake's shallow water have grown unusually thick in profile. Female salmon prefer such shapes, and extremes of river currents no longer weed out the hunks.

These differences between river- and beach-favoring salmon somehow persist, although the populations still mix. At least a third of fish along the beach is recently arrived river stock, the researchers find. Yet even in this mixed group, river and beach types seem to prefer mates of their own kind, Hendry says.

Such a preference could represent an oncoming isolation in mating, one of the vital characteristics of emerging species. The force driving the split appears to be the fish's adaptation to a new territory, not the appearance of an absolute geographic barrier.

Another population that's adapting to slight differences in adjacent habitats is a wild fruit fly in a narrow canyon in Israel. Abraham Korol of the University of Haifa and his colleagues from the University of Bialystok in Poland last year described mating experiments with flies collected on opposite sides of the canyon.

The south-facing slope gets up to six times as much sun as the north-facing slope does. The canyon's walls at its base come within about 100 meters of each other, well within the flies' range.

Earlier work established that despite the short distance between the walls, northern and southern flies vary in more than location. They prefer different temperatures for laying eggs, tolerate different degrees of drought, and tend toward different life spans.

In the Oct. 31, 2000 PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES, the researchers described the mate choices of flies from various canyon settings. Flies in the lab accepted just about any partner from the same wall, even if the home elevations didn't match. However, the flies showed much less interest in potential mates from the other side, even from equivalent elevations.

Natural selection, while honing flies for better survival on their home wall, could also be revising mate choice, say the researchers. That combo, again, suggests a species in the making.

Other researchers of speciation have employed a different strategy. They've worked back from current species to their origins. Years of research on finches in the Galapagos Islands of Ecuador suggest that food choices affect beak shape, which restricts the kind of mating calls a bird can trill (SN: 8/26/00, p. 143). Today's 13 finch species on the islands, therefore, may have arisen in part from menu changes.

Something roughly similar may be going on with Canada's abundant three-spine stickleback fish, says Schluter. Seafaring ancestors moved into freshwater lakes when the glaciers receded at the end of the Pleistocene epoch. Today, six species inhabit three typical Canadian lakes--two species in each of the lakes Priest, Paxton, and Enos. A benthic species pokes along the lake bottom In each body of water, while a limnetic cousin hunts in open water.

In the Jan. 14 SCIENCE, Schluter and his colleagues reported more than 700 mating-choice experiments that mixed and matched all permutations of bottom-feeders and cruisers from the various lakes. The benthic species were at least twice as likely to spawn with another benthic species, even from a different lake, than with a limnetic species from home waters. Similarly, the limnetic species preferred other open-water sticklebacks as mates.

Schluter notes that evolution seems to have marched along in parallel in lakes that probably had no consistent connection.

With these and other unconventional examples before them, Mallet and his colleagues present an equally nontraditional scenario to explain the origin of two closely related Heliconius butterfly species. Heliconius melpomene and Heliconius cydno don't look like each other, but each resembles one of another pair of Heliconius species. All four species apparently taste terrible to birds.

Mallet's team proposes in the May 17 NATURE that the natural selection for nasties mimicking nasties powered the origins of H. melpomene and H. cydno.

Mallet and Christopher Jiggins at the Smithsonian Tropical Research Institute in Naos, Panama, analyzed the DNA of the four butterfly species. Members of the second pair, Heliconius erato and Heliconius sapho, have a lot more differences between their DNA than H. melpomene and H. cydno do and therefore seem to be the older species. Could the older ones have been the models that new mimics copied?

Natural selection seems to favor foul-tasting creatures that resemble other undesirables. The similarity gives the predators plenty of extra opportunities to learn that a particular fashion statement means, "Yuck." Mallet says he finds it easy to believe that some ancestors of the younger pair happened upon color variations that resembled the older species. The mimic's look spread fast because predators avoided butterflies sporting it.

"These things come up with new color forms all the time," Mallet says, indicating the multicolored butterflies fluttering across his Web site.

There's a problem, though. As the Web site shows, a lot of variety can flutter through a species without leading to a split. So, to argue that a color shift led to a new species, Mallet needed to find some link between the color variation and a barrier in mating.

The researchers now think they've found it. If mimicry fashions change, male sexual tastes must also evolve to keep up, so a male butterfly isn't as likely to court a female if her wing-bar color doesn't match his. This same-color attraction proved so strong that males in a lab experiment hovered hopefully over disembodied wings that the researchers set out or even over paper that researchers streaked with the right color of Magic Markers.

Mallet argues, therefore, that changes in color could trigger mating upheavals.

In considering some of the recent explorations of natural selection, Nick Barton of the University of Edinburgh asks, Why don't we see more species?

Barton raises the possibility that new species do form often, "but only rarely do they evolve sufficiently to be recognized by biologists." He adds that extinction, too, may turn out to be more rapid than scientists expect.

The world in which we live may be much more dynamic than we have realized, with species forming and failing in mere generations. Thank goodness that biologists' Web pages can be updated instantaneously.