All in the Family

For some animals, the ideal mate is a brother, sister or cousin

In late March, as winter unclenches its frigid grip on upstate New York, a spotted salamander’s thoughts turn fleetingly to love. After early spring rains soak the forests where the salamanders live, thousands of the slimy little creatures descend on small vernal pools for the amphibian equivalent of an orgy.

SPOTTY FAMILY. Each spring, spotted salamanders (Ambystoma maculatum) descend on Northeastern ponds to breed for just a few days. Many mate with cousins. H.H. Greene

BABYSITTER. For cichlids native to streams in Western Africa, brothers and sisters make ideal parents. iStockphoto

“It’s sort of a frenzy,” says Kelly Zamudio, an ecologist at Cornell University who studies the five-day ritual. “All these males are competing with each other and nudging each other and putting down sperm as quickly as they can.”

Spotted salamander sex, it turns out, is an evolutionary Easter egg hunt. Males lay scores of sperm-filled pouches onto the leaves and twigs that litter the pond floor, while females pluck away the sperm to fertilize their eggs. The pouches—called spermatophores—look like little soccer trophies, “but made out of jelly,” Zamudio says. A female often collects more than a dozen trophies left by various males. Then, “she walks away from this aggregate of males who are going crazy putting down their spermatophores. She’s got everything she needs.”

Zamudio and former student Chris Chandler wanted to know which males passed on their genes most successfully. Since spotted salamanders don’t copulate, females have no direct way to assess the potential fathers of their children. So the scientists analyzed DNA collected in the field from males, females and larvae and came to a surprising conclusion.

“She seems to be fertilizing her eggs with gametes of animals that are a little bit more closely related to her,” Zamudio says. In other words, the salamanders are inbreeding.

In fact, many animals prefer to mate with their brothers, sisters and other relatives. Humans, too, might even favor kissing cousins. Zamudio and Chandler published their findings last month in Molecular Ecology. Other researchers have uncovered the same surprising trend in species of fish, birds and beetles.

Long stigmatized because of the birth defects that often afflict children of closely related couples, inbreeding sometimes comes at a high price. Humans and other animals have two versions of most genes—one from mom and one from dad. Inbreeding ups the chances that a child will inherit two versions of a disease-causing gene. The son of first cousins, French artist Henri de Toulouse-Lautrec suffered from an inherited form of skeletal dysplasia that left the artist with short legs and weak bones. And consanguinity among royal families in 19th century Europe contributed to a high incidence of the blood disease hemophilia. England’s Queen Victoria was a carrier of the disease, and hemophilia scourged the royal houses of Spain and Russia, as well.

But inbreeding can have its perks, says Patrick Bateson, a biologist at the University of Cambridge in England. Many organisms might have slight genetic tweaks or adaptations tuned to their local habitats, and too much genetic mixing with outsiders can dilute these adaptations, he says. For instance, horticulturalists self-fertilize plants to preserve genes that confer advantages like pest resistance. “What you see then is a kind of trade-off between the costs of inbreeding and the costs of outbreeding,” Bateson says. “It’s not that inbreeding as such is beneficial. It’s getting the balance between inbreeding and outbreeding that is important.”

Zamudio’s analysis of spotted salamander mating hints at such a trade-off. Comparing the DNA of fathers, mothers and larvae, she and Chandler found an intermediate amount of inbreeding—at the level of first cousins, on average. Despite having hundreds of possible mates to choose from, females tended to fertilize their eggs with sperm from related males. The females don’t choose spermatophores at random, and they certainly don’t avoid their kin, she says.

One question Zamudio hopes to answer is how female salamanders tell a cousin’s spermatophore from the hundreds of others. She says the females might detect some genetically determined pheromone wafting off the sperm. Another possibility is that sperm from related males outcompetes sperm from less-related males to fertilize eggs.

She also doesn’t know why her spotted salamanders appear to prefer to inbreed. The amphibians might use inbreeding to hold onto local genetic adaptations, she says. “If a male moves from one pond to a neighboring pond, he may carry with him genes that are just slightly deleterious for the pond where the female lives—just slightly off—so she would benefit from actually choosing males from her own pond because they’re best adapted.” Zamudio has noted tiny differences among the DNA of animals from different ponds.

When brothers are better

Though spotted salamanders frequently inbreed, Zamudio hasn’t tested whether the offspring pay an evolutionary toll. Ambrosia beetles, however, clearly benefit from inbreeding. The tiny Asian insects, which invaded Europe beginning in the 1950s, colonize newly fallen trees in the early summer. Females carve out chambers, where they cultivate gardens of fungus to nourish their young. Brothers and sisters tend to mate, but males occasionally strike out to a nearby chamber on the same log.

To see if the consanguineous couples spawned less fit children—a phenomenon called inbreeding depression—Katharina Peer and Michael Taborsky of the University of Bern in Switzerland mated related and unrelated ambrosia beetles (Xylosandrus germanus) in specially designed laboratory chambers, complete with test tube–grown fungus. After the couples laid their eggs, the team allowed some to hatch and eventually mate, providing the researchers with two generations of insects in which to look for the ill effects of inbreeding.

The inbred beetles fared no worse than outbred insects, and the eggs produced by brother-sister pairs were likelier to hatch than the eggs of unrelated pairs. The researchers don’t know why brothers and sisters produce more progeny, but inbreeding might help create new species. Ambrosia beetles are one of 1,200 closely related species, and inbreeding may cement the slight genetic differences between the insects, the researchers suggest.

Animals may gain other benefits from inbreeding. Several years ago, Harald Kullmann, an ecologist at the University of Bonn in Germany, was studying how brightly colored cichlid fish, Pelvicachromis taeniatus, choose mates. The fish, native to small streams and rivers in Nigeria and Cameroon, are monogamous and both parents care for the young. Males typically defend miniature caves that serve as cichlid nurseries from predators.

Kullmann expected visual traits like color and size to determine who paired with whom. His team re-created the caves to test this idea and found that the fish preferred to mate with brothers and sisters. Kullmann’s team also found that fathers from brother-sister couples spent more time, on average, defending their caves and that both parents tended to pay more attention to their kids than unrelated couples. The finding suggests that inbreeding may promote good parenting by cichlids.

“Couples which are full siblings are more cooperative in brood care,” he says. “In these fishes, the males and females stay with the offspring for several weeks and guard them—they defend them—and there’s less aggression between full siblings.”

Laboratory experiments such as Kullmann’s offer the control needed to test whether animals prefer to mate with kin. But, as with beetles, inbreeding in the wild might be a result of necessity, not choice. Such might be the case with extremely isolated, dispersed or small populations. Given no other options, animals will happily breed with siblings, cousins, even parents. More surprising are the beasts that choose kin when they have ample access to healthy strangers in the wild.

A colony of great frigate birds in the French Frigate Shoals near Hawaii offers an example. The birds, with 2-meter wingspans, can drift up to 2,000 kilometers in search of a fishy meal. In 2004, ecologists found that the tropical birds tended to mate with relations. The frigate couples, on average, shared more blood than second cousins. The birds had access to plenty of potential mates, and the researchers think the birds actively choose to keep it in the family.

Kissing cousins

It’s no secret that humans interbreed too. Charles Darwin married his first cousin, Emma Wedgewood. More recently, a 1997 study of Pakistani hospitals found that three out of five marriages were between first cousins, while a study of one South Indian city found that one-fifth of marriages occurred between uncles and nieces and a third between first cousins.

But close inbreeding comes with a high cost for humans. “First cousins, when they have babies—it’s like a textbook example—tend to have higher mortality,” Zamudio says. In contrast, scientists know little about the effects of inbreeding between more distantly related couples—third cousins and beyond. But recent work on Icelanders suggests that some family loving might be a good thing.

A team of researchers at the Icelandic firm deCODE genetics sifted through 165 years of genealogy data from 160,000 couples. Pairs who shared a great-great-grandparent—third cousins—tended to have more children and grandchildren than did more distantly related spouses. For instance, women born between 1925 and 1949 who married third cousins had 3.3 kids and 6.6 grandkids, on average. Women who married eighth cousins bore 2.5 children and 4.9 grandchildren. Yet the study, published in the Feb. 8 Science, doesn’t give carte blanche to forbidden love. More closely related couples—first and second cousins—had fewer children than less-related couples, and the inbred kids died at a younger age.

“That was a very nice confirmation of work people have done with other animals,” says Bateson, who showed in the 1970s that Japanese quail prefer first cousins over brothers and sisters and over less-related birds. He and other researchers stress that animals in the wild must balance the pluses and minuses of inbreeding and outbreeding to do best for their children.

Given this evolutionary calculus, some researchers wonder whether biologists should come up with a new term for the phenomenon. “We shouldn’t call it inbreeding,” Zamudio says, only half jokingly. “Inbreeding conjures all these negative things—people with three eyes.” Her suggestion: genetic complementation.

More than Skin Deep

Specific gene helps animals find healthy mates

When seeking out that special someone, humans and other animals gauge a myriad of social and biological cues, from scent to mating call to income. A set of genes that’s involved in detecting infections seems to help animals assess the relatedness of a potential mate. Called the major histocompatibility complex, these genes help vertebrates to battle viruses, bacteria and parasites.

The MHC genes encode proteins that latch onto molecules made by pathogens, keeping the immune system alert. Numerous studies have suggested that animals judge potential mates by their MHC genes. For instance, female stickleback fish tend to choose males with different versions of MHC genes. The extra diversity allows their offspring to recognize a wider variety of pathogens, which could boost survival.

Humans probably use MHC to discriminate among mates, too, says Craig Roberts, an evolutionary psychologist at the University of Liverpool in England. In 2005, Roberts found that women prefer the faces of men who had the same MHC genes. Another report found that women fancy the smell of sweaty T-shirts from men with MHC genes similar to their own, though other studies have come to the opposite conclusion, he notes. No matter the effect of MHC among human mate choice, all animals must balance genetic quality with compatibility, Roberts says. “We all prefer different people,” he says. “We can agree that Brad Pitt and Jennifer Aniston are attractive, but when it comes down to it, I might prefer Gwyneth Paltrow.”

From the Nature Index

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