Biology

8

Regulationof ovulation byhumanpheromones Kathleen Stern & Martha K. McClintock

Department of Psychology, The University of Chicago, 5730 Woodlawn Ave, Chicago, Illinois 60637, USA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Pheromones are airborne chemical signals that are released by an individual into the environment and which affect the physiology or behaviour of other members of the same species1. The idea that humans produce pheromones has excited the imagination of scientists and the public, leading to widespread claims for their existence, which, however, has remained unproven. Here we investigate whether humans produce compounds that regulate a specific neuroendocrine mechanism in other people without being consciously detected as odours (thereby fulfilling the classic definition of a pheromone). We found that odourless compounds from the armpits of women in the late follicular phase of their menstrual cycles accelerated the preovulatory surge of luteinizing hormone of recipient women and shortened their menstrual cycles. Axillary (underarm) compounds from the same donors which were collected later in the menstrual cycle (at ovulation) had the opposite effect: they delayed the luteinizing-hormone surge of the recipients and lengthened their menstrual cycles. By showing in a fully controlled experiment that the timing of ovulation can be manipulated, this study provides definitive evidence of human pheromones.

The existence of human pheromones was first suggested by the demonstration that women living together can develop synchro- nized menstrual cycles under specific conditions2–5. In rats, a similar process of ovarian synchrony occurs and is mediated by the exchange of two different pheromones6–7. One, produced before ovulation, shortens the ovarian cycle; the second, produced at ovulation, lengthens the cycle. These two opposing pheromones were predicted by a coupled-oscillator model of ovarian synchrony and shown by computer simulation to be sufficient for producing not only synchrony, but also the other observed effects of ovarian asynchrony and cycle stabilization7,8. By applying this model to humans, we demonstrate the existence of human pheromones and

identify a potential pheromonal mechanism for menstrual syn- chrony, as well as for other forms of social regulation of ovulation.

We found that the recipients had shorter cycles when receiving axillary compounds produced by donors in the follicular phase of the menstrual cycle ( 2 1:7 6 0:9 days) and longer cycles when receiving ovulatory compounds (þ1:4 6 0:5 days), which represent significantly different opposite effects (Fig. 1). The response was manifest within the first cycle, rather than requiring three cycles of exposure as suggested previously2,7, and the sequence of compound presentation had no effect. The two types of axillary compounds had effects that were significantly different from each other and from the baseline cycle. The carrier had no effect on cycle lengths of the control recipients. In five of the cycles, women had mid-cycle nasal congestion, which could have prevented their exposure to pheromones; including these cycles in the analysis made the results slightly less robust (follicular compounds: 2 1:4 6 0:9 days; ovu- latory compounds: þ1:4 6 0:5 days; ANOVA: follicular versus ovulatory compounds Fð1; 18Þ ¼ 4:32, P # 0:05; cycle 1 versus

letters to nature

NATURE | VOL 392 | 12 MARCH 1998 177

Cycle 1 Cycle 2

Follicular pheromone

Carrier controls

Ovulatory pheromone

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Figure 1 Effect of axillary compounds, donated by women during the follicular or

ovulatory phases of their menstrual cycle, on the menstrual cycle length of

recipients. This was measured as a change in length from the recipient’s baseline

cycle with a repeated measures analysis of variance: within-subject factors were

follicular versus ovulatory compounds ðFð1; 18Þ ¼ 5:81;P # 0:03Þ and cycle 1

versus cycle 2 of exposure (not significant, NS); the between-subjects factor

was: order of presentation (NS); all interactions between factors were not

significant). Cycles were shorter than baseline during exposure to follicular

compounds (t ¼ 1:78, P # 0:05, 37 cycles) but longer duringexposure to ovulatory

compounds (t ¼ 2:7, P < 0:01, 38 cycles). Cycles during exposure to the carrier

were not different from baseline (t ¼ 0:05, P # 0:96, 27 cycles).

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Follicular phase

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r = 0.55 P ≤ 0.0001

Luteal phase

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r = 0.24 P ≤ 0.004

Menses phase

Phase length (days)

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Figure 2 Each of the three phases of the menstrual cycle are variable in length (x-

axis) and correlate with overall menstrual cycle length (Pearson’s r), establishing

each as a potential mediator of the effects of axillary compounds. Menses phase

(X, day 1 to the end of menses); follicular phase (O, day after menses to the day

before the preovulatory LH surge); luteal phase (B, three days after the LH surge

to day before menses, verified to be functional by ovulatory levels of

progesterone glucuronide (PG) and rise in basal body temperature. The ovulatory

phase is a fixed 3 day interval (day of LH surge onset plus 2 subsequent days).

Note that the luteal phase of these normal subjects is significantly more variable

than the 12–16-day range described in standard medical texts.

Nature © Macmillan Publishers Ltd 1998

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