Not when cupid strikes

“Not when cupid strikes.”

That was Christine Drea’s response at the Animal Behavior meeting last summer. She had just given a talk on her latest study, showing the dramatic effects of hormonal contraception on the way lemurs communicate with the opposite sex¹. I was asking her what advice she gives to women about birth control. On the 50^thanniversary of the Pill, scientists like Drea were adding to the evidence that we might want to think twice about our widespread use of these drugs. The lemur research suggests that hormonal contraception could be replacing one “problem that has no name” – Betty Friedan’s idea of the dissatisfaction felt by modern women – with another².

Like many primates, ring-tailed lemurs have a complicated system of signaling to one another through scent. Males are able to detect the sex, fertility and even the identity of a particular female by smell alone³. At first glance, the connection to humans might seem far-fetched, since our noses are pretty poor compared to other mammals. But we are relatively well-endowed when it comes to scent production: humans have more scent glands on the surface of our skin than any other primate⁴.

We also have some surprising olfactory abilities lurking beneath the surface. The classic example is the T-shirt test. In the 1990s, researchers at the University of Bern in Switzerland gave a group of men T-shirts to take home, with instructions to sleep and sweat in them over the next two nights⁵. When women were later asked to sort the dirty T-shirts based on pleasantness of smell, they did something surprising. Their rankings came down to genes: the more genetically distinct a man was from a female rater, the more she liked his scent.

Biologists think this hidden talent might help us choose genetically compatible mates. The genes in question in the T-shirt study were part of what is known as the MHC complex. They encode a number of proteins that are used by the immune system to recognize invaders. Having diverse MHC genes might confer better immunocompetence, so it could be advantageous for your offspring if you choose a mate with MHC genes that differ from your own. The women in the study did not know it, but their noses led the way towards healthier kids.

Since then, the evidence that people use subtle scent cues when choosing a mate has grown. In some human populations, partner choice is related to MHC similarity^6,7. Another recent study found evidence that a woman’s scent-based preference for genetically dissimilar men might depend on her relationship status⁸.

Men might pick up on scent messages too. In a role-reversed version of the T-shirt test, men preferred the smell of women at the fertile peak of their menstrual cycles – and all they had to go on were bits of cotton that the women had worn under their armpits⁹. These signals may be automatic to us now, but perhaps we were aware of them at one point. Think of the way your mother smelled during childhood. Or being charmed by a sweetly scented newborn. We may not be conscious of it, but odour cues permeate our memories.

Evidence is also mounting that hormonal contraception can interrupt these deep-seated messages. One of the earliest clues was in the results of the first T-shirt study in the 1990s: women showed the opposite pattern if they were on the Pill, preferring the smell of men who were most genetically similar to them⁵. A more recent test supported this, showing that women’s scent preferences changed just months after starting on a new Pill prescription⁸. Some researchers have even speculated that the widespread use of hormonal contraception could be altering natural mate choice, in ways that are potentially detrimental¹⁰. When partners are too genetically similar, there may be a decreased ability to conceive, and the impact on offspring health could also be negative.

Enter the ring-tailed lemur: to understand the causes and consequences of these hormonal effects, we need a model system to conduct experiments that are difficult or impossible with humans. The scientists in Christine Drea’s lab have spent years working out a detailed understanding of lemur scent secretions, including how scent chemistry translates into signals of genetic identity. Coupled with the ability to train the animals at the Duke Lemur Center for behavioural experiments, the ring-tails were the ideal place to start.

In the present study, Drea and her coauthors Jeremy Crawford and Marylène Boulet looked at the effects of Depo-Provera injections, another commonly-used method of contraception among women today¹. The drug induced a striking change in the chemical odorants found in female genital secretions. These effects were not limited to signal strength. Contraception also altered the chemical profile of the signals, decreasing the uniqueness of individual females and altering the chemicals that normally signal lemur MHC genes. In other words, Depo-Provera has a dramatic effect on the secretions that give a female lemur her unique chemical “signature”.

Next, the research team looked at how these modifications affect male lemurs, by presenting males with bits of female-scented cotton on wooden dowels. When given the choice of a natural female odour versus the smell of the same female when she was contracepted, the males preferred her fertile scent.

The lemur study lays the groundwork for further investigation of these effects in humans. Does Depo-Provera alter odour secretions in women? And how do different hormonal contraceptive drugs compare? Do these effects ultimately influence mate choice decisions, relationship outcomes and fertility for human couples? Are there negative health effects for children conceived by women who were on hormonal birth control during courtship and partner choice?

In the meantime, Christine Drea’s cautionary advice suggests that we might want to take a contraception vacation when a relationship starts to get serious. When I assigned this paper as an essay topic in the Biology of Sex class at Queen’s University, this was the tack that most of my students took. I was disappointed that none took the opposite stance.

Why is messing with nature necessarily a bad thing when it comes to mating in humans? We are unique among our primate relatives, with babies that demand long-term investment from both mom and dad. Choosing a partner today is no doubt very different from the situation when our scent-based signals evolved. Depending on who you ask, there are many different ways to define success and satisfaction in modern relationships – but the one thing it is almost never based on is achieving high fertility.

By disrupting our innate scent preferences, hormonal contraception might even help us base our choices on aspects of compatibility more appropriate for modern life. What if contraception, by altering a female’s scent to make her less attractive to men initially, helps women weed out men who are only seeking short-term liaisons? Speculation at this point, but it should be considered, and the ring-tailed lemurs might help us get a better handle on what goes on under our noses.

References