What's Worth Saving?

Conservation biologists became so worked up at this summer's annual meeting that nearly 100 of them convened a special late session at a local pizza parlor. The previous 2 days of talk did not seem to have dimmed passions, and their debate, fueled by pepperoni and extra cheese, raged for 4 hours. The only reason it didn't last all night, or perhaps all week, was that the restaurant staff ushered the crowd out at 11:30 p.m.

The topic that caused so much excitement? How to define an evolutionarily significant unit. Really.

"It's not just eggheads arguing," says Sue Haig, coorganizer of the pizza seminar and a geneticist with the U.S. Geological Survey in Corvallis, Ore. The struggle to define the basic units of conservation "has huge consequences," she says.

If people want to preserve the living world, somebody has to decide what the significant parts are before conservationists can focus on saving them. An evolutionary significant unit, or ESU, represents the basic building block of conservation. It's generally considered to be a category smaller than a species.

Depending on which definition prevails, laws will shelter some organisms but not others. Old-growth forests will get closed to loggers--or they won't. Land will get cleared for housing developments--or it won't. Conservation dollars will flow, or they won't.

In one extreme scenario for defining an ESU, the squirrels of New York's Central Park might qualify. At the other extreme, a different definition might blend all the salmon in the Pacific Northwest.

The ESUs' impact stretches beyond the decision about whether to officially categorize a population as endangered. For example, if birds from two islands fall within the definition of an ESU, those from one island might get moved by conservationists to bolster an expiring population the other.

Scientists are currently so riled up over ESUs because the recent abundance of genetic information enables them to begin applying a decade's worth of theories.

"It's so important," Haig murmurs. Yet even she recognizes that many people outside scientific and conservation circles, especially outside of salmon country, have never heard of ESUs. But she predicts, "They're going to start hearing more and more."

The first widespread plea to define an ESU came more than a decade ago from zoo professionals alarmed by how few organisms they could preserve in their institutional arks. In making sense of the conservation crisis, they said, the old taxonomy just didn't cut it.

"There are no illusions that zoological parks can conserve but a very small proportion of biotic diversity," explained Oliver Ryder of the Zoological Society of San Diego in a 1986 paper usually cited as sparking the ESU debate. Biologists had estimated that institutions could save 925 kinds of mammals, birds, and reptiles. Even that estimate, barely a blip compared with 45,000 vertebrate species on the globe, he warned, was "optimistic."

The abundance of subspecies particularly troubled the zoo community. If humanity decided that zoos should save the tiger, which tiger would that be? The Sumatran? The Indian? Zoos need more than Noah's two animals to maintain a healthy, self-sustaining population of even one subspecies, and tiger taxonomists identify five.

This diversification goes beyond tigers. For example, 16 of 37 high-priority animals monitored by a conservation coalition called Species Survival Plan have subspecies.

However, Ryder noted, the term subspecies isn't applied consistently. In one extreme case, taxonomic descriptions of two subspecies were based on two individuals from the same litter. At the opposite extreme, muntjacs in India and China once ranked as separate subspecies but couldn't produce fertile hybrids.

The zoo professionals Ryder spoke for "willingly discarded the concept that all subspecies are equal," he reported. Rather than wait for the taxonomy of the living world to straighten out, Ryder, Bill Conway of the Bronx Zoo in New York, and a cohort of frustrated colleagues called for a new term. Biologists "ought properly to address the conservation of evolutionarily significant units (ESUs) within species," Ryder declared 14 years ago.

The zoo crowd may have had tigers in mind, but some of the first biologists to embrace ESUs were studying fish.

In 1990, petitions to list Pacific salmon as endangered started to swim up the regulatory channel at the National Marine Fisheries Service (NMFS). They tickled one of the most controversial provisions of the Endangered Species Act, the potential for listing not only a whole species but also a "distinct population segment" of vertebrates.

The law had included that provision since a 1978 revision, but "salmon introduced a whole new dimension," recalls Robin Waples, NMFS geneticist and another pizza-party coorganizer. "For grizzly bears or bald eagles, people might argue whether there's one or two or three distinct populations within the species, but not 500."

Yet that boggling possibility arose with salmon because they generally return to their natal streams to breed. The Pacific Northwest boasts "hundreds or thousands" of salmon streams, Waples points out. "Depending on how you interpreted distinct, you could argue--and some people did argue--that every little stream was distinct."

To cope with such prospects, Waples proposed that distinct population segments be considered the equivalent of ESUs. In 1991, he wrote the first guidelines for trying to define an ESU in the real world. Waples boiled down the concept to two criteria.

First, an ESU requires substantial reproductive isolation, that is, evidence that the organisms in the group find their mates among themselves instead of mixing with another group. The salmon of a single stream wouldn't often satisfy that criterion. Streamfuls of salmon tend to receive occasional strays from other streams' populations, which could recolonize the waterway should some disaster befall the current fish population.

The squirrels in Central Park, however, would probably meet this requirement for reproductive isolation, acknowledges Waples. During breeding season, they don't take the Long Island Railroad to find suburban mates, and the suburban squirrels wouldn't move in if there were park vacancies.

Don't worry, though, Waples says. He won't propose those squirrels for protection under the Endangered Species Act because they would probably flunk his second test for an ESU: representing "an important component in the evolutionary legacy of the species." The Central Park squirrels, he notes, don't differ much from their suburban relatives.

"We're not trying to identify which groups are going to be important in the future and which aren't," Waples says. Instead, he argues for determining the major units that make up a species and then saving as many of the building blocks as possible.

With this philosophy--and 8 years of study and debate--NMFS began designating Pacific salmon ESUs for the Endangered Species List. So far, the total has reached 25.

To define salmon ESUs, Waples called on any evidence he could find, from geographic to genetic. In 1994, however, the ESU world got a jolt from a proposed definition from Craig Moritz at the University of Queensland in Australia. This definition depended entirely on genetics.

The growing ease of sequencing DNA and improvements in family-tree analysis have lengthened the human view into a species' past, Moritz notes. He relies on such information to determine the significant branches of evolutionary history.

Mortiz looks initially at the DNA in mitochondria--organelles separate from a cell's nucleus and its DNA. The first of his two criteria for dividing a group into ESUs is that a family tree based on similarities in animals' mitochondrial DNA, or mtDNA, should show the proposed ESUs as full, separate branches, a situation scientists refer to as reciprocal monophyly.

To make sure that the mtDNA represents deep, strong branches, Moritz also suggested a second criterion: Nuclear DNA should show "significant divergence" between the ESUs.

For groups that just miss ESU status under these rules, Moritz proposed a lesser category: management unit, or MU. For these, he required only that certain versions of genes be more common in one MU than another.

Moritz's approach offers the allure of having clear-cut, quantifiable terms. Haig has not adopted this definition, but she recognizes the appeal: "You can go to court and defend it."

With so many factors to balance-defensibility in court, the galloping pace of genomics, the ancient philosophical abyss between taxonomists who split and those who lump--there's plenty of diversity among definitions.

Just this year, Robert Wayne of the University of California, Los Angeles has suggested picking out ESUs that are based on traits with adaptive value, such as an ability to withstand saltier water or dryer summers.

Definitions and variations just keep on coming. As Waples wearily says, "Your mother probably thinks you are evolutionarily significant."

How will these definitions work in the real world? Reports are starting to appear from biologists trying to translate theories into research that conservationists can use, especially for the inflamed problems of choosing creatures for legal protection. As Brian Bowen of the University of Florida in Gainesville puts it, "The Endangered Species Act forced biologists to get real."

One of the clearest examples of such reality comes from salmon. Following the approach described by Waples, fish biologists are already creating plans to try to bring back more than two dozen populations of the fish in the Pacific Northwest. However, Waples observes that if they had adopted the all-genetics, deep-branch ESU definition proposed by Moritz, "probably none of the salmon would make it."

The salmon runs of a region do differ genetically, Waples explains, but not as much as required by Moritz's definition. They show different frequencies of variations in particular genes, with some degree of overlap between populations but not the strong split that defines diverging lineages.

Accepting the Moritz definition "would have saved us a lot of work," Waples jokes. Instead of tracing out so many ESUs, salmon biologists would just have considered the all-or-nothing question of whether the entire group of Pacific salmon is endangered. However, deciding yes would have placed many Alaskan salmon runs, now relatively healthy populations, under the same fishing restrictions as the homes of faltering salmon in the Pacific Northwest.

Spotted-owl genetics has posed a difficult challenge to defining an ESU. Federal regulators have decided that two groups are threatened: the subspecies known as the northern and Mexican spotted owls. Biologists have petitioned to add the third subspecies, the California spotted owl. That's where it's starting to get tricky, Haig explains.

She and her colleagues have just finished a survey of mitochondrial and nuclear DNA in spotted owls, which they described at this summer's Society for Conservation Biology meeting. According to genetic evidence, Haig says, the northern spotted owl and its California cousins don't meet Moritz's criterion for a full ESU.

However, Haig sees strong evidence for proposing them as a lesser category, a management unit. She also finds evidence that the northern and California spotted owls are interbreeding where their ranges meet.

Depending on how someone interprets the data, the interbreeding might be taken as a sign of the need for listing the California owls. Haig suggests that habitat fragmentation is driving the California owls to seek refuge in more northerly woods where they may mate with the residents and lose their southern distinction.

Haig admits that her DNA evidence complicates the owl's legal situation. "We didn't mean to do it," she teases. "Science happens."

Even without evidence of interbreeding, the California gnatcatcher's conservation status might require reevaluation on the basis of recent genetic findings. Listed as a threatened subspecies, the small songbird has complicated property development along the Pacific coast from Los Angeles to the tip of the Baja California peninsula. The bird frequents lands covered with the rare vegetation known as coastal scrub. Along the coast, such real estate can sell for up to $3 million an acre.

On the basis of its color and other morphological characteristics, the California bird has ranked as one of five subspecies of gnatcatchers. Yet the first analysis of mitochondrial DNA finds nothing distinctive to separate it from the other gnatcatchers in Baja California, reports Robert Zink of the J.E Bell Museum in St. Paul, Minn., and his colleagues. In the October CONSERVATION BIOLOGY, they state that "the species as a whole is not threatened."

The matter awakens echoes of a recent, heated debate over turtle genetics. In 1999, Bowen and Stephen Karl published a genetic analysis of the rare, troubled black turtle. International lists considered it a distinct--and very endangered--species. However, according to the analysis of its mitochondrial DNA, "it wasn't a distinctive anything," says Bowen. Based on genetics alone, the turtle looked like part of an ESU of green turtles, which sport shells of various dark greens.

"We really got a lot of pressure to reinterpret those results," Bowen remembers. Turtle conservationists charged that such data would ruin the chance of protecting the black turtle. Bowen fears that an emphasis on ESUs invites such conflicts.

But Haig sees promise for using genetic information to turn the ESU into a finely targeted tool. For example, consider the southern torrent salamander. Reddishbrown with yellow bellies and about 4 inches long when full-grown, it dries out rapidly, even for a salamander. A creature of old-growth forests, it never ventures more than a few meters from swift, cold streams.

Earlier this year, the Fish and Wildlife Service had denied a petition to list the species as threatened, in part because the salamander seems stable in much of its range, Now, however, Steve Wagner, a student of Haig, is finishing a genetic analysis that might reopen the question.

Wagner found genetic markers that delimit a southern torrent salamander ESU in California, an area of conservation concern. This genetic information opens the possibility of designating one trouble spot as a distinct ESU.

"Now, they could just list that part," Haig says. That way, the healthy parts of the range wouldn't suffer under needless restrictions, a particularly delicate problem for a creature that's not exactly charismatic to the public. Haig shudders at the thought of reliving the debacle of a small, unbeloved fish stopping construction of a dam. The salamander "could have been another snail darter," she says.

The ESU debate highlights the upheaval in conservation biology as scientists try to work out how to take advantage of abundant genetic information.

"The salmon people have been doing this for years, but for the other people, I'd just like them to know what's out there," Haig says. "I don't think genetics is the only answer," she says, but "I do think they should pay attention to genetics more than they do."