The laysan albatross is a downy seabird with a seven-foot wingspan and a notched, pale-yellow beak. Every November, a small colony of albatrosses assembles at a place called Kaena Point, overlooking the Pacific at the foot of a volcanic range, on the northwestern tip of Oahu, Hawaii. Each bird has spent the past six months in solitude, ranging over open water as far north as Alaska, and has come back to the breeding ground to reunite with its mate. Albatrosses can live to be 60 or 70 years old and typically mate with the same bird every year, for life. Their "divorce rate", as biologists term it, is among the lowest of any bird.

When I visited Kaena Point in November, the first birds were just returning. There are about 120 breeding albatrosses in the colony, and gradually, each will arrive and feel out the crowd for the one other particular albatross it has been waiting to have sex with again. Once together, pairs will copulate and collaboratively incubate a single egg for 65 days.

Speaking on Oahu a few years ago as First Lady of the United States, Laura Bush – the wife of George W – praised Laysan albatross couples for making lifelong commitments to one another. But Lindsay C Young, a biologist who studies the Kaena Point colony, told me: "They were supposed to be icons of monogamy: one male and one female. But I wouldn't assume that what you're looking at is a male and a female."

Young has been researching the albatrosses on Oahu since 2003; the colony was the focus of her doctoral dissertation at the University of Hawaii, Manoa, which she completed last spring. (She now works on conservation projects as a biologist for hire.) In the course of her doctoral work, Young and a colleague discovered, almost incidentally, that a third of the pairs at Kaena Point actually consisted of two female birds, not one male and one female. Laysan albatrosses are one of countless species in which the two sexes look basically identical. It turned out that many of the female-female pairs, at Kaena Point and at a colony that Young's colleague studied on Kauai, had been together for four, eight or even 19 years – as far back as the biologists' data went, in some cases. The female-female pairs had been incubating eggs together, rearing chicks and just generally passing under everybody's nose for what you might call "straight" couples.

Young would never use the phrase "straight couples". And she is adamantly against calling the other birds "lesbians" too. For one thing, the same-sex pairs appear to do everything male-female pairs do except have sex, and Young isn't really sure, or comfortable judging, whether that technically qualifies them as lesbians or not. But moreover, the whole question is meaningless to her; it has nothing to do with her research. "'Lesbian,"' she told me, "is a human term."

A discovery like Young's can disorient a wildlife biologist in the most thrilling way – if he or she takes it seriously, which has traditionally not been the case. Various forms of same-sex sexual activity have been recorded in more than 450 different species of animals by now, from flamingos to bison to beetles to guppies to warthogs. Within most species, homosexual sex has been documented only sporadically, and there appear to be few cases of individual animals who engage in it exclusively. For more than a century, this kind of observation was usually tacked on to scientific papers as a curiosity, if it was reported at all, and not pursued as a legitimate research subject. Biologists tried to explain away what they'd seen, or dismissed it as theoretically meaningless – an isolated glitch in an otherwise elegant Darwinian universe where every facet of an animal's behaviour is geared towards reproducing.

"There is still an overall presumption of heterosexuality," the biologist Bruce Bagemihl told me. "Individuals, populations or species are considered to be entirely heterosexual until proven otherwise." While this may sound like a reasonable starting point, Bagemihl calls it a "heterosexist bias" and has shown it to be a significant roadblock to understanding the diversity of what animals actually do. In 1999, Bagemihl published Biological Exuberance, a book which pulled together a colossal amount of previous piecemeal research and showed how biologists' biases had marginalised animal homosexuality for the past 150 years – sometimes innocently enough, sometimes in an eruption of anthropomorphic disgust. Courtship behaviours between two animals of the same sex were persistently described in the literature as "mock" or "pseudo" courtship – or just "practice".

"What Bagemihl's book really did," the Canadian primatologist and evolutionary psychologist Paul Vasey says, "is raise people's awareness around the fact that this occurs in 'nature' – in animals. And that it can be studied in a serious, scholarly way." But studying it seriously means resolving a conundrum. At the heart of evolutionary biology, since Darwin, has been the idea that any genetic traits and behaviours that outfit an animal with an advantage – that help the animal make lots of offspring – will remain in a species, while ones that don't will vanish. In short, evolution gradually optimises every animal toward a single goal: passing on its genes.

In the past decade, however, Vasey and others have begun developing new hypotheses based on actual, prolonged observation of different animals, deciphering the ways given homosexual behaviours may have evolved and the evolutionary role they might play within the context of individual species. Different ideas are emerging about how these behaviours could fit within that traditional Darwinian framework, including seeing them as conferring reproductive advantages in roundabout ways. Male dung flies, for example, appear to mount other males to tire them out, knocking them out of competition for available females.

The point of heterosexual sex, Vasey said, no matter what kind of animal is doing it, is primarily reproduction. But that shouldn't trick us into thinking that homosexual behaviour has some equivalent, organising purpose. "All this homosexual behaviour isn't tied together by that sort of primary function," Vasey said. Even what the same-sex animals are doing varies from species to species.

It's possible that some homosexual behaviours don't provide a conventional evolutionary advantage; but neither do they upend everything we know about biology. For the past 15 years, for example, Vasey has been studying Japanese macaques, a species of two-and-a-half-foot-tall, pink-faced monkey. He has looked almost exclusively at why female macaques mount one another during the mating season. "It isn't functional," he told me; the behaviour has no discernible purpose, adaptationally speaking. Instead, it's a byproduct of a behaviour that does, and the supposedly streamlining force of evolution just never flushed that byproduct from the gene pool. "Evolution doesn't create perfect adaptations," Vasey said.

About two dozen birds were knocking around when Lindsay Young and I arrived at Kaena Point one afternoon. "I'm just writing down who's here," Young said, reading the numbers on the birds' leg bands and marking them on her clipboard.

Young and the biologist Marlene Zuk are now applying for a 10-year National Science Foundation grant to continue studying the female albatross pairs. One of the first questions they want to answer is how these birds are winding up with fertilised eggs. Typically, albatrosses fend off birds who aren't their mates. So Young has been trying to determine if males who arrive back at the colony before their own partners do are forcing themselves on these females or whether these females are somehow "soliciting" the males for sex. She was staking out Kaena Point on a daily basis, trying to watch these illicit copulations unfold for herself. This was Young's third year; so far, she'd only managed to see it happen twice.

Homosexual activity is often observed in animal populations with a shortage of one sex – in the wild, but more frequently at zoos. That's basically the situation at Kaena Point: there are fewer male albatrosses than females (although not every male albatross has a mate). Because it takes two albatrosses to incubate an egg, switching on and off at the nest, a female that can't find a male has no chance of producing a chick and passing on her genes. Quickly mating with an otherwise-committed male, then pairing with another single female to incubate the egg, is a way to raise those odds.

Still, pairing off with another female creates its own problems: nearly every female lays an egg in November whether she has managed to get it fertilised or not, and the small, crater-like nests that albatross pairs build in the dirt can accommodate only one egg and one bird. So Young was also trying to figure out how a female-female pair decides which of its two eggs to incubate and which to chuck out of the nest – if the birds are deciding at all, and not just knocking one egg out accidentally.

And these were only preambles to more questions. With the male of an albatross pair replaced by another female, every step of the species' normal, well-honed process for fledging a chick seemed suddenly to present a fresh dilemma. Ultimately, either the rules of albatrossdom were breaking down and the lesbian couples were booting up some alternate suite of behaviours, governed by its own set of rules, or else science had never thoroughly understood the rules of albatrossdom to begin with.

What animals do – what's perceived to be "natural" – seems to carry a strange moral potency: it's out there, irrefutably, as either a validation or a denunciation of our own behaviour, depending on how you happen to feel about homosexuality and about nature.

It's naïve to slap conclusions about a given species directly on to humans. But it's disingenuous to ignore the possibility of any connection. "A lot of zoologists are suspicious, I think, of applying the same evolutionary principles to humans that they apply to animals," Vasey told me. There's an understandable tendency among some scientists to play down those links to stave off ideological misreading and controversy. "But broadly speaking, research on animals can inform research on humans," Vasey says.

Since 2003, Vasey has been studying a particular group of men in Samoa. "Westerners would consider them the equivalent of gay guys, I guess," he told me – they're attracted exclusively to other men. But they're not considered gay in Samoa. Instead, these men make up a third gender in Samoan culture – neither men nor women, they are called fa'afafine. While there's no stigma attached to being fa'afafine in Samoan culture, homosexuality is seen as different and often repugnant, even by some fa'afafine.

In a paper published earlier this year, Vasey and one of his graduate students at the University of Lethbridge, Doug P VanderLaan, report that fa'afafine are markedly more willing to help raise their nieces and nephews than typical Samoan uncles. This offers support for a hypothesis that has been toyed around with speculatively since the Seventies, when the Pulitzer prize-winning biologist EO Wilson raised it: if a key perspective of evolutionary biology urges us to understand homosexuality in any species as a beneficial adaptation (if the point of life is to pass on one's genes), then maybe the role of gay individuals is to somehow help their family members generate more offspring. Those family members will, after all, share a lot of the same genes.

Vasey and VanderLaan have also shown that mothers of fa'afafine have more kids than other Samoan women. And this fact supports a separate, existing hypothesis: maybe there's a collection of genes that, when expressed in a male, make him gay but when expressed in a woman, make her more fertile. Like Wilson's theory, this idea was also meant to explain how homosexuality is maintained in a species and not pushed out by the invisible hand of Darwinian evolution. But unlike Wilson's hypothesis, it doesn't try to find a sneaky way to explain homosexuality as an evolutionary adaptation; instead, it imagines homosexuality as a byproduct of an adaptation.

"What we're finding in Samoa now," Vasey told me, "is that it's not an either-or." Neither of the two hypotheses, on its own, can neatly explain the existence, or evolutionary contribution, of fa'afafine. "But when you put the two together," he said, "the situation becomes a whole lot more nuanced."

"there's two mating right there," Lindsay Young called out. She read the female's leg band with her binoculars. "You just hit the jackpot," she told me. The bird was part of a female-female pair. The male had another mate.

The next morning, Young spotted a female from one of the female-female pairs calling to a male about 15 feet away. The female was standing right where the male and his partner usually build their nest. Her head was straight up in the air, and she clapped her beak animatedly. In Young's experience, it was rare for a bird to call so determinedly to another that's not her partner; this would definitely count as "solicitation", she said, if the two birds wound up copulating.

We sat on the ground expectantly for a while. Eventually, the male albatross took a few steps toward the calling female. Then it stopped and looked around.

"I'm not sure if he's taking her up on it, or just going, 'Why are you in my spot?'" Young said.

The male stopped again and tucked his beak into the feathers behind his neck. Then he turned around and retreated. "Well, his partner should be very proud of the self-control," Young said.

More than 4,000 miles across the Pacific, at a place called Taiaroa Head in southeastern New Zealand, two female Royal albatrosses (a related species) were building their nest. Later that winter, those two birds would become one of only a few known female-female pairs to successfully fledge a chick at Taiaroa Head in more than 60 years of continuous observation of the colony. The tourism board of Dunedin, a gay-friendly region of New Zealand, held a publicity-grabbing contest to name the "lesbian albatross" couple's chick.

A biologist working with the albatrosses at Taiaroa Head, Lyndon Perriman, seemed to bristle at the idea of naming any albatrosses – "They are wild birds," he wrote to me in an e-mail message. He noted that the female-female pair made for an inconvenient tourist attraction because their nest was not visible from any of the public viewing areas. It seemed fitting: people's ideas about the couple were riveting enough – it wasn't necessary to see the actual birds.