Female orangutans are forced to copulate against their will more frequently than has been observed in any other mammal. Scientists have generally believed that this is because females spurn mating with inferior "unflanged" males. Rejected males have no chance to mate unless they use coercion--or so it was thought.

But new studies, using the first hormonal data from wild orangutans, collected noninvasively from the urine of females, suggests that orangutan sex may be a lot more subtle than meets the eye.

Although coerced to mate by most males they encounter, the females may have evolved advantages in their mating interactions to influence who gets to father their offspring and to protect the resultant babies from being killed by the males who didn't.

"Rather than being helpless victims of forced sex, female orangutans employ subtle counterstrategies," says Cheryl Knott, a Boston University anthropologist and National Geographic emerging explorer, who led the research.

Photo by Tim Laman

In the orangutan world males with flanges--or cheek pads--are also the dominant males. They defend territories and emit loud "long calls" to attract receptive females. The cheeky ornaments are perhaps attractive to females because they show that the orangutan has 'made it' to flanged male status, which perhaps indicates better genetic quality, and thus make those that have them good candidates to sire healthy offspring.

"Using the first hormonal data from wild orangutans, we show that around ovulation females preferentially encounter and mate with prime males whose impressive size and ornamentation are probable indicators of genetic quality," Knott and others write in their research paper, which was published by the biological research journal Proceedings of the Royal Society B.

Knott and her team came to this conclusion after observing hundreds of encounters between male and female wild orangutans in Gunung Palung National Park, West Kalimantan, Indonesia. The 220,000-acre (90,000-hectare) sanctuary contains a resident population of 2,500 wild orangutans.

Photo of Cheryl Knott in the field by Tim Laman

Orangutan mating is often lengthy and can include elements of both coercion and cooperation, the researchers noted. Nonetheless, by devising a method to rate sexual behavior, the scientists were able to determine when the females were primarily resistant to the males and when they were primarily receptive.

Almost a thousand urine samples were collected on filter paper from 10 of the females involved in the encounters, enabling the researchers to determine their reproductive status.

By combining all the data, the researchers found that ovulating females mated almost exclusively with prime males, perhaps in part because they engineered encounters with prime males by responding to the long calls made by those males.

Photo by Tim Laman

Unflanged males do not make long calls, so rather than "sit and wait" for mates as the prime males do, they must search for potential partners. When they find them, the data show, they often have their way, but typically and unbeknown to them when the females are not fertile and have little or no chance of becoming impregnated.

"Females mated most frequently with unflanged males overall, but they did so exclusively when conception risk was low," the scientists concluded. "A single peri-ovulatory [period of fertility] mating with a past-prime male was highly resisted, while non-periovulatory matings met less resistance, and pregnant matings were not resisted at all," they observed

Strategy of paternity confusion

Lowered mate selectivity outside of the peri-ovulatory period is consistent with another form of risk avoidance, the researchers said--"the anti-infanticide strategy of paternity confusion."

"This strategy, wherein females mate with potentially infanticidal males in order to increase their perception of paternity probability, is common in...primates as well as some species of carnivores and rodents," the researchers noted.

Photo by Tim Laman

Although infanticide has not been observed in wild orangutans, the scientists say that willingness to create confusion about paternity by mating during pregnancy, and avoidance of long calls from strange males, all indicate female strategies to reduce infanticide.

Said Knott, "Because orangutan don't have sexual swellings [a signal of fertility to potential mates in other female primates], we couldn't tell just by looking at them when they were ovulating. Now, with this new hormonal data, we see that females can use this lack of a visual signal to their advantage in their mating interactions."

The research paper Female reproductive strategies in orangutans, evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion, was published by by Cheryl Denise Knott, Department of Anthropology, Boston University, Melissa Emery Thompson, Department of Anthropology, University of New Mexico, Albuquerque, Rebecca M. Stumpf, Department of Anthropology, University of Illinois, Urbana-Champaign, and Matthew H. McIntyre, Department of Anthropology, University of Central Florida, Orlando.

The research was sponsored in part by the National Geographic Society's Committee for Research and Exploration.

The photos on this page are courtesy of Tim Laman. You might like to see more of his pictures of orangutans on the National Geographic Magazine Web site Orangutans in the Wild.

Watch this National Geographic video about Kalimantan's orangutans:

Female mosquitofish prefer males that have longer genitals, according to Australian research.

"This is a relatively novel result, as selection on genitals is generally thought to occur during or after copulation," say the authors of the study "Females prefer to associate with males with longer intromittent organs in mosquitofish," published this month in the science journal "Biology Letters." The research was done by Andrew Kahn, a graduate student at the Australian National University, and others.

According to the abstract of the paper, sexual selection is a major force behind the rapid evolution of male genital morphology among species.

"Most within-species studies have focused on sexual selection on male genital traits owing to events during or after copulation that increase a male's share of paternity," the abstract says.

"Very little attention has been given to whether genitalia are visual signals that cause males to vary in their attractiveness to females and are therefore under pre-copulatory sexual selection."

To look into this dearth of knowledge, the researchers "reduced" male mosquitofish genitalia to varying lengths, as shown in the photos on the right, then tested the reactions of the females.

"On average, female eastern mosquitofish Gambusia holbrooki spent more time in association with males who received only a slight reduction in the length of the intromittent organ (gonopodium) than males that received a greater reduction," the researchers observed.

"This preference was, however, only expressed when females chose between two large males; for small males, there was no effect of genital size on female association time."

Male mosquitofish do not court females, but rely on forced matings, according to a news statement about the research released by Biology Letters. "This means association preferences likely lead to mating biases. Thus, it appears size really does matter for these little fish."

Photos courtesy Australian National University 

Same-sex behavior is a nearly universal phenomenon in the animal kingdom, common across species, from worms to frogs to birds, according to a review of existing research, funded by the University of California, Riverside.

"It's clear that same-sex sexual behavior extends far beyond the well-known examples that dominate both the scientific and popular literature: for example, bonobos, dolphins, penguins and fruit flies," said Nathan Bailey, the first author of the review paper and a postdoctoral researcher in the Department of Biology at UC Riverside.

A female-female pair of Laysan albatross. Females cooperatively build nests and rear young when males are scarce, according to biologists at the University of California, Riverside.

Photo by Eric VanderWerf

However, the review paper points out, "same-sex behaviors are not the same across species," and that researchers may be calling qualitatively different phenomena by the same name.

"For example, male fruit flies may court other males because they are lacking a gene that enables them to discriminate between the sexes," Bailey said. "But that is very different from male bottlenose dolphins, who engage in same-sex interactions to facilitate group bonding, or female Laysan Albatross that can remain pair-bonded for life and cooperatively rear young."

An example of existing research was a study by Sara Lewis, an evolutionary ecologist at Tufts University, published in the Journal of Evolutionary Biology in November, 2008. Read the National Geographic News report about it: Homosexual Beetle Activity Offers Reproductive Edge. The picture above shows two beetles in a homosexual encounter.

Photo courtesy Sara Lewis, Tufts University

Published June 16 in the journal Trends in Ecology & Evolution, the review of existing research by Bailey and Marlene Zuk, a professor of biology at UCR, also finds that although many studies are performed in the context of understanding the evolutionary origins of same-sex sexual behavior, almost none have considered its evolutionary consequences.

    "Same-sex behaviors--courtship, mounting or parenting--are traits that may have been shaped by natural selection."

"Same-sex behaviors--courtship, mounting or parenting--are traits that may have been shaped by natural selection, a basic mechanism of evolution that occurs over successive generations," Bailey said. "But our review of studies also suggests that these same-sex behaviors might act as selective forces in and of themselves."

A selective force, which is a sudden or gradual stress placed on a population, affects the reproductive success of individuals in the population, a UCR news release about the research explained.

"When we think of selective forces, we tend to think of things like weather, temperature, or geographic features, but we can think of the social circumstances in a population of animals as a selective force, too," Bailey said. "Same-sex behavior radically changes those social circumstances, for example, by removing some individuals from the pool of animals available for mating."

Bailey, who works in Zuk's lab, noted that researchers in the field have made significant strides in the past two and a half decades studying the genetic and neural mechanisms that produce same-sex behaviors in individuals, and the ultimate reasons for their existence in populations.

Evolutionary Consequences

"But like any other behavior that doesn't lead directly to reproduction--such as aggression or altruism--same-sex behavior can have evolutionary consequences that are just now beginning to be considered," he said. "For example, male-male copulations in locusts can be costly for the mounted male, and this cost may in turn increase selection pressure for males' tendency to release a chemical called panacetylnitrile, which dissuades other males from mounting them."

According to UCR, the review paper:

• Examines work done to test hypotheses about the origins of same-sex behavior in animals.
• Provides a framework for categorizing same-sex behavior, for example, is it adaptive, not adaptive, occurs often, infrequently?
• Discusses what has been discovered about the genetics of same-sex behavior, especially in the model organism, the fruit fly Drosophila, and in human beings.
• Examines connections between human sexual orientation research, and research on non-human animals, and highlights promising avenues of research in non-human systems.

The reviewers expected the research papers they read for their article would give them a better understanding of the degree to which same-sex behaviors are heritable in animals, UCR said.

Genes vs. Environment

"How important are genes to the expression of these behaviors, compared to environmental factors?" Bailey said. "This is still unknown.

"Knowing this information would help us better understand how the behaviors evolve, and how they affect the evolution of other traits. It could also help us understand whether they are something that all individuals of a species are capable of, but only some actually express."

Bailey recommends that fellow evolutionary biologists studying same-sex behavior in animals adopt some of the research approaches that have been successful in human studies, UCR said.

"We have estimates, for example, of the heritability of sexual orientation in humans, but none that I know of in other animals," he said. "Scientists have also targeted locations on the human genome that may contribute to sexual orientation, but aside from the fruit fly, we have no such detailed knowledge of the genetic architecture of same-sex behavior in other animals."

Bailey and Zuk plan to begin experimentally addressing some of the many issues raised in their review.

Said Bailey, "We want to get at this question: what are the evolutionary consequences of these behaviors? Are they important in the evolution of mating behavior, or do they just add extra 'background noise'?

"We are pursuing work on the Laysan albatross, in which females form same-sex pairs and rear young together. Same-sex behavior in this species may not be aberrant, but instead can arise as an alternative reproductive strategy."

Related National Geographic News stories:

Homosexual Activity Among Animals Stirs Debate

Damselfly Mating Game Turns Some Males Gay

Rattlesnakes Show Strong Family Bonds, Study Says

Homosexual Beetle Activity Offers Reproductive Edge

Photo of two sea lampreys by Daymon J Hartley/Courtesy MSU

A synthetic chemical version of what male sea lampreys use to attract spawning females can lure them into traps and foil the mating process of the destructive invasive species, Michigan State University scientists say.

"The pheromone is expensive to synthesize," said Weiming Li, MSU professor of fisheries and wildlife. "But only a very small amount is needed for it to work successfully. It's very potent. Only a few hundred grams, less than a pound, would be used each year."

Sea lampreys are a scourge in the Great Lakes of the U.S., where they have no natural predators. They live in both salt and fresh water and likely found their way into the Great Lakes via shipping channels.

NGS photo of sea lampreys attacking Great Lakes fish by James L. Amos