SEX in the DARK: a REVIEW of the LITERATURE and IDEAS CONCERNING CONCEALED OVULATION in the HUMAN FEMALE by Ashley A.E. Clarke T

SEX IN THE DARK: A REVIEW OF THE LITERATURE AND IDEAS CONCERNING CONCEALED OVULATION IN THE HUMAN FEMALE

Ashley A.E. Clarke

Thesis

submitted in partial fulfillment of the

requirements for the Degree of

Bachelor of Science with

Honours in Biology

Acadia University

April, 2006

This thesis by Ashley A.E. Clarke

is accepted in its present form by the

Department of Biology

as satisfying the thesis requirements for the degree of

Bachelor of Science with Honours

Approved by the Thesis Supervisor

______(Marlene Snyder) Date

Approved by the Head of the Department

______(Dan Toews) Date

Approved by the Honours Committee

______Date

I, Ashley A.E. Clarke, grant permission to the University Librarian at Acadia University to reproduce, loan or distribute copies of my thesis in microform, paper or electronic formats on a non-profit basis. I however, retain the copyright in my thesis.

______Signature of Author

______Date

Acknowledgements

Many people contributed to this thesis; however, the following individuals and sponsors require especial thanks. I would like to express my gratitude to Dr. Marlene Snyder; your enthusiasm, patience, and help were essential to every step of creating this thesis and I owe you a profound thank you. I am also grateful for all of the support and knowledge that I have received over the past four years from the Department of Biology at Acadia

University. I would also like to thank my family for your encouragement and love. I would like to thank the Acadia University Faculty Association for funding my research.

Finally, I am also thankful for the generous support I received from the Dr. J. Murray

Beardsley Research Scholarship in Biology which assisted me with the completion of my research during the summer months.

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Table of Contents List of Tables ...... v List of Figures...... vi List of Appendices ...... vii Abstract...... viii Introduction...... 1 Chapter 1: the human female menstrual cycle...... 1 Generalities of the human menstrual cycle...... 1 Hormone regulation of the human menstrual cycle...... 2 Follicular development ...... 3 The midcycle hormone surge and resulting ovulation...... 6 The progression of the corpus luteum...... 8 Menses and the proliferative phase...... 9 Other important hormones ...... 11 Variation in the menstrual cycle ...... 12 Menstrual cycle irregularities ...... 13 Chapter 2: Is ovulation truly concealed? ...... 15 Clarification of the Basic Concepts: loss of estrus, continual sexual receptivity and concealed ovulation ...... 15 Is Ovulation Truly Concealed? ...... 17 Why has ‘novel’ become the new buzz word in science? ...... 20 Research Studies: The Proof of Concealment ...... 22 Are women correctly aware of ovulatory events? ...... 22 Do people in societies which more closely resemble ancient humans have an awareness of ovulation? ...... 26 Do forms of sexual behaviour increase in response to ovulation, indicating times of maximum fertility?...... 28 Is human ovulation detectable by pheromones? ...... 35 Menstrual Synchrony and its relevance ...... 39 Chapter 3: Primates and their reproductive cycles ...... 41 Why study primates?...... 41 Technical issues ...... 42 Displays related to ovulation: Behaviour and Sexual Swellings ...... 43 The connection between sexual swellings and multimale groups ...... 45 Concealed ovulation in primate species...... 48 Can Phylogeny explain concealed ovulation? ...... 52 Can social structures explain concealed ovulation?...... 52 The application of primate research to the study of concealed ovulation...... 53 Chapter 4: theories explaining the significance of concealed ovulation...... 55 An introduction to the proto-human ...... 55 Overview of theories...... 55 Concealed ovulation and its evolution...... 59 Conclusion ...... 64 References...... 66 Appendices...... 77

List of Tables

Tables Page

1 The degree of sexual swelling and menstruation in 32 primates 49 representatives from seven primate families (Data regarding menstruation and swelling from Hrdy and Whitten, 1987; Hutchins, 2003. Data on mating systems from Lindenfors, 2002).

2 Reproductive features of six extant primate species including 52 whether or not concealed ovulation is present, the average length of an ovulatory cycle, the length of female receptivity to sexual encounters, and the duration of the breeding season. Sources are listed.

3 Reproductive characteristics of females from six extant primate 53 species including body mass, age of sexual maturity, length of gestation, number of offspring produced per reproductive events and the interval between reproductive events. Data from Lindenfors (2002) with the exception of body mass data which were collected from Lindenfors and Sillen Tullberg (1998).

4 Social structures of six extant primate species. 53

List of Figures

Figure Page

1 Folliculogenesis begins with the development of the oogonia from 6 undifferentiated cells and the association of these cells with those of the surrounding environment. This follicle advances from the stages of a primordial follicle pool to the primary follicle and finally into the preantral follicle which is composed of both granulosa and theca cells. Pictorial representation of follicles reprinted from Henry and Norman (2003: p. 657).

2 Hormone concentrations throughout the menstrual cycle. A 7 sudden increase in concentration of LH, FSH and estradiol is evident at the time of ovulation. Figure reprinted from Pocock and Richards (1999: p. 447).

3 Follicular development, hormone levels and endometrial changes throughout the menstrual cycle shown in relation to each other during a standard 28-day menstrual cycle. The cycle is divided into both follicular and luteal phases as well as the corresponding menstrual, proliferative, and secretatory phases.

4 Phylogenetic relationships among the major groups of extant 55 primates. Reprinted from Sillén-Tullberg and Møller (1993).

5 Chronological placement of ten predominant theories explaining 59-60 the evolutionary significance and adaptive advantages of concealed ovulation. Each theory is identified by the last names of its author and summarized by a brief statement elucidating its primary arguments.

List of Appendices

Appendix Page

A An annotated bibliography of several of the resources used 77 throughout this thesis and their relevance to the study of concealed ovulation.

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Abstract

Most mammalian females engage in sexual activity during distinct periods of receptivity termed estrus, which coincides with the period of fertility. Sexual activity in human females, however, is characterized by the absence of specific times of receptivity or proceptivity, and by the lack of advertised fertility (via either behavioural or physical cues), which is dubbed “concealed ovulation”. Although strikingly rare, concealed ovulation is not confined to human females, yet there has been little investigation of its occurrence in other organisms. An examination of the literature has revealed several prominent theories hypothesizing the adaptive value of this phenomenon in humans: a strategy to obtain parental care, prevention of infanticide by reducing male-male competition, female avoidance of copulation during estrus to evade pain and death associated with child-birth, increasing cuckoldry of males after established monogamy, female acquisition of meat from successful male hunters, psychological self-deception, preference for prolonged paternal investment over mate quality, increased paternal care, and the result of structural and functional changes related to bipedalism. Interest in concealed ovulation has generated a wealth of research about such diverse topics as primate mating systems, human pheromones, women’s perceptions of their time of fertility, menstrual synchrony, and coital frequencies. To date, consensus regarding the evolutionary origins of concealed ovulation as well as its role in human sexual adaptation continues to be contested. Avenues for future research include obtaining more extensive data on primate reproductive cycles and behaviour, providing a more complete phylogenetic understanding of concealed ovulation, and a meta-analysis of literature

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suggesting possible cues indicating maximum fertility in humans, which would facilitate examination of the validity of the research available.

Introduction The concealment of ovulation refers to a general unawareness of fertility as well as the lack of any behavioural or physical cues linked to the increase in fertility.

Concealed ovulation is a reproductive oddity limited to only a four primate species including humans. This thesis outlines the primary components of concealed ovulation as well as the theories explaining this phenomenon.

It becomes evident as one reads through this body of research that the study of concealed ovulation is limited by several factors. First, studies concerning primate reproduction and its phylogenetic significance are scarce. Additionally, the biased publication of positive findings allows concepts that are not entirely representative become a feature of mainstream theory.

Overall, the study of concealed ovulation requires the integration of a broad range of topics, several of which have been included in this thesis. I begin with a summary of the human menstrual cycle, and continue on to clarify whether concealed ovulation truly exists in humans. I discuss primate reproduction, and then I review the prominent theories explaining the evolution of concealed ovulation and its significance. Concealed ovulation is an extensive area of study that requires the investigation of many interdisciplinary topics.

Chapter 1: the human female menstrual cycle Generalities of the human menstrual cycle The number of eggs produced by a female is species-specific. In female humans, women produce a single gamete, the oocyte, each month from the onset of menarche to menopause (Namnoum and Hatcher, 1998). Although seven million oocytes are present

in each ovary of human females during the twentieth week of gestation, the majority of these oocytes will not be viable and will be discarded (Eppig et al., 1997).

The reproductive process of the human female is cyclic, and the beginning of the cycle is arbitrarily designated as the first day of menses. Based on this it takes approximately 28 days for an average cycle to return to the first day of menses.

Ovulation occurs approximately midcycle on day 14.

The human menstrual cycle can be separated into the ovarian cycle and the uterine cycle (Palter and Olive, 2002) which can both be further subdivided. The first fourteen days of the ovarian cycle are considered to be part of the follicular phase, while the last fourteen days comprise the luteal phase. The uterine cycle is divided into the proliferative and secretory phases, which correspond to the divisions of the ovarian cycle

(Palter and Olive, 2002). Some researchers choose to divide the menstrual cycle into four categories based on the physiological changes which transpire. The other possible divisions of the menstrual cycle are the following four phases: the follicular (pre- ovulatory), ovulatory, luteal, and menstrual (Namnoum and Hatcher, 1998).

Hormone regulation of the human menstrual cycle

Regardless of the divisions subjectively assigned to each phase of the menstrual cycle, the events described have been verified empirically. The regulation of the menstrual cycle is dependent on hormones produced in the hypothalamus, pituitary, and ovary (Namnoum and Hatcher, 1998). Gonadotropin-releasing hormone (GnRH) is produced in the arcuate nucleus in the hypothalamus (Palter and Olive, 2002), and can be found in all vertebrate and some invertebrate brains, in which it regulates reproduction in both males and females (Temple et al., 2003). GnRH is a decapeptide that is secreted in

pulses through the portal vessels (Palter and Olive, 2002). The delivery of GnRH to the anterior pituitary stimulates the production of the gonadotropins Follicle-stimulating hormone (FSH) and Leutinizing hormone (LH) (Namnoum and Hatcher, 1998). The pulsatile nature of GnRH release from the hypothalamus is compulsory for proper gonadotropin secretion (Knobil, 1992), as the half-life of GnRH is only 2 to 4 minutes due to prompt proteolytic cleavage (Palter and Olive, 2002). Based on animal studies, secretion of GnRH in a consistent concentration will not properly stimulate the pituitary and the production of the gonadotropins ceases (Knobil, 1992). The pulses of GnRH occur every 60 to 90 minutes depending on the stage of the menstrual cycle (Namnoum and Hatcher, 1998). Both FSH and LH are secreted in a pulsatile fashion in response to the oscillations of GnRH (Namnoum and Hatcher, 1998). Both FSH and LH are structurally similar, as the two glycoproteins share the same alpha subunit and only vary in the structure of their beta subunits (Palter and Olive, 2002).

Follicular development

GnRH, FSH, LH, estrogens, and progesterone play an integral role in the endocrine cycle, which in turn induces changes in both ovarian and endometrial histology

(Palter and Olive, 2002). However, the initial recruitment and growth of a cohort of follicles occurring over several months is gonadotropin-independent (Palter and Olive,

2002). During this stage of follicle development, the primordial follicle is comprised of an oocyte suspended in the diplotene stage of the first meiotic prophase that is concealed by a layer of granulosa cells (Eppig et al., 1997). Once a cohort of follicles is recruited, ovarian follicular development transitions from being completely independent of gonadotropins to relying on production of FSH (Eppig et al., 1997). FSH determines

follicular differentiation and growth, specifically, oocyte growth and the development of additional layers of granulosa cells into a multilayer of cuboidal cells (Palter and Olive,

2002).

Gonadal steroids are low when the menstrual cycle commences due to production of progesterone and inhibin by the corpus luteum during the luteal phase of the previous cycle (Palter and Olive, 2002). As the previous cycle proceeds and the corpus luteum declines, FSH levels rise, further stimulating proliferation of the granulosa cells within a cohort of follicles (Palter and Olive, 2002). The cohort of primordial follicles are converted to secondary follicles as the oocytes continue to mature and produce a glycoprotein-rich substance, the zona pellucida, which separates the developing oocyte from the granulosa cells (Palter and Olive, 2002). This development of the oocyte marks the transformation of the follicle into a preantral follicle in which miotic division of the granulosa cells persists (Palter and Olive, 2002). At some point in granulosa cell maturation, the theca cells, located in the stroma surrounding the granulosa cells, proliferate (Palter and Olive, 2002).

As preantral follicles develop, interplay between the theca cells and the granulosa within the developing follicle leads to estrogen production. LH induces the theca cells, located in the ovary, to produce the androgens testosterone and anderostenendione

(Namnoum and Hatcher, 1998). These androgens diffuse from the theca cells to the granulosa cells within the follicle; there the androgens are converted into estrogens by the enzyme aromatase (Namnoum and Hatcher, 1998). The conversion from androgens to estrogens is essential for growth of the follicle and is dependent on increasing sensitivity of granulosa cells to FSH (Speroff and Fritz, 2005). The subdivision and

compartmentalization of estrogen synthesis between the theca and granulosa cells is necessary as the granulosa cells possess the receptors needed for FSH stimulation, but lack some of the enzymes required to produce estrogen and thus must employ androgens as a substrate for aromatization and estrogen production (Palter and Olive, 2002).

The synergistic production of estrogens by the developing follicles create a microenvironment within the follicle that further aids in development; as well, estrogen is secreted into the circulatory system (Palter and Olive, 2002). Additionally, inhibin, a protein consisting of both alpha and beta subunits, is synthesized in the theca and granulosa cells of the follicles (Namnoum and Hatcher, 1998). There are two known forms of inhibin differing in their beta subunits, inhibin-A and inhibin-B (Speroff and

Fritz, 2005). Inhibin-B is secreted into the circulation system, affecting the suppression of FSH from developing follicles and subsequently acting as a primary mechanism influencing follicle dominance (Speroff and Fritz, 2005). It is now that a dominant follicle must be selected by a mechanism which remains ambiguous, while the others undergo atresia, which is the degeneration and resorption of ovarian follicles before maturation (Eppig et al., 1997). Rising levels of estrogen produced within follicles act as negative feedback on secretion of FSH (Palter and Olive, 2002). Depression in FSH inhibits further follicular growth, except within the dominant follicle which has a rich microenvironment of estrogen and has FSH receptors that have a strong enough affinity for FSH that the follicle can obtain enough of this gonadotropin to allow for further development despite depleted FSH titres (Palter and Olive, 2002). Thus the dominant follicle is often characterized by the higher mitotic state of its granulosa cells, detectable levels of FSH and estradiol in its follicular fluid, and its size which is larger relative to

the other follicles (Eppig et al., 1997). The oocyte within this follicle remains adhered to the follicular wall by an extension of the granulosa cells which create a stalk referred to as the cumulus oophorus (Palter and Olive, 2002). The development of the follicle is an ongoing process that lasts for the first half of the menstrual cycle. Figure 1 illustrates the stepwise maturation of a developing follicle.

Oogonia associating with somatic cells

Pool of primordial follicle cells Early folliculogenesis Primary follicle

Preantral follicle

Antral follicle

Figure 1. Folliculogenesis begins with the development of the oogonia from undifferentiated cells and the association of these cells with those of the surrounding environment. This follicle advances from the stages of a primordial follicle pool to the primary follicle and finally into the preantral follicle which is composed of both granulosa and theca cells. Pictorial representation of follicles reprinted from Henry and Norman (2003: p. 657).

The midcycle hormone surge and resulting ovulation

As previously mentioned, the rising estrogen levels have a negative feedback effect on FSH secretion, yet these levels of estrogen peak twice and consequently have a biphasic influence on LH (Palter and Olive, 2002). Particularly, when estrogen levels are low LH are inhibited, however, as estrogen levels increase the concentration of LH

subsequently increases. The positive feedback induced by estrogen occurs when estrogen is concentrated at a level of at least 200 pg/ml for a period of at least 48 hours.

This prolonged release of a high concentration of estrogen induces a substantial surge in

LH (Palter and Olive, 2002). The midcycle surge in LH is evident in figure 2.

Figure 2. Hormone concentrations throughout the menstrual cycle. A sudden increase in concentration of LH, FSH, and estradiol are evident at the time of ovulation. Figure reprinted from Pocock and Richards (1999: p. 447).

The maximum peak in LH, FSH and estradiol all occur either directly before or during ovulation (fig. 2). It is interesting that most women assume that menses is the time of greatest hormone fluctuation, probably because of physical sensations and awareness of reproductive status at this stage in the cycle, when in actuality it is during ovulation that the greatest fluctuations occur.

Coinciding with the surge in LH, the interactions between estrogen and FSH of the dominant follicle stimulate the presence of LH receptors on the granulosa cells (Palter and Olive, 2002). The drastic increase in LH concentration elicits a response in the follicle which consists of leutinization of the granulosa cells, progesterone production, and ovulation. The human ovulatory period persists for 36 to 38 hours, and occurs approximately 10 to 12 hours after the peak in LH (Palter and Olive, 2002). At this point in the cycle, mediators synthesized in response to LH degrade the extracellular matrix or promote vascular changes, specifically, an increase in prostaglandins and proteolytic enzymes. Either of these modifications generates a positive intrafollicular pressure which causes the follicular wall to be forced outward and decreases the tensile strength of the follicular wall, allowing a perforation to form. The pressures exerted on the follicular wall led researchers to believe that the fertilizable oocyte slowly extrudes from the perforation rather than explosively exiting once the wall ruptures (Palter and Olive,

2002).

The progression of the corpus luteum

Once ovulation occurs, the portion of the follicle that remains after the oocyte has been released transforms into the corpus luteum, a structure which will mediate the luteal phase, the next phase of the ovarian cycle (Palter and Olive, 2002). The pigment lutein is taken up by the corpus luteum, causing the structure to become characteristically yellow

(Palter and Olive, 2002). The granulosa cells within the corpus luteum also absorb low- density lipoproteins through the basement membranes of the follicle which have been imbued with blood vessels (Eppig et al., 1997). The low-density lipoproteins that enter the corpus luteum serve as a substrate for the active secretion of progesterone, a steroid

hormone which acts similarly to estrogen as a negative feedback that decreases both FSH and LH secretions at this point in the cycle (Palter and Olive, 2002). Progesterone production by the corpus luteum inhibits further development of successive pools of follicles (Palter and Olive, 2002).

The corpus luteum also continues to produce estrogen as the developing follicle once did (Palter and Olive, 2002). During the beginning of the luteal phase, estrogen levels decrease; however, once the middle of the luteal phase is reached and the corpus luteum begins to produce estrogen again as well, the concentration of estrogen coincidingly increases. Also, the corpus luteum produces inhibin A which continues to suppress FSH. The perforation of the basement membrane of the corpus luteum enables the hormones produced to directly enter systemic circulation. Furthermore, the secretions of the developed corpus luteum enable both progesterone and estrogen levels to remain high until the regression of the corpus luteum (Palter and Olive, 2002). The corpus luteum persists for approximately 14 ± 2 days (Eppig et al., 1997). If fertilization of the oocyte does not occur and LH levels fall, the corpus luteum begins to regress forming an avascular scarlike corpus albicans (Eppig et al., 1997).

Menses and the proliferative phase

At this point, secretions of the corpus luteum cease and the deciduas functionalis, the superficial two-thirds of the endometrium, is shed during the process of menses

(Palter and Olive, 2002). The cessation of progesterone and estrogen production decreases blood flow to the endometrial wall, causing acute vascular constriction leading to spasm which results in endometrial ischemia, which is a decrease in the blood supply because of the restriction of blood vessels (Palter and Olive, 2002). Concurrent to

endometrial ischemia, the lysosomes in this area degrade, resulting in proteolytic enzyme discharge (Palter and Olive, 2002). These enzymes further promote the breakdown of the endometrial wall; eventually the interstitial hemorrhage and tissue disorganization leads to menstrual flow (Namnoum and Hatcher, 1998). Menstrual flow lasts 4 to 6 days and consists of approximately 20 to 80 ml of blood loss, 90 percent of which is lost by the second day of menstruation (Namnoum and Hatcher, 1998). The remaining decidua basalis, the deepest layers of the endometrium, is the area from which endometrial regeneration will take place during the next menstrual cycle (Palter and Olive, 2002).

As previously mentioned, the uterus undergoes changes which are classified into two stages which correspond to the phases of the ovarian cycle and the subsequent production of hormones. The two stages are the proliferative phase and the secretory phase, both of which refer to the histological state of the endometrium (Palter and Olive,

2002). The proliferative phase begins on the first day of the menstrual cycle, which by consensus among members of the scientific community is upon the initiation of menses.

During the proliferative phase, elevated levels of estrogen cause the deciduas functionalis to grow by mitotic expansion, creating a site suitable for implantation of a fertilized oocyte. Forty-eight to 72 hours after ovulation, the corpus luteum produces eosinophilic protein-rich material that indicates the commencement of the secretory phase, which is heavily reliant also on the effects of progesterone. Within 6 to 7 days after ovulation the endometrium is most apposite for implantation of a zygote. At this stage of the secretory phase, edema progressively increases and the spiral arteries in the endometrium are visible and continue to develop until the onset of menses (Palter and Olive, 2002). A

clear depiction of the phases of the menstrual cycle and the events that occur within each phase are presented in figure 3.

Figure 3. Follicular development, hormone levels and endometrial changes throughout the menstrual cycle shown in relation to each other during a standard 28 day menstrual cycle. The cycle is divided into both follicular and luteal phases as well as the corresponding menstrual, proliferative and secretatory phases. Information from Duksta et al. (2001: p. 291).

Other important hormones

In addition to the neurohormone GnRH, the gonadotropins FSH and LH, and the steroid hormones progesterone and the estrogens, the ovary produces several peptide hormones that play an important role throughout the menstrual cycle (Namnoum and

Hatcher, 1998). Activin, composed of two inhibin beta subunits, promotes FSH secretion

(Namnoum and Hatcher, 1998), while inhibiting prolactin (Speroff and Fritz, 2005).

Both inhibin and activin operate within the ovary, secreted into the follicular fluid and ovarian venous effluent (Speroff and Fritz, 2005), controlling androgen and estrogen levels (Namnoum and Hatcher, 1998). Follistatin also assists in regulating FSH secretions by inhibiting activin through binding and consequently promoting the activity of inhibin (Namnoum and Hatcher, 1998; Speroff, and Fritz 2005).

Also of importance within the ovary is insulin-like growth factor (IGF), a peptide that is structurally and functionally similar to insulin, and also mediates the actions of growth hormones (Speroff and Fritz, 2005). There are two forms of IGF, IGF-I and IGF-

II, with IGF-II being the most abundant in humans (Speroff and Fritz, 2005). IGF-I promotes androgen production in the theca cells that is stimulated by LH, and also enhances the effect of FSH on granulosa cells (Namnoum and Hatcher, 1998). IGF-II is responsible for amplifying gonadotropin actions, and intensifying aromatase activity, granulosa cell proliferation, and the production of progesterone (Speroff and Fritz, 2005).

Since stages of the menstrual cycle do not occur independently of the actions of the rest of the body, a variety of other peptides influence this cycle, but to lesser degrees than those hormones described above.

Variation in the menstrual cycle

Although the menstrual cycle has been described as a rather invariable sequence of cyclic events, deviations from this model exist. The idealized 28-day cycle occurs in only 15 percent of the population (Namnoum and Hatcher, 1998). The majority of the population experience regular cycles that last for 21 to 35 days (Speroff and Fritz, 2005).

While 20 percent of the population are subject to irregular cycles, only 1 percent of the population experience cycles that are regularly less than 21 days or greater than 35 days in length. The variations in cycle length are most often a result in the variability in the duration of the follicular phase of the ovarian cycle. Once the menstrual cycle has regulated after menarche, the majority of women experience a luteal phase that is consistently 13 to 15 days until perimenopause (Speroff and Fritz, 2005).

Age is a variable that greatly influences cycle length and regularity. Anovulatory cycles are most prevalent in women older than 40, or younger than 20, as the period of 5 to 7 years after menarche is marked by relatively long and inconsistent cycles (Speroff and Fritz, 2005). By age 25 it is estimated that more than 40 percent of menstrual cycles range from 25 to 28 days in length (Speroff and Fritz, 2005). Furthermore, from ages 25 to 35, greater than 60 percent of menstrual cycles are 25 to 28 days long (Speroff and

Fritz, 2005). The most regular cycles are observed in women between the ages of 40 and

42 (Speroff and Fritz, 2005). However, the 8 to 10 year period prior to menopause is characterized by longer and irregular cycles (Speroff and Fritz, 2005).

Menstrual cycle irregularities

There are five common temporal menstrual cycle irregularities. When the menstrual cycle does not develop by age 16 in an individual with secondary sexual characteristics, or by age 14 in an individual without visible secondary sex characteristics, it is termed primary amenorrhea (Schillings and McClamrock, 2002).

Secondary amenorrhea is present when menstruation is absent in a women for three normal menstrual cycles or a period of six months in a women who has previously experienced menses (Schillings and McClamrock, 2002). Conversely, polymenorrhea is

used to describe frequent episodes of menses that cycle regularly for a period of 21 days or less (Palter and Olive, 2002). Bleeding between normally cycling menstrual periods is referred to as intermenstrual bleeding, while periods of bleeding that are irregularly timed are classified as metorrhagic (Palter and Olive, 2002). In addition, irregularly timed cycles that are infrequent and possess cycles longer than 35 days are termed oligomenorrhea (Palter and Olive, 2002). Irregularly timed cycles that are frequent and possess periods of prolonged bleeding are considered to be menometorrhagic (Palter and

Olive, 2002).

Chapter 2: Is ovulation truly concealed? Clarification of the Basic Concepts: loss of estrus, continual sexual

receptivity and concealed ovulation

To examine the concealed ovulation, it is necessary to define loss of estrus, continual sexual receptivity , and concealed ovulation based on their meanings in this thesis, as they are commonly used interchangeably in other literature. The term estrus is derived from the Greek term oistros, meaning gadfly in English and translated into the phrase ‘in a frenzied state’. Historically, the term has been used to describe the reaction of cows to the deposition of gadfly eggs on the skin; however, the term estrus has also been used to describe the state of temporary distraction from daily activities experienced by females during specific phases of the reproductive cycle (Hrdy and Whitten, 1987).

Estrus can occur at any point in the female reproductive cycle, but refers “primarily to a set of behaviours that is indicative of the female’s readiness to mate and that may or may not coincide with the time of ovulation” (Steklis and Whiteman, 1989: p.419). It is important to recognize that estrus describes a set of behaviours resulting in female receptivity to sexual endeavors, rather than physical and hormonal manifestations that accompany a state of fertility. Consequently, the loss of estrus would refer to the absence of defined period of observable female proceptivity, receptivity, and attractivity to males.

Continual sexual receptivity is used in reference to the relatively consistent willingness to extend mating throughout the entire reproductive cycle. This term is slightly more complex, as illustrated by Alexander and Noonan (1979) who view the classification of human sexual behaviour as continually receptive to be a “gross oversimplification”; in turn they choose to describe female sexual behaviour as minimal

since often her sexual relations are with a single male during a specific period in time while she rejects almost all others. Alexander and Noonan (1979) suggest that the term

“continuous nonreceptivity” may be more apt in defining the human condition.

Additionally, although copulation among primates is most frequent during the period of fertility, it often occurs outside the ovulatory phase in many species (Hrdy and Whitten,

1986). To eliminate any possible misinterpretations or incorrect applications of the concept ‘continual sexual receptivity’, it will be used in this paper to define recurrent sexual activity outside of the fertile period with fixed frequency during all phases of a female’s reproductive cycle.

The ovulatory event would be revealed if the period of estrus corresponded with the period of maximum fertility, or sexual receptivity was restricted to ovulation. Thus, the concealment of ovulation would require both the loss of estrus and continual sexual receptivity. However, these two criteria alone do not ensure the complete concealment of ovulation as often physical cues, such as sexual swellings, also signal periods of fertility.

In most primate species the physiological process of ovulation is highly conserved.

Many species also produce visual indicators in response to hormonal shifts during ovulatory periods which indicate the time of ovulation as it is associated with these specific physical manifestations (Nunn, 1999). Therefore, it is essential to include the absence of physical manifestations, in addition to a loss of estrus and continual sexual receptivity, as one of the criteria of concealed ovulation. Within the literature related to this topic, there is some variation in the definition of concealed ovulation. Within this thesis, ‘concealed ovulation’ will be defined as requiring continual sexual receptivity in

conjunction with no obvious behavioural cues, displays, or signals such as estrus, as well as the absence of physical changes associated with the onset of ovulation.

Is Ovulation Truly Concealed?

In addition to ambiguity about concealed ovulation, biologists often challenge the belief that ovulation is in fact undetectable in humans. The majority of mammals, including many non-human primate species, experience a period of estrus during which females become increasingly receptive and proceptive to coitus (Tarín and Gómez-

Piquer, 2002). Although it is debated whether or not human ovulation is entirely concealed, several biologists have noted a lack of variation in both sexual behaviour and physical signals during midcycle, as well as the continuous receptivity of women (Brewis and Meyer, 2005; Harvey, 1987; Tarín and Gómez-Piquer, 2002) all necessary for ovulation to be concealed. Numerous studies have attempted to explain the evolutionary history and the ramifications of concealed ovulation by observing the reproductive cycles of modern women. Steklis and Whiteman (1989) note that studies investigating the effects of stages of the menstrual cycle on sexual behaviour rarely include non-Western women, so that conclusions may not be representative of the entire human female population. A specific concern when using only a Western sample is the unique environmental pressures experienced only by this group which may influence any conclusions made. Steklis and Whiteman (1989) draw attention to the fact that Western populations have been exposed to many facets of industrial life, such as chemical contraceptives, which may not be present in the lives of women in other areas of the world. It is further proposed that these industrial influences would not be representative

of the evolutionary history of humans. Consequently, conclusions derived from the study of groups exposed to modern forces may not apply to Hominoid evolution.

Several constraints also exist on current research that limit its effectiveness.

Particularly, ethical concerns arise that often limit the intensity with which people can be studied. Additionally, it is difficult to study humans with the same amount of objectivity that can be used when observing non-human primates. In a comparison of the hormone profiles of a select number of female primates and humans, Rowell (1972) notes that although there are reliable endocrinological data available, the majority of behavioural information about the human female is “…expressed in psychoanalytic terms impossible to compare with information on other primates” (p.72). Rowell’s concern persists as one of the main impediments to studying humans since often the underlying cultural expectations within a society influence and frequently restrict the actions of its researchers. These constraints are exemplified by the observation that humans are the only primate that is not publicly sexually active (Brewis and Meyer, 2004), an additional impediment in the study of reproductive behaviour of humans.

In addition to difficulties that arise from the study of human subjects, the interpretation of data can be variable, often generating both ambiguities and controversy.

Frequently, in published studies the definition of the menstrual cycle differs in the absolute values of time allotted to each phase by researchers. When studying something as variable as the menstrual cycle, researchers attempt to account for variation among women and within successive cycles of the same individual by standardizing the observed cycles by a variety of methods. One of the most common methods of standardization is to adjust all cycles to 29 days in length (the presumed average length of

human menstrual cycles). This type of standardization is accomplished by counting forward from the first day of menses by 11 days, accounting for a luteal phase of average length, and counting 18 days back from the onset of menses to account for a follicular phase of customary length (Steklis and Whiteman, 1989). Another technique used to account for variations in cycle length is to time major events in the ovulatory cycle based on the absolute length of a cycle by determining the proportion of time elapsed in each phase (Urdy and Morris, 1977). This method assumes that the proportion of time spent in each phase is constant despite variations in overall cycle length, and that the hormonal events occur in synch with phase changes (Urdy and Morris, 1977). It is also common to make comparisons only of cycles which are the same length, assuming once again that the proportion of time spent in each phase is consistent, as are hormonal changes; therefore, ovulation is presumed to occur at the same time in cycles of identical length

(Urdy and Morris, 1977).

In a review of the timing of events throughout a human reproductive cycle, Urdy and Morris (1977) examine some of the aforementioned methods of standardization, illustrating through direct comparison of different methods that if one was to deliberately select a specific technique to account for variation in cycle length and pick a complimentary method of analysis, they may be able to construct results which “…would allow the support of nearly any conclusion one would wish to reach” (p. 424). Steklis and Whiteman (1989) expand on this possible cause for inaccuracy by suggesting that the division of the reproductive cycle into phases of predetermined length, rather than employing a more accurate method of cycle division by adjusting phase length to the temporal hormone profiles of each individual cycle, can lead to disagreement about the

timing of events such as ovulation. The example provided is that the postmenstrual phase of one study may be termed the midfollicular phase of another based on how one chooses to divide the phases of the reproductive cycle (Steklis and Whiteman, 1989). As a result, the same data set may yield different interpretations based on the mode of analysis, and ultimately, one may conclude that midcycle peaks in sexual activity occur in humans when in reality only a small proportion of the sample is experiencing increases in coital frequency at the time of ovulation (Steklis and Whiteman, 1989). Furthermore, the variations in methods of standardization and the interpretation of phase lengths can create ambiguity and confusion when comparing multiple studies (Urdy and Morris, 1977).

Why has ‘novel’ become the new buzz word in science?

“The empirical evidence demonstrates that studies with significant results or favourable results are more likely to be published or cited than those with non-significant or unfavourable results” (Song et al., 2000: p. iii). This is important to all research dependent entirely on the published works of others. The accessibility of literature is crucial to all fields of study; therefore, the bias against publishing negative results or results that prove a null hypothesis are unnerving, especially since it is likely that these studies will be repeated by people unaware that they have been conducted previously.

Publication biases occur when there is a marked difference between the results of published and unpublished research (Møller and Jennions, 2001). Several factors that lead to such biases are 1) time lag which occurs when the direction or strength of results directly influence the time it takes for that information to be published, 2) when studies with multiple results report only the positive or significant ones, 3) the dominance of the

English language and its restrictions on the available journals for people who use other

languages to publish in as well as language barriers which arise when retrieving information, 4) negative results are often published in journals with low circulation, 5) the continued citation of articles that are retracted, 6) the interest of the general public in new and interesting findings (Møller and Jennions, 2001; Song et al., 2000), 8) small sample size which can produce results that can be interpreted in a wide-ranging manner leading to highly variable conclusions open to manipulation.

The following examples detail a few of the possible sources of bias highlighted above. Numerous studies have found that researchers decided not to publish because they found their results to be either inexplicable by modern theories, or simply uninteresting (Møller and Jennions, 2001). Coursol and Wagner (1986) found that in a survey of 1000 psychologists, approximately 66% would submit a study that refuted the null hypothesis while only 22% would be willing to submit research supporting the null.

Similarly, Csada et al. (1996) found that of 1201 articles in 43 different biology journals 91% of these papers reported statistically significant findings. This is a remarkably high percentage of positive findings and strongly supports the existence of bias in publication.

Lastly, Møller and Jennions (2001) in a survey of the members of the editorial boards of 19 prominent management journals found a strong preference for publishing papers by investigators with firmly established reputations. Additionally, reviewers were biased based on the prestige of an author, favouring those who were already well received by the academic community (Møller and Jennions, 2001).

Publication biases are difficult to avoid; however, Møller and Jennions (2001) suggest that increased popularity of online journals may reduce the competitiveness for

publication among authors as these journals would all possess essentially infinite space.

In doing so, it is possible that the strong bias for studies with statistically significant findings that refute a null hypothesis may subside. Also, a meta-analysis of the proportion of positive findings in a field could be investigated and the possible forces directing the acceptance of specific outcomes could be more easily recognized.

Research Studies: The Proof of Concealment

Are women correctly aware of ovulatory events?

Small (1996) attempted to elucidate whether modern humans possess accurate knowledge of ovulation and its occurrence by administering a questionnaire to 408 undergraduate university students. Questions asked to determine the understanding of ovulation, its timing, and whether one can identify its occurrence within their own body, or the body of a female partner were provided in a multiple choice format and additional space was provided for recording of possible cues indicating ovulation. Small (1996) only analyzed data from cycles of women who did not use any hormonal supplements, asking women who did use hormonal supplements to answer the questionnaire using the memory of cycles prior to the use of such compounds. The reliability of Small’s (1996) choice to use data provided by memory from the subjects of her study is questionable as often this information is distorted with time and often imprecise. Additionally, Small

(1996) provided no accompanying scientific analysis of the true times of ovulation to verify the beliefs of her respondents. Thus it is questionable whether the typical physical cues used by female participants to indicate times of ovulation are valid.

In any case 90% of the 411 participants believed they knew what ovulation meant

(Small, 1996). However, only 70% of these participants could correctly establish the timing of ovulation. Of the entire sample, 67% were able to correctly identify the timing of ovulation, while 24% believed it to occur either at the beginning or end of the menstrual cycle, and 9% indicated that they did not know when ovulation took place.

Small (1996) found that women indicated the correct time of ovulation during the menstrual cycle more often than men. Additionally, 25% of the female respondents claimed to always be aware of their own ovulation and 28% stated that they sometimes knew (Small, 1996). Of the male respondents in a relationship with a female, 28% claimed that they always knew when their partners ovulated and 21% suggested that they sometimes were aware of this ovulatory event (Small, 1996). Men who were aware of their partner’s fertility often possessed this knowledge due to direct verbal cues indicating their partner’s awareness of the event, while another significant percentage of men gained awareness by counting days from the onset of menses allowing them to anticipate its occurrence. Only a small proportion of men specified that they were aware of fertility because of physical signs displayed by their partner. Conversely, most women who claimed that they knew the timing of their fertility acquired this knowledge from physical signals, particularly abdominal pain and changes in vaginal mucus (Small, 1996).

Another substantial proportion of women were aware of their ovulatory periods because of counting forward or backward from the time of menstruation (Small, 1996).

The counting method employed by many males and some females to judge the timing of ovulation is a relatively accurate indicator of a woman’s fertility period if her cycles adhere to the predetermined phases of the menstrual cycle. However, since the

phases of the menstrual cycle are variable, particularly the follicular phase, this method may only be useful in the general approximation of fertility periods. However, this method does not indicate that knowledge of the ovulatory event is derived by an innate awareness of female periods of fertility; rather it is based on knowledge which is gained through formal education.

The fact that many men were informed of ovulatory events because of direct indication from their partner can lead to the speculation that the female fertility period is not clear to many men. Additionally, although over 50 percent of men in heterosexual relationships in this study stated that they were aware of their partner’s ovulation, it means that close to fifty percent of men in male-female relationships are completely unaware of their partner’s fertility time. In sum, it is unlikely that many males possess a knowledge of the timing of ovulation.

Sievert and Dubois (2005) tested if perceived ovulation corresponds with the increase in LH which biologically denotes ovulation. Thirty-six women participated, all of whom experienced regular menstrual periods 25 to 35 days in length, did not take hormonal contraceptives, and believed they knew when they ovulated (Sievert and

Dubois, 2005). A total of 87 urine samples were provided with collection beginning on the fifth day of menses and ceasing on the perceived day of ovulation. The three days prior to perceived ovulation were analyzed for a typical surge in LH associated with ovulation.

When women were asked how they knew when they ovulated, Sievert and Dubois

(2005) were provided with a set of indicators similar to those supplied to Small (1996), including, but not limited to changes in cervical discharge, abdominal pain, basal body

temperature, increased libido, changes in mood or energy level and general timing within the menstrual cycle. Sievert and Dubois’ (2005) most frequently reported indicators were changes in cervical secretions, abdominal pain, and timing within the menstrual cycle.

Overall correspondence of these indicators with an LH surge demonstrated that in 36.8% of cycles where altered cervical discharge was associated with ovulation women correctly identified the time of ovulation. Correct identification of ovulation was also found in

29.4% of cycles where abdominal pain was used as a cue, while women using the timing of ovulation within the menstrual cycle were correct in their identification of ovulation in only 4.4% of these cycles (Sievert and Dubois, 2005).

In the majority of instances, the aforementioned cues were used in conjunction with another indicator. Often basal body temperature (BBT) is used to monitor ovarian activity as women often experience an increase of one degree at the time of ovulation and

Sievert and Dubois (2005) successfully demonstrate that when used independently as a signal the LH surge was identified in four out of five individuals. However, in the other

25 women who did not use BBT as a cue to ovulation, seven correctly identified their time of ovulation Sievert and Dubois (2005). Since BBT would only elevate by a single degree Fahrenheit that persist for a short period of time, it is unlikely that this subtle change was used to identify menses would not be a method employed by ancestral

Hominoids. It can be argued that the other signals which are based on physical and behavioural cues are more transient and less effective indicators of ovulation. Overall,

Sievert and Dubois (2005) determine that among women who claim to know their period of ovulation there is a concordance rate of 42.5%. When extrapolating these findings to a greater population it is estimated that 14% of women might accurately determine their

own ovulation, suggesting that “…ovulation is concealed to the vast majority of women

(Sievert and Dubois, 2005:318).

Do people in societies which more closely resemble ancient humans have

an awareness of ovulation?

The majority of studies attempting to discern whether females can detect periods of ovulation primarily, and often exclusively, use Western women as participants. Both

Steklis and Whiteman (1989) and Pawlowski (1999) introduce this source of bias and suggest that an analysis of a society living within more natural conditions may more properly assess women’s ability to distinguish ovulatory events from the rest of the menstrual cycle.

Marlowe (2004) attempted to address these biases and determine if more natural conditions facilitate the detection of ovulation by interviewing the members of the Hadza hunter-gatherer society located in Tanzania. In the area the Hadza inhabit, there is little drinking water and consequently personal hygiene, such as bathing, is not attended to for long periods of time (Marlowe, 2004) thus it is proposed that this may promote the accumulation and communication of odours which could act as cues to ovulation.

Marlowe (2004) interviewed 46 adult men and 38 adult women of the Hadza, asking when a woman could get pregnant. Marlowe (2004) was unable to specifically ask when a women ovulated since this is not a familiar concept to the Hadza, nor could answers be quantified completely as the Hadza do not have a numeric system beyond

‘four’. Consequently, Marlowe (2004) ensured that the period considered as ovulatory would span a long period of time (days 9 to 25 of the cycle) to ensure that answers such as ‘the week after…’ or ‘several days following…’ could be included in a separate

category and to also make it difficult to reject the hypothesis that ovulation can be determined by these people.

All but one Hadza individual was aware that sex caused pregnancy. Additionally, more than 50% of the people interviewed believed that conception occurred directly after menses. Marlowe (2004) explained that this answer may originate from the peak in sexual activity experienced by the Hadza after a period of abstinence during menstruation. In agreement with Marlowe’s (2004) findings, Strassman (1996) also demonstrated in a cross-cultural study of 186 women that the most common belief was that conception occurs immediately following menstruation.

The next most common assumption (15.5%) of the maximum time of female fertility was directly prior to menses. 9.5% of people interviewed believed that conception occurred during menstruation. Only 9.5% of participants correctly answered that conception occurred during midcycle. This is a surprising result as it was expected based on the broad range of acceptable answers which would fit into the category of

‘during midcycle’ that 60.7% of participants were likely to give this as an answer

(Marlowe, 2004). Also, women were no more likely than men to correctly identify the time of ovulation (Marlowe, 2004).

Marlowe (2004) noted that menstruation is an observable marker of non-fertility in humans and based on this knowledge and the results of this study he concluded that:

The largely flat frequency of sex through the rest of the cycle then suggests that men may attempt to detect ovulation but that the best they can achieve is a decreased interest in copulation during menses and an increased interest at all other times, waiting until menstruation ends and then having sex regularly starting the day after (p. 431).

Ultimately, Marlowe’s (2004) conclusions do not support an awareness of ovulation among a group of people thought to more closely represent our evolutionary ancestors.

Do forms of sexual behaviour increase in response to ovulation,

indicating times of maximum fertility?

For the past half-century, scientists have eagerly attempted to ascertain whether peaks in sexual behaviour occur at any particular time throughout the menstrual cycle. It is proposed that if a peak occurred at the time of ovulation, it would be correct to assume that, on some level, the timing of ovulation was known. To date, there is no consensus regarding any form of sexual behaviour at ovulation (Urdy and Morris, 1968).

It should once again be mentioned that a recurrent phenomenon biasing the publication of positive or significant results exists. This is pertinent to determining if a peak in sexual behaviour exists. As it is possible that findings suggesting a peak in sexual activity midcycle would be published more than literature supporting an absence of any fluctuations in sexual behaviour (Urdy and Morris, 1968).

Additionally, a small sample size is a common feature among many published studies demonstrating an increase in coitus during ovulatory periods. As noted in a paper identifying common causes of research biases, “…the results from smaller studies will be more widely spread around the average owing to greater random error”(Song et al., 2000:

32). This same study further states that often the variable results produced present a range of findings which can be selectively published (Song et al., 2000).

The possibility of variation in sexual activity in response to the changes in menstrual phases has implications for determining whether human ovulation is truly concealed.

One of the most frequently cited papers concerning the distribution of sexual activity across the menstrual cycle is by Urdy and Morris (1968). They attempt to detect changes in coital frequency throughout the menstrual cycle using two groups of women varying in level of education. They concluded that variations in coital frequency were related to the menstrual cycle; particularly, “The highest rates of intercourse and orgasm occur about the time when ovulation is thought to occur” (Urdy and Morris, 1968: 595).

The conclusions of Urdy and Morris (1968) can be criticized as self-reports were used as the primary method of data collection. This is problematic as memory of past events is often characterized by omissions and inaccuracies. Additionally, the reports generated by one of the groups were only collected yearly, enhancing the possibility that data were erroneously recorded by participants (Urdy and Morris, 1968).

Hedricks et al. (1987) also concluded that coital rate was elevated during the ovulatory phase of the menstrual cycle in a sample of 25 women. In their study the peak in LH was used as an indicator of ovulation and it was found that the rate of coitus increased on the same day as the onset of the LH surge. However, Hedricks et al. (1987) did not report a peak in coitus coinciding with the day of the maximum LH peak.

The importance of excluding women who were avoiding pregnancy, and subsequently using contraceptives, is emphasized by Hedricks et al. (1987) as it is thought that it may act as a confound depressing rates of coitus midcycle. Additionally, all participants said they wanted children in the future within an average time frame of 15 months (Hedricks et al., 1987). Although the authors do not report the proportion of the sample aware of maximum times of fertility, they do claim that “To our knowledge, however, couples were not using family planning methods to estimate the time of

ovulation” (Hedricks et al., 1987: p.237). Despite this, it is plausible that some of the women participating in this study were aware of the fact that female fertility peaks at ovulation and therefore, their desire to procreate motivated them to identify their ovulatory period, using technologies or sources other than their own feelings and senses, and engage in intercourse more frequently at this time in their cycles. This would unavoidably bias the results reported by Hedricks et al. (1987).

Another commonly cited study is by Harvey (1987). To reduce the influence of male-partner sexual behaviours, all types of sexual activities, including alone and with a partner of the opposite sex, were observed (Harvey, 1987). The sample included 69 normally menstruating women participating in heterosexual intercourse at least weekly, who were not using contraceptives and were not attempting to get pregnant. A biphasic increase in basal body temperature was used to determine the time of ovulation and it was found that women engaged and initiated in autosexual activities (masturbation) during midcycle more than at any other point in their cycle. As well, Harvey (1987) reports the highest rates of pleasure derived from sexual behaviours and the strongest feelings of sexual desire occurred before menstruation in a significant portion of the sample (Harvey,

1987).

Two factors which may have influenced the findings of Harvey (1987) include the fact that some women, although participating in intercourse at least once a week, were single which may have affected the timing of coitus as it would have only occurred based on the availability of a partner. Harvey (1987) stated that “Chance factors may have affected the opportunities for heterosexual activity more for the single women than the married or cohabitating subjects” (p.103). Steklis and Whiteman (1989) also commented

on the effect of partner availability on the distribution of coitus during the menstrual cycle in both single and married subjects, stating that it can have dramatic effects which are likely to influence findings. Published studies regarding partner availability and its influence on coital rates were not found.

Second, Harvey (1987) reports that 87% of participants correctly identified midcycle as the correct time of maximum fertility and the entire sample was not interested in becoming pregnant nor were they using contraceptives. It could be hypothesized that this knowledge led to a decrease in coitus midcycle to avoid pregnancy.

Furthermore, the decrease in one form of sexual activity may have resulted in an increase in other forms of sexual behaviour to satiate a consistent level of sexual desire. If forms of sexual behaviour which do not cause pregnancy, such as autosexual activities, were chosen to replace normal coital events, then the peak in autosexual activity can be explained as an artefact of the conscious effort to avoid reproduction. Thus the frequency of autosexual activities is not increasing midcycle as a result of the timing within the menstrual cycle; rather it is increasing because of the awareness that intercourse during the ovulatory period may lead to unwanted pregnancy.

Matteo and Rissman (1984) observed sexual encounters of seven sexually active lesbian couples over a 14 week period. The motivation for using a sample completely composed of lesbian women was to eliminate the fear of pregnancy, methods of contraception, and male influence as possible confounds. Peaks in sexual activity and orgasms occurred midcycle which was defined as days 6 to 11 of the menstrual cycle and no decline in sexual encounters with others was reported during menses. Matteo and

Rissman (1984) hypothesize that the peaks in orgasm are due to heightened senses at the

time of ovulation and to the fact that a taboo is not placed on sexual activity during menses as it is in many heterosexual couples.

Despite Matteo and Rissman’s (1984) statistically significant findings, they do not have universal application due to the small sample size of 14 women used. Additionally reverse cycle day (RCD) and forward cycle day (FCD) counting was used to determine periods of ovulation and standardize cycles among women. According to Harvey (1987),

RCD counts are estimated to be accurate 48 to 75% of time and FCD is not viewed as a significantly more reliable method of menstrual phase identification. Therefore, Matteo and Rissman’s (1984) findings are subject to criticism.

In an attempt to determine whether coital trends exist throughout the menstrual cycle, Brewis and Meyer (2005) analysed data collected through the Demographic and

Health Surveys (DHS). The DHS is considered by demographers as “the most valid and reliable source of cross-sectional data on the reproductive status and experience of women in developing countries” (Brewis and Meyer, 2005:466) and information detailing how subjects are chosen, what is asked, and the data can be accessed through the World Wide Web (www.measuredhs.com ). The sample tends to be larger and more diverse than that used in most studies from North America.

In total, Brewis and Meyer’s (2005) sample consisted of 20,304 potentially ovulating women from 13 countries, all of whom were in stable relationships and participated in intercourse. It was theorized that there is a propensity for women to copulate more frequently during the ovulatory phase of their menstrual cycle. Therefore, women using chemical contraceptives were excluded from the study, as they suppressed ovulation and could not experience such increases in sexual behaviour. Women in stable

unions did not display variation in the frequency of coitus according to cycle phase with the exception of menses during which copulatory incidents were greatly reduced (Brewis and Meyer 2004).

The number of publications reporting positive findings exceeds those reporting statistically insignificant findings; this suggests that it is correct to assume that the frequency of sexual behaviour increases in response to ovulation. However, many researchers vehemently disagree and criticise aspects of studies with such positive results.

The studies detailed in this thesis represent the most common methods used to arrive at the findings reported in this area of research. Furthermore, my challenges of these studies are the same as those made by researchers in the field.

To highlight the inconsistent interpretation of results and to address the disagreement among researchers, Urdy and Morris (1977) reviewed the findings of six common techniques of menstrual cycle standardization using the same data set of 85 women. Nine years after their initial study providing evidence supporting a peak in coitus during the menstrual cycle, Urdy and Morris (1977) found that different techniques produced distinct and dissimilar conclusions.

There were six methods employed: FCD, RCD, Standardized cycle days, Spitz-

Gold-Adams, BBT, and LH surges. The Spitz-Gold-Adams technique divides a natural or variable cycle into seven phases, assigning a specific number of days to each phase

(Urdy and Morris, 1977).

When these six techniques were graphed, all exhibited depressions associated with menstrual flow as well as a constant increase in desire a few days before midcycle and a decline to a low about a week after mid-cycle. No observable or statistical trends

gave evidence to a peak in sexual behaviour at any point throughout the cycle, and Urdy and Morris (1977) concluded that there was no common pattern of sexual behaviour among the different samples of women as different techniques produced diverse results.

The findings of Urdy and Morris (1977) demonstrate that differing conclusions could easily be derived from the same set of observations. Additionally, their work emphasizes the importance of selecting a method of analysis prior to collection of data.

When researchers decide on a method of data analysis which may best interpret the observations made, the method selected is chosen for its ability to represent the data in a manner that adheres to a researcher’s preconceived perception of what findings should be made and biases are incurred. Also, in a review of sixteen years of research, Morris and Urdy (1982) ultimately conclude that the available data do not suggest a “clear-cut answer to the question of the existence or cause of a pattern of intercourse related to the female menstrual cycle” (p. 151).

Others suggest that the high degree of variability of the distribution of sexual activity can be attributed in part to weekly and daily rhythms originating from the predetermined, often rigid, schedules of particular types of work (Pawlowski, 1999).

“This evolutionary quite new seven-day periodicity may influence the distribution of sexual activity across the menstrual cycle, perhaps postponing its peak for a few days”

(Pawlowski, 1999: 261). Particularly, this culturally imposed factor, which influences the amount of leisure time an individual possesses, may cause the frequency of copulation to increase outside of working hours. Subsequent peaks in sexual activity do not correspond to any increase in desire due to cycle phase, but rather they are representative of opportunity.

Is human ovulation detectable by pheromones?

It has been suggested by several researchers that chemical odorants, produced by humans, facilitate recognition among closely associated individuals (Schleidt, 1980;

Porter and Moore, 1981; Schleidt et al., 1981; Cernoch and Porter, 1985; Hepper, 1988).

Karlson and Lüscher (1959) introduced the term “pheromone”, a substance excreted externally by one individual that evokes a response in a second individual. The reaction produced by the second individual can range from a behavioural to a developmental process. Presently, four categories of pheromones have been identified which are primer pheromones, signaler pheromones, releaser pheromones, and modulator pheromones

(Wysocki and Preti, 2004).

Extensive research has tested if pheromones are present in humans. To date, no human pheromone has been isolated through a bioassay guided study (Wysocki and Preti,

2004). It is postulated that human pheromones would originate as secretions in the axillary scent glands (Wysocki and Preti, 2004) which contain many odorant-producing aprocrine glands (Montagna, 1964; Hays, 2003).

Women possess 75% more apocrine glands in their armpits than do men (Brody,

1975); women have more coccal bacteria, while in men more cornyeform bacteria are found (Jackman and Noble, 1983); the axillary glands of men are larger (Doty et al.,

1978); and in both sexes the axillary glands only become active with the onset of sexual maturity (Hays, 2003). Hays (2003) asserts that if axillary glands produce pheromones, they may be implicated in sexual communication due to the abovementioned reasons.

It has been proposed that human pheromones are detected by a vomeronasal organ

(VNO) in the nasal septa, as is the case for other mammals (Hays, 2003). VNOs have

been observed in 90% of adult humans (Garcia-Velasco and Mondragon, 1991; Moran et al., 1991; Stensaas et al., 1991; Bhatnagar and Smith, 2001). In non-human mammals,

VNOs are connected to accessory olfactory bulbs (AOBs) located in the brain (Hays,

2003). However, adult human brains lack AOBs as they recede during the fetal stages of development (Hays, 2003). Human VNOs appear to possess sensory neurons (Stensaas et al., 1991), yet a connection between the VNO and the central nervous system has not been found (Witt et al., 2002). Based on how the VNO functions in other mammals, it is thought that the human VNO may be nonfunctional (Wysocki and Preti, 2004) and possibly vestigial (Hays, 2003).

Despite the uncertainty regarding a mechanism for perceiving human pheromones, the odor produced by the axillary glands is comprised of an array of branched, unsaturated chains of six to eleven carbons (Wysocki and Preti, 2004). The effects of the axillary steroids androstenone, androstadienone, and androstenol are frequently explored, as they are proposed to be the human pheromones (Hays, 2003).

Studies have assessed the effects of these three steroids; claims range from improvement in the women’s feelings towards males when exposed to androstenol (Cowley et al.,

1977, Cowley and Brooksbank 1991), to feelings of submissiveness (Filisinger et al.,

1984). Androstenone has been deemed as an attractant for some women (Kirk-Smith and

Booth, 1980), while others have found that it worsened women’s feelings towards men

(Filsinger et al., 1985; Miworm and Langthaler, 1992). Filsinger et al. (1984, 1990) found androstenone had no effects on the feelings of women and Black and Biron (1982) came to the same conclusions and also found that androstenol had no effects.

Gower et al. (1988) found that both androstenol and androstenone have musky odors, a common scent mimicked by commercial perfumes; therefore, if a musky control is not employed in pheromone studies women may display a bias to the familiar musk scent. In a review of such studies, Hays (2003) found that only the Filsinger et al. (1984,

1990) and Black and Biron (1982) studies incorporated a musky smelling control; furthermore, neither study found any significant behavioural effects caused by the supposed human pheromones. It could be argued that a variety of scents must be incorporated by the control; however, this controversy will only be resolved upon the identification of a human pheromone. One of the most plentifully produced acids of the axillary gland is (E)-3-methyl-2-hexenoic (E-3M2H), which is present in concentrations

50-100 times stronger than androstenone and androstenol (Wysocki and Preti, 2004).

Hays (2003) notes that this level is not enough to produce an odor which is detectable.

Despite these criticisms, the epithelial cells of a female VNO demonstrate an electrochemical response to androstadienone (Monti-Bloch and Grosser, 1991).

Furthermore airborne androstadienone increased the activity of the limbic system in women, and altered skin temperature and conductance in both sexes (Jacob et al., 2001).

Additionally, the epithelial cells of a male VNO have electrochemical responses to airborne estratentraenol, an odorless steroid present in the urine of pregnant women

(Monti-Bloch and Grosser, 1991). Specifically, airborne estratentraenol induced increased brain activity in males (Sobel et al., 1999), and altered skin temperature and conductance in both sexes (Jacob et al., 2001). In these experiments, a control group lacking VNOs was not used, making it difficult to discern whether the effects were

caused solely by the presence of the VNO, or if another area of the brain is implicated

(Hays, 2003).

Vaginal aliphatic acids have also been tested in their role as pheromones in sexual communication. Six aliphatic acids have been recorded in the secretions of the Rhesus macaques ( Macaca mulatta ), each of which demonstrates cyclic variations which heighten at the time of estrous (Micheal et al., 1971). Together, all six aliphatic acids are referred to as the copulins (Hays, 2003). Topical application of these aliphatics to non- estrus females induced male copulatory behaviours towards these females (Michael and

Zumpe, 1982). Michael et al. (1975) noted that acetic acid was found in the vaginal secretions of human females, finding that one third of the women participating in their study exhibited all of the copulins which increased in concentration during the fertile pre- ovulatory week of the ovarian cycle and depressed directly after ovulation. Huggins and

Preti (1981) conducted a similar experiment and found the same proportion of women possessed the copulins; however, they did not observe the same cyclic variation in their production throughout the ovarian cycle.

Notable changes in the cervical mucus would also be contrary to concealed ovulation if they were related to the cyclic variations in hormones associated with ovulation. Reliable literature related to this topic is scarce, and noticeable changes in the mucus have yet to be substantiated as a reliable indicator of ovulation (Huggins and Petri,

1981). Moreover, present studies fail to substantiate subtle changes in mucosal composition as a cue used by women or their partners to accurately identify their reproductive status.

Menstrual Synchrony and its relevance

Others have attempted to implicate odorants, particularly axillary secretions, in the cyclicity of the ovarian cycles of mammals. McClintock (1978, 1983) demonstrated that in mice and rats, the urine of another female of the same species can cause variation in cycle lengths. Specifically, within 3 to 4 cycles the female rat, which does not display a period of menses, can synchronize its ovulation with another female if it is exposed to airborne chemical signals, or pheromones, of another female rat (Baker and Bellis, 1995).

Reproductive synchrony of female squirrel monkeys, Saimiri spp., occurs seasonally based on environmental influences, such as food availibility (Hutchins et al.,

2003). Conversely, in the hamadryas baboons, Papio hamadryas (Kummer, 1968), gelada baboons, Theropithecus gelada (Dunbar, 1980), lion tamarins, Leontopithecus rosalia , and chimpanzees, Pan troglodytes (Wallis, 1985), synchrony has been observed in response to social interactions. Synchrony occurs only within harems, but not within entire troops, suggesting that close social exchanges rather than environmental factors influence menstrual synchrony (Baker and Bellis, 1995).

The possibility that pheromones cause menstrual synchrony has also been tested in humans. Since McClintock (1971) suggested the menstrual cycles of human females were not autonomous from those of surrounding women, the scientific community has avidly generated research on the topic of menstrual synchrony. The findings have varied, and to date, the evidence regarding menstrual synchrony is inconclusive. However, researchers do agree that either common environmental influences or pheromones could promote menstrual synchrony (Weller and Weller, 1993). However, since McClintock’s

(1971) initial study, many in the scientific community believe that the manipulation of a

physiological process in response to human pheromones is the more valid possibility

(Weller and Weller, 1993).

Many of the studies performed since McClintock (1971) have attempted to replicate her findings using similar methodological approaches. Some researchers have found that synchrony occurs (McClintock, 1971, 1978, 1983) and others have not identified significant synchrony (Reviewed in Wilson, 1992). All of these studies have been criticized, and in Wilson’s (1992) review, he identifies three areas which are commonly flawed in the majority of studies. These are the failure to acknowledge the probability that of the pairs sampled: some will synchronize by chance, the miscalculation of the absolute difference between initial menses onset dates, and the exclusion of subjects from the study for the reason that they do not suit the specifications of the research design. Wilson (1992) concludes that, as the majority of studies are inherently flawed by design, menstrual synchrony has yet to be established.

Weller and Weller’s (1993) review divided the studies into categories varying in level of association among women and the types of interactions transpiring; they evaluate how many studies conclude synchrony was present. Although support is found in some of the groups, between roommates, each group contains studies that negate menstrual synchrony and Weller and Weller (1993) conclude that menstrual synchrony does occur in some cases.

Weller and Weller (1993) also elaborate on the initial criticisms of Wilson (1992) and in addition, suggest two other common flaws. First, the inconsistent integration of women using oral contraceptives in research, causing variation in methods and exclusion of members of the sample, and second, the tendency to collect information about onset

dates from participants’ memories (Weller and Weller, 1993). Similarly, Baker and

Bellis (1995) suggest that previous findings indicating the presence of menstrual synchrony make two additional errors: synchrony is overestimated and its influence on human actions is granted too much power, and the incidence of menstrual synchrony is interpreted as an indication of ovulatory synchrony as well.

Overall, the data regarding menstrual synchrony seem to suggest a pheromonal mechanism as a likely underlying cause. However, research on pheromones is yet to firmly establish their existence in humans. Additionally, menstrual synchrony has not been substantiated thoroughly. The lack of supporting data for both pheromones and menstrual synchrony makes it difficult to assess their joint function in influencing human female reproduction. With no conclusive results after four decades of research, it may be necessary to assume that ovulation remains concealed from humans, even on a subconscious level.

Chapter 3: Primates and their reproductive cycles Why study primates?

Information that can be obtained from our closest relatives is often of interest to humans as it may shed more light on the human condition. There are several reproductive features of primates as compared to other mammals that are ubiquitous: long gestation period, offspring well developed at time of birth (with the exception of the tree shrew), sexual maturation delayed to allow for an extended period of development, typically single births, and long lactation. These characters comprise what Martin (1990) terms the precocial complex, which results in low reproductive turnover, giving species an extended period of time for the transmission of vital social knowledge. Another

character of species that are typically precocial is ovulation that is not influenced by the act of mating, termed spontaneous ovulation (Martin, 1990). Despite the physiological importance of ovulation to the female reproductive cycle and its outcomes, it is one of the most covert events of the reproductive cycle and is difficult to identify accurately in humans (Graham, 1981).

Technical issues

Laboratory studies are useful because they can provide detailed information on a range of reproductive characteristics; however, behavioural information inferred from these studies can be inaccurate as they may not reflect the behaviour of these animals in their natural environments (Rowell, 1972). Studies of caged groups represent behavioural tendencies of a group of animals as they are relatively undisturbed in this setting, yet the reproductive data compiled from these studies is often incomplete

(Rowell, 1972). Field studies of wild populations are the most reliable indicator of behaviour; however, it is difficult to determine reproductive information without disturbing these populations (Rowell, 1972). Currently, researchers recognize the biases which are often encountered when data are gathered on primates in a laboratory and therefore information collected from field studies is often considered more representative of natural populations (Butler, 1974).

At present, the analysis of blood samples is considered to provide best representation of the endocrine characteristics of an animal (Shimizu et al., 2003).

However, the analysis of urine is often preferred since it is viewed as less invasive, and is also thought to provide an accurate evaluation of hormone profiles (Shimizu et al., 2003).

Faecal hormone analyses are beginning to be considered reliable and are becoming more widespread (Heistermann et al., 1996).

Steroid hormones and their metabolites, as well as gonadotropins, are considered to accurately reflect endocrine cycles of the great apes, correctly identifying the reproductive status of subjects under analysis (Shimizu et al., 2003). Regardless of the technique employed, hormone analysis provides researchers with a general profile of hormone changes throughout the menstrual cycle which is useful information (Shimizu et al., 2003). However, differences among samples, procedure modifications, and variable methods of analysis and techniques employed, result in a body of data that cannot be easily compared; therefore, attempts to compare primate endocrine cycles using multiple published sources are often faulted by others in the field since methods of hormone analysis used are inconsistent.

Displays related to ovulation: Behaviour and Sexual Swellings

Behavioural modifications resulting from the fluctuations of hormones throughout the reproductive cycle are known as proceptive and receptive behaviours. Proceptive behaviours are those that promote relations with males and are initiated by the female, while receptivity is defined as acts that facilitate copulation (Hrdy and Whitten, 1987).

Proceptive behaviours range from the presentation of hindquarters to a male, as in the

Prosimii, to tongue flicks, as in the Anthropoidea (Hrdy and Whitten, 1987). Receptivity can last anywhere from two hours or a few days, as in the Prosimii, to continual receptivity throughout the reproductive cycle, present in some species of Anthropoidea

(Hrdy and Whitten, 1987).

Sexual swellings are overt physical cues produced during more fertile periods of a female’s cycle and are defined by Nunn (1999a) as an alteration in the overall size, shape, turgidity, and colour of the perineal skin in the pelvis surrounding the urogenital passages and the rectum. Numerous primates visually indicate the time of ovulation with sexual swellings, and a great degree of variability in these swellings exists. Despite variation in the timing of such swellings across primate species, it has consistently been observed that during periods of female sexual swelling coital frequencies increase (Hrdy and Whitten,

1987; Nunn, 1999a). Therefore, researchers often associate these swellings with female receptivity and attractiveness, and consider them to be a moderately reliable indicator of peak ovulatory times (Small, 1993; Dixson, 1983; Martin, 1992 as cited by Nunn, 1999a).

Sexual swellings are produced by some members of the families Lorisoidea, Lemuroidea,

Callitrichidae, Cebidae, Cercopithecoidae, Hylobatidae, and Pongidae (Hrdy and

Whitten, 1987; Butler, 1974; Hutchins, 2003).

The production of swellings requires a large energetic investment on the part of females and may possibly have deleterious effects in some cases (Nunn, 1999a). Several potential problems associated with sexual swellings which could reduce female fitness are outlined by Nunn (1999a) in his comprehensive review of non-human primate reproductive swellings. These factors include the possibility that parasites may be a threat to the female as would possible infections of the swollen area as a result of increased fluid retention and visibility, the reduced availability of water to other areas of the body as a result of the swelling, and the restriction of mobility due to swelling which increases an organism’s mass (Nunn, 1999a). Despite these possible disadvantages, sexual swellings also have observable benefits, including improved awareness of female

fertility, and heightened interest of males in females who are maximally swollen (Hrdy and Whitten, 1987).

Although no single hypothesis has been unanimously accepted by the scientific community, one potential explanation for sexual swellings is Nunn’s (1999a) Graded

Signal Hypothesis. The Graded Signal Hypothesis proposes that exaggerated swellings are cues to female fertility, causing dominant males to guard females only during times of peak swelling (Nunn, 1999a). Although ovulation tends to occur around peak swelling, ovulation can occur during a range of times throughout swelling; thus males must continually guard females throughout the duration of swelling. If the period of swelling of multiple females overlaps, then many males may choose to abandon a female after her period of maximal swelling to monopolize the time of another female who is experiencing maximum swelling. If this is to occur females have the ability to mate with multiple males, including subordinates, confusing paternity, and possibly decreasing the instance of infanticide (Nunn, 1999a).

The connection between sexual swellings and multimale groups

Although sexual swellings are present in the Tarsioidea and some species of New

World monkeys, exaggerated sexual swellings are limited to the Old World monkeys and great apes (Table 1). Furthermore, exaggerated sexual swellings occur most frequently in females living in multimale breeding systems (Hrdy and Whitten, 1987; Nunn, 1999a;

Table 1). Nunn (1999a) also suggests that non-seasonal breeders are more likely to possess exaggerated sexual swellings as there would be less probability of the overlap of female fertility; thus swelling could function as a means of reducing a dominant male’s monopoly over a single female. Table 1 compares the degree of swelling and

menstruation both ranging from overt, meaning highly visible, slight, meaning partially visible, none, meaning no visible cues are present and unknown, meaning that data is yet to be collected.

Table 1. The degree of sexual swelling and menstruation in 32 primates from seven primate families (Data on menstruation and swelling from Hrdy and Whitten, 1987 and Hutchins, 2003. Data on mating systems from Lindenfors, 2002).

Degree of sexual swelling Degree of Menstruation Family Species None Slight Overt UNK None Slight Overt UNK Mating System Tarsiidae Tarsier ● ● Monogamous/Unimale Cebidae Mantled howler ● ● Multimale Brown capuchin ● ● Multumale Squirrel monkey ● ● Multimale Tufted capuchin ● ● Multimale northern night monkey ● ● Monogamous Central American spider monkey ● ● Multimale Callitrichidae Common marmoset calltrix jac ● ● Monogamous/PA Cotton top tamarin ● ● Monogamous/PA Cercopithecidae Hanuman langur ● ● Multimal/Unimale Patas Monkey ● ● Unimale

Talapoin Monkey ● ● Multimale

Rhesus monkeys ● ● Multimale 47 Barbary macaque ● ● Multimale Japanese macaque ● ● Multimale Vervet ● ● Multimale Blue monkey ● ● Unimale DeBrazza’s monkey ● ● Unimale Grey-cheeked mangabey ● ● Multimale White-collared Mangabey ● ● Multimale Yellow baboon ● ● Multimale Hamadryas baboon ● ● Unimale Gelada baboon ● ● Unimale Drill ● ● Unimale Hylobatidae Hoolock gibbon ● ● Monogamous Lar gibbon ● ● Monogamous Pongidae Orangutan ● ● Multimale/Unimale Lowland gorilla ● ● Unimale Mountain gorilla ● ● Unimale Common chimpanzee ● ● Multimale Pygmy chimpanzee ● ● Multimale Hominidae Human ● ● Monogamous

Concealed ovulation in primate species

Of six non-human primate species, I consider three that are known to exhibit the attributes considered necessary for concealed ovulation as defined above. The other three primates do not possess concealed ovulation, but are close relatives to at least one of the other three belonging to the same family. The three primates considered to possess concealed ovulation are the vervet, Cercopithecus aethiops , the orangutan, Pongo pygmaeus , and the Sumatran orangutan, Pongo abelii . Conversely, the blue monkey,

Cercopithecus mitis as well as DeBrazza's monkey, Cercopithecus neglectus display ovulatory cues and are closely related to Cercopithecus aethiops (Sillén-Tullberg and

Møller, 1993), while both the orangutan and Sumatran Orangutan are phylogenetically similar to the western gorilla, Gorilla gorilla (Sillén-Tullberg and Møller, 1993) which is receptive during only two days of its reproductive cycle. Sets of closely related organisms were included for comparison to identify any differences in reproductive features, life histories, and social characteristics which may exist among organisms that display ovulatory signals versus those that do not exhibit ovulation.

A summary of the reproductive features of these six non-human primates is included in Table 2, 3, and 4. Table 2 highlights the length of each species’ reproductive cycle and the corresponding number of days within the cycle during which females are receptive to copulations. Table 3 defines the length of the breeding season for each of the six primate species. Further reproductive characteristics, such as female body mass, age of sexual maturity, gestation length, number of offspring per reproductive event, and the time separating reproductive events are recorded in table 3. Finally, table 4 provides a comparison of the social structures of each of the six primate species outlining average

group size, the number of females and males within a group, and the mating system. The mating systems of the six primate species fall into three categories: unimale, multimale, and monogamous. The unimale system of the blue monkey, DeBrazza’s monkey, gorilla, and sometimes the orangutan refers to a group with a single sexually mature male that breeds with all of the females within the group. Multimale groups of the vervet and some orangutans possess multiple breeding males that are polygynous, as they often mate with more than one female throughout a breeding season.

Table 2. Reproductive features of six extant primate species including whether or not concealed ovulation is present, the average length of an ovulatory cycle, the length of female receptivity to sexual encounters, and the duration of the breeding season. The sources that information are also listed. Concealed Ovulatory cycle Length of Duration of Sources for length of ovulatory Species ovulation length (days) receptivity breeding season cycle and length of receptivity (days) per year (days) Cercopithecus Yes 33 33 92 Hrdy and Whitten, 1987; Nunn, 1999b aethiops

Cercopithecus No 30 4-5 * 120 Hrdy and Whitten, 1987; Nunn, 1999b mitis

Cercopithecus No - 1 – 28** 90 Hrdy and Whitten, 1987; Nunn, 1999b

neglectus 50

Pongo Yes 31 31 365 Hrdy and Whitten 1987; Nadler, 1982 pygmaeus

Pongo Yes - - 365 Nadler, 1982 abelii

Gorilla No 28 2 365 Nadler, 1982; Nunn, 1999b gorilla

* not related to cycle ** recorded receptivity ranging from 1 to 28 days as well as throughout cycle

Table 3. Reproductive characteristics of female representatives from six extant primate species including body mass, age of sexual maturity, length of gestation, number of offspring produced per reproductive event and the interval between reproductive events. Data from Lindenfors (2002) with the exception of body mass data are from (Lindenfors and Tullberg, 1998). Body mass Age of sexual Length of Average number Average interval Species (kg) maturity (months) gestation (days) of offspring between births (years) Cercopithecus aethiops* 3.56 54 163 1 1.33 Cercopithecus mitis 4.15 70 140 1 1.67 Cercopithecus neglectus 3.96 62.3 182 1 1.62 Pongo pygmaeus* 38.70 84 249.5 - 6.5 Pongo abelii* 244 - 7 Gorilla gorilla 97.70 78 260 1 3.83 * indicates that ovulation in particular species is concealed.

Table 4. Social structures of six extant primate species. Group Structure** 51 Species Mating system*** Average group Number of females Number of males per size per group group Cercopithecus aethiops* 7 4.25 3 Multimale Cercopithecus mitis 19 18 1 Unimale (polygyny) Cercopithecus neglectus 4 3 1 Unimale Pongo pygmaeus* Solitary - - Unimale and Multimale Pongo abelii* Solitary - - - Gorilla gorilla 8.4 § 3 1 Unimale * indicates that ovulation in particular species is concealed. ** data for group structure from Nunn, 1999b. *** data for mating systems obtained from Lindenfors and Tullberg, 1998, with the exception of the Cercopithecus neglectus for which data was obtained from Wahome et al. 1993. § group size from alternative source (Parnell, 2002).

Can Phylogeny explain concealed ovulation?

Sillén-Tullberg and Møller (1993) assumed that the phenomenon of concealed ovulation evolved by one of either two ways. First, in the Catarrhini it was passed on to the members of the Hominoidea who evolved from the previous group, or by evolving separately in both the

Cercopithecoidea and Hominoidea (fig. 4). When the superfamily Cercopithecoidea is examined in greater detail, the vervet is the only member that has concealed its ovulation. Additionally, the majority of species in the superfamily Hominoidea do not possess concealed ovulation, as the orangutan and human are the only exceptions. Based on this, it is likely that concealed ovulation evolved independently in all three groups and is therefore not present as an ancestral trait in the species exhibiting it.

Figure 4. Phylogenetic relationships among the major groups of extant primates. From Sillén-Tullberg and Møller (1993).

Can social structures explain concealed ovulation?

Varying social structures are present in different species of primates. Notably,

vervets have a matrilineal social heriarchy where females remain within their natal troop,

maintaining relationships with their maternal relatives (Melnick and Pearl, 1987). The

hierarchies of female-dominated vervet societies are established at birth as offspring inherit the rank of their mother and that rank does not diminish or change with age

(Melnick and Pearl, 1987). While the Blue Monkey and the DeBrazza’s monkey also possess similar matriarchal patterns, they differ from the multimale social system of the vervet in that they are both unimale social systems (Wahome et al., 1993). The orangutan species are the only known example of a naturally solitary primate, inhabiting large, overlapping home ranges (Hutchins, 2003). Conversely, gorillas live in age-graded groups containing one sexually mature male (Robbins, 1995).

Based on variation in observed social structures both among species possessing concealed ovulation and among species that display their fertility, it can be concluded that social structure does not explain why some primates possess concealed ovulation.

Furthermore, the mating systems practiced within these social units are also highly variable showing no apparent similarity which could be used to explain concealed ovulation within particular primate species.

The application of primate research to the study of concealed ovulation

Although data on free-ranging primate populations are scare, primates are important subjects to study because of their relatedness to humans. If we accept that human ancestors displayed their fertility as most primates do, we might assume that some selective advantage has come with the loss of advertisement. Understanding the purpose of sexual behaviours and swellings in primates may help to explain advantages, such as increased reproductive success.

The similarity of the hormone profiles of all primates, including humans, illustrates the conserved nature of the physiological mechanisms of female reproduction.

However, more conclusive data could be drawn from such evaluations if a more complete data set existed that was comparable. Although three non-human primate species were identified as possessing concealed ovulation, it is likely that other species exist and that our knowledge about these species is currently limited. It may also be possible that concealed ovulation exists in non-human primate mammals. Further investigation of mammalian reproduction would determine if more species concealing their ovulation exist. A larger sample would provide more opportunities for understanding factors that could be acted upon by natural selection.

Chapter 4: theories explaining the significance of concealed ovulation

With an increase of knowledge about primates in their natural habitat during the second half of the twentieth century, several researchers recognized the uniqueness of the human strategy of reproduction, specifically the concealment of ovulation.

Consequently, discussion of human concealed ovulation erupted as publications investigated its significance and adaptive value. The debate over the evolution of concealed ovulation endures and uncertainty continues to surround this facet of female reproduction.

An introduction to the proto-human

The origin of modern humans ( Homo sapiens sapiens ) has been widely investigated using a variety of techniques. DNA hybridization studies support sharing of a common ancestor between humans and chimpanzees more recently than with other apes (Parker 1987). DNA, archaeological evidence, and fossil remains suggest that the ancestors to modern humans originated in Africa (Aiello, 1993). Similar to their primate relatives, humans are predicted to have lived in groups comprised of multimale societies

(Alexander and Noonan, 1979). It is also generally accepted that proto-hominids displayed their fertility and that concealed ovulation is a derived character.

Overview of theories

Theories to explain concealed ovulation are summarized in chronological order in figure 5. Although the ten theories examined in this thesis are not presented in order of

their publication, figure 5 serves well to highlight the main arguments of the theories addressed.

Alexander and Noonan: Burley: females avoided Spuhler: larger adrenal Strassmann: females covert ovulation copulation during ovulatory glands resulted in the concealing ovulation were not promoted extended periods to evade pain and adaptation of a higher degree attractive mates, allowing consortships leading to death; the women to of sexual receptivity in subordinate males to pursue the enhancement of reproduce were those females, acting to conceal prolonged partnerships and 1979 parental care unaware of ovulatory status ovulation 1981 provide extended paternal care

57 Benshoof and Thornhill: Hrdy: concealed ovulation cuckoldry allows females to seek obscures paternity resulting in superior genes through the decrease of male aggression, copulations outside of the pair in the form of infanticide, bond, while males are unaware towards offspring which males of female fertility may have fathered

Figure 5. Chronology for ten predominant hypotheses explaining the evolutionary significance and adaptive advantages of concealed ovulation. Each theory is identified by the last names of its author and summarized by a brief statement elucidating its primary arguments.

Daniels: concealed Turke: concealment of Andelman: Based on Schröder: concealed ovulation resulted from the ovulation paired with observations of vervets it ovulation served to deletion of this information synchronized is probable that deceive dominant males from female consciousness ovulatory periods concealed ovulation and provide females with allowing for a more facilitated prolonged served to reduce male- a greater selection of cohesive and cooperative pair bonds and male competition and mates while reducing 198 3 society 1984 enhanced paternal care 1987 infanticide 1993 infanticide 58

Concealed ovulation and its evolution

Consensus is yet to be reached regarding the selective pressures promoting the concealment of ovulation or its adaptive advantages. Most of the theories possess common elements. Specifically, these hypotheses often predict similar advantages over possessing a discreet period of fertility, including the extension of consortships promoting the enhancement of paternal care, prevention of infanticide, successful cuckoldry, and the critical importance of biparental care due to the altricial nature of human offspring. In sum, a brief review of the most important elements of each of the ten theories follows.

Alexander and Noonan’s (1979) hypothesis that concealed ovulation came from the extension of consortships leading to the establishment of paternal care, provides the foundation for several subsequent theories. In particular, the idea that parental care was a significant benefit to altricial young, improving their survival, is incorporated into the framework of many theories. Alexander and Noonan (1979) have been criticized for not explaining why successful male polygynists would willingly choose a reproductive strategy which would decrease their reproductive success. Smuts (1985, cited by Turke,

1988) argue that for prehistoric males to invest energy providing parental care, confidence of paternity needed to be absolute. Alexander and Noonan (1979) have also been criticized regarding the validity of their assumption that confidence of paternity is low in groups containing females with estrus swellings or other indicators of fertility.

Unfortunately, we are unable to gauge primate confidence of paternity through field observations which limits our ability to test these and alternate hypotheses. Overall,

Alexander and Noonan’s (1979) hypothesis remains respected and is often used as the basis for other hypotheses attempting to account for concealed ovulation.

Strassmann (1981) modified the preceding hypothesis and proposed that the lack of estrus signals decreased female attractiveness, allowing subordinate males to court females no longer monopolized by dominant males. As parental care became increasingly important for the survival of offspring, females valued it to an extreme extent. Eventually, the benefits of paternal care exceeded those of superior genetics

(Strassmann, 1981) explaining the transition from a highly polygynous society to a more monogamous one. Strassmann’s (1981) hypothesis establishes a more plausible scenario explaining the shift toward concealed ovulation.

One criticism of Strassmann’s (1981) hypothesis originates from the argument that concealed ovulation promoted the development of monogamy. In the majority of other monogamous species, concealed ovulation is not present; monogamy is practiced by less than 3 percent of mammalian species, among which scarcity of resources and available territory, substantial paternal investment, and altricial young requiring prolonged periods of development, are common features (Kleiman, 1977). Based on this evidence it is more probable that monogamy evolved as a result of the selective pressure incurred by one of the aforementioned factors rather than concealed ovulation.

Hrdy (1979) proposes the possibility that extended consortships served to reduce male aggression towards offspring as paternity was often confused by hidden ovulatory periods. If females suppress sexual swellings that give males information regarding times of fertility it is plausible that multiple males could incorrectly assume their consortship with this female led to impregnation, providing the scenario necessary for

Hrdy’s (1979) claim that the confusion of paternity by hidden ovulation decreased male- initiated infanticide. Primate studies suggest that males are less likely to harm offspring that they may have sired. Thus infanticide is less likely to be motivated by the possibility of increasing one’s own reproductive success (Dunbar, 1980; Graham, 1981; Hrdy and

Whitten, 1987).

Andelman (1987) concurs with Hrdy (1979), believing that concealed ovulation initiated the reduction of male competition and aggressive behaviour. Andelman’s

(1987) conclusions are based on observations of vervet colonies and the behaviours they displayed. Thus this hypothesis is applicable to both humans and other primate species.

Unfortunately, the same ambiguity regarding whether human ovulation is truly concealed also surrounds vervet ovulation. Evidence from coital peaks and observations of behaviours over prolonged periods of time suggest that ovulation is concealed. Yet it remains to be determined if vervets produce chemical odorants in response to hormone changes, or any other subtle ovulatory cues.

Benshoof and Thornhill (1979) argue that females concealed ovulation to facilitate cuckoldry. They propose that males continue to invest in offspring while females’ discreetly sought extra pair copulations with males who would provide them with superior genes or resources. In a study conducted in the 1940’s on humans, blood samples were collected from 1000 infants and their parents in hospitals in the USA and it was revealed that 10% of children were a product of cuckoldry (Diamond, 1992).

Diamond (1992) concludes that,

The true incidence of extramarital sex must have been considerably higher than 10 percent, since many other blood-group substances now used in paternity tests were not yet known in the

1940s, and since most bouts of intercourse do not result in conception (p.86).

The results of this study were so shocking to researchers that they were not submitted for publication. Diamond (1992) suggests that these findings are best interpreted as a result of game theory, where success is defined by the production of offspring. It is evident that the majority of reproductive responsibility falls on females who invest in offspring for a prolonged period in comparison to their mates.

Subsequently, the drive for maximum genetic representation in subsequent generations can lead to mixed reproductive strategies, whereby females often choose to increase cuckoldry, attaining superior genes and parental care, and are successful because of concealed ovulation and internal fertilization.

Similarly, Schröder (1993) maintains that the concealment of ovulation allowed females to pursue mating relationships with males outside of the pair bond. However,

Schröder’s (1993) hypothesis differs from Benshoof and Thornhill (1979) as Schröder maintains that females were often paired with dominant males and sought subdominant males in EPCs. In Schröder’s (1993) argument females benefit not from superior genetic material for offspring, but by receiving additional resources (such as meat) and enhanced alliances with males, possibly reducing the incidence of infanticide (Schröder, 1993).

However, the suggestion of additional meat is speculative as it would be assumed that dominant males would be more successful hunters and better able to provide for females than would be subordinate males.

Turke (1984) proposes that in conjunction with the development of concealed ovulation, the synchronization of ovulatory periods among females enhanced the success of this covert reproductive strategy. Although Turke’s (1984, 1988) hypothesis

incorporates aspects from other researchers his findings regarding menstrual synchrony are debatable. Menstrual synchrony continues to be a subject popularized by the media

(see Chapter 2); however, the empirical evidence supporting such a phenomenon is not compelling. Furthermore, the assumption that the synchrony of periods of menses corresponds to a synchronization of ovulatory events is incorrect as it does not account for the natural variability of the menstrual cycle.

Daniels (1979) provides an equally controversial hypothesis promoting the concept that unnecessary and possibly disruptive information must be deleted from human consciousness to allow for the existence of a cooperative society based on reciprocal sharing. Daniels (1979) maintains that once visible estrus signals were diminished, self-deception eliminated female and male awareness of ovulatory periods.

Although Daniels (1979) suggests a mechanism by which ovulation became hidden from human awareness, it is ambiguous and it does not function on the level of the individual; thus her theory remains contested by the scientific community as selective deletion of information is yet to be substantiated by the scientific community.

In contrast to Daniels’ (1979) emphasis on the psychological concealment of ovulation, Spuhler (1979) argues that ovulation became hidden as a result of unrelated physical adaptations. Spuhler (1979) asserts that bipedal locomotion caused an enlargement of the adrenal gland which triggered the increased production of female sex steroids which concealed ovulation. This framework provides an explanation for the loss of overt sexual swellings, as sexual swellings would no longer be as effective due to a shift in posture and the resulting decrease in the visibility of the female genitalia that

would accompany bipedal movement. However, Spuhler’s (1979) hypothesis does not clearly explain or clarify the evolution of concealed ovulation.

Burley (1979) is the first of her contemporaries to suggest a plausible mechanism by which concealed ovulation was established and inherited by successive generations.

Burley (1979) suggests that with the development of the intellectual ability to associate conception with copulation at the time of ovulation and the possibility of pain and death during pregnancy and childbirth, egocentric women motivated by a desire for their own survival ceased to participate in intercourse during periods of fertility. Subsequently, the only women who experienced reproductive success were those unaware of their periods of ovulation; thus this trait was passed on to their daughters (Burley, 1979).

In conclusion, it is appropriate to restate that substantial differences and discrepancies exist among the hypotheses for the evolution of concealed ovulation and its adaptive advantages. Most hypotheses are not mutually exclusive, as all incorporate several elements common to other arguments. However, the distinctiveness of the collection of ten hypotheses discussed illustrates the ambiguity which continues to be a facet of the study of concealed ovulation. Furthermore, these studies all agree upon the need for further research to develop a more comprehensive understanding of this female reproductive phenomenon. Of particular interest would be the development of a theory which could account for the incidence of concealed ovulation in all primate species.

Conclusion

It is apparent throughout this thesis that concealed ovulation is controversial. My review suggests that self-awareness of reproductive status, human pheromones, and

menstrual synchrony do not exist. However, gaps in the available literature influence the conclusions which can be legitimately drawn.

It is possible that publication biases and the incomplete data associated with concealed ovulation have caused the diversity of hypotheses that have been published.

Furthermore, variation among these hypotheses may be accounted for because of the biases and omissions in available literature. These inconsistencies could be better accounted for if a meta-analysis of literature concerning the awareness of ovulation, pheromones, and menstrual synchrony was performed.

Because concealed ovulation is such a broad topic, there are several worthwhile avenues for further research. First, attaining a more complete set of data about the hormone cycles of primate reproduction would allow for further comparison of trends between humans and other primates. More preferable would be a data set that was collected and analyzed by the same methods, allowing for the comparison of absolute values; this would allow researchers to recognize variations among primate cycles and possibly determine which variation in the hormone production during the reproductive cycle is associated with the concealment of ovulation. Additionally, if the assumption that concealed ovulation is a derived character is valid, it would be valuable to investigate the necessary shift in female qualities found attractive by males, as they may provide insight into the evolutionary steps leading to the concealment of female fertility.

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Appendices Appendix A. An annotated bibliography of several of the resources used throughout this thesis and their relevance to the study of concealed ovulation.

Alexander, R.D., and K.M. Noonan. 1979. Concealment of ovulation, parental care,

and human social evolution, pp. 436-453 in Evolutionary Biology and Human

Social Behaviour . Edited by N.A. Chagnon and W. Irons. Duxbury Press,

North Scituate.

Alexander and Noonan’s work is considered to be the pivotal piece that fueling

interest in human concealed ovulation. In this article Alexander and Noonan

argue that the concealment of ovulation enhanced the length of consortships and

as a result parental care also increased. Their argument is based on the belief that

parental care greatly impacts the survival of offspring and that when young

receive more care they are better equipped to survive and in turn procreate.

Although other works had been written prior to this piece, no other is discussed as

in depth or cited as frequently by other articles. Familiarity with this piece of

work prior to reading subsequent articles discussing concealed ovulation is

helpful as ideas are often compared and contrasted to those of Alexander and

Noonan.

Andelman, S.J. 1987. Evolution of concealed ovulation in vervet monkeys

(Cercopithecus aethiops ). Am. Nat . 129: 785-799.

Andelman’s examination of concealed ovulation is useful because he uses the

vervet monkey as his model organism. Diverging from the human centered

discussion of concealed, Andelman considers which of the previously established

theories is applicable to non-human primates. Andelman concludes that the most

plausible explanation of the evolution of concealed ovulation is that it was

developed to deter the incidence of infanticide. By confusing paternity males

were unable to discriminate between their own offspring and the offspring of

competing males. Subsequently, males chose to decrease aggression towards any

offspring that they may have sired to improve their own reproductive success. As

a result, the aggression towards offspring decreased substantially and offspring

survival increased.

Baker, R.R., and M.A. Bellis. 1995. Human Sperm Competition: Copulation,

Masturbation, and Infidelity. Chapman and Hall, London.

This book is primarily oriented around human sperm competition and its role and

possible implications in other physiological processes and human behaviours.

The topic of human sperm competition has generated increased interest over the

past decade as it provides unique and often unconventional ways of explaining a

variety of phenomenon, including concealed ovulation. Baker and Bellis argue

that concealed ovulation created greater pressure on males to compete more

effectively to attain reproductive success and suggest that sperm competition was

one means do so. Although the conclusions drawn about concealed ovulation by

this book continue to be tentative and rely on incomplete research, it provides

well-established information about an array of human reproduction characters,

such as historical methods of studying sexuality, a comparison of the magnitude

of reproductive anatomy among various primate species, and some plausible

explanations for idiosyncratic human behaviours.

Benshoof, L., and R. Thornhill. 1979. The evolution of monogamy and loss of estrus

in humans. J. Soc. Biol. Struct. 2: 95–106.

Benshoof and Thornhill (1979) were the first to propose that cuckoldry had an

implicit role in the development of concealed ovulation. They argue that

concealed ovulation facilitated the ease with which females could covertly

participate in extra-pair copulations (EPCs). Furthermore, they maintain that

EPCs were worthwhile to females as it provided them with the ability to conceive

offspring with a genetically superior male, while continuing to receive parental

care from their unsuspecting mate. Benshoof and Thornhill provide a unique

perspective that has been recently demonstrated by studies showing an

unexpectedly high rate of human babies who were not the legitimate offspring of

the men who believe to be their fathers. Despite this support, the scientific

community has not accepted this theory as the sole force that caused the evolution

of concealed ovulation.

Brewis, A., and M. Meyer. 2005. Demographic evidence that human ovulation is

undetectable (at Least in Pair-Bonds). Curr. Anthropol. 46: 465-471.

The information presented in this study is based on data gathered by the

Demographic Health Survey, a worldwide questionnaire. Because the data are a

collection of over 20 000 participant responses and the participants are not from

Western countries, a unique perspective is presented. Brewis and Meyer examine

whether humans possess variation in sexual behaviour and if any of the possible

variation is related to changes in the phases of the menstrual cycle. It is

concluded that coital frequency remains consistent throughout the cycle and thus

humans do not possess an awareness of female fertility. Brewis and Meyer are

confident in their findings because they have eliminated the Western bias and

their sample size is considerably robust.

Burley, N. 1979. The evolution of concealed ovulation. Am. Nat. 114: 835-58.

Examining previous theories suggesting reasons for the evolution of concealed

ovulation, Burley argues that when people gained the intellectual capacity to

recognize the connection between ovulation, copulation, and childbirth women

made an egocentric decision to cease sexual activity during periods of fertility.

The females who were attune with their ovulatory periods successfully evaded the

pain and possibility of death associated with childbirth; however, these women

also failed to produce subsequent generations. Consequently, the only females

who produced offspring were those who were unaware of their fertility and passed

this characteristic on to their daughters, as a result, ovulation became concealed.

Burley is the only researcher who provides a mechanism explaining the gradual

shift to concealed ovulation, thus her theory is important and should be given

consideration.

Daniels, D. 1983. The evolution of concealed ovulation and self-deception. Ethol.

Sociobiol. 4: 69-87.

Daniels provides a very controversial explanation for the evolution of concealed

ovulation. She argues that females and males selectively deleted information

concerning female fertility because this information would be disruptive to the

functioning of large social groups. Although Daniels does not provide a

mechanism that would have enabled for the development of concealed ovulation

her ideas are intriguing. Daniels also briefly outlines previous theories; however,

her interpretation of some of them, particularly Burley’s (1979), is incorrect.

Diamond, J. 1992. The Third Chimpanzee: The Evolution and Future of the Human

Animal . Harper Perennial, New York.

This has become a popular novel that discusses the advent of agriculture and its

bearing on humans, our relation to other primates, and our impact on the world.

Jared compares humans to their closest relatives, the chimpanzee, in an attempt to

elucidate what effects a small difference in genetic composition can have. Jared

briefly considers the possible implications of concealed ovulation, particularly the

possibility that it enhanced the effectiveness of female reproductive strategies.

Looks at what differentiates us from our closest relative, the chimpanzee.

Graham, E.C. 1981. Menstrual cycle of the great apes, pp.1-43 in Reproductive

Biology of the Great Apes: Comparative and Biomedical . Edited by E.C.

Graham. Academic Press, New York.

This is a useful resource as it compares the reproductive cycles of the great apes.

The research presented was carried out by the same group of researchers and

therefore methods are more consistent. Although some variation in analysis

techniques was used by these researchers, it is still valid to make comparisons

based on general trends in the data presented. However, because some

dissimilarity in techniques does exist, direct comparisons of the absolute values in

hormone concentration are not valid. This was the only chapter used in the text it

is found; yet the entire book would be a valuable and reliable resource for

research focused on endocrine comparisons of reproductive cycles of the great

apes.

Gray, J.P., and L.D. Wolfe. 1983. Human female sexual cycles and the concealment

of ovulation problem. J. Soc. Biol. Struct. 6: 345-352.

This article provides a useful summary of seven major theories explaining the

evolution and purpose of concealed ovulation in the human. Gray and Wolfe also

investigate whether variation exists in coital frequency, concluding that peri-

menstrual peaks do exist. Although they believe that coital rates do fluctuate in

response to the progression of events during the menstrual cycle, it is suggested

that modification of previously proposed theories would accommodate these

peaks while arguing that ovulation remains concealed. Gray and Wolfe provide

an interesting perspective; however, their conclusions are based on data which

remains highly speculative.

Hays, W.S.T. 2003. Human pheromones: have they been demonstrated? Behav.

Ecol. Sociobiol. 54: 89-97.

This review includes numerous of pheromone research over the past five decades

studies and concludes that the evidence is incomplete and that human pheromones

are yet to be demonstrated. An investigation of the signaling among non-human

primates is included and the significance of chemical odorants in these species is

emphasized. Hays also suggests that if menstrual synchrony existed or if men

could influence the menstrual cycle, then pheromones may be the cause.

However, to date conclusive evidence has not been provided. This article

provides a clear examination of human pheromones and because it is a review it

includes a comprehensive reference section that includes many of the human

pheromone research integral to the understanding of this field of work.

Henry, H.L., and A.W. Norman. 2003. Encyclopedia of hormones . Vol. 1. Academic

Press, Amsterdam.

This is a three volume set that includes a detailed summary of human hormones.

It includes in depth information of hormone structures and simplifies the

complicated interactions of the major reproductive hormones. This reference was

also useful as it provided an explanation of important reproductive events such as

ovulation, the formation and degredation of the corpus luteum, and menses. In

order to gain a complete understanding of the female reproductive cycle it is

crucial to recognize the interplay of the variety of hormones and their effects and

this encyclopedia contains an explanation of all of this information allowing one

to gain a thorough understanding from a single resource.

Hrdy, S.B. 1979. Infanticide among animals: a review, classification, and

examination of the implications for the reproductive strategies of females.

Ethol. Sociobiol. 1: 13-40.

Hrdy argues that concealed ovulation was developed in response to the selective

pressure generated by the practice of infanticide. Through a continual display of

estrous females were better able to conceal ovulation until the eventual depression

of these signs completely. Hrdy argues that males who are unaware of female

fertility will subsequently be unsure of what offspring they sired and as a result be

less likely to harm these offspring. Therefore, concealed ovulation served to

decrease male aggression and enhance female reproductive success. Hrdy’s

article is useful, but it contains detailed information about other aspects of primate

reproductive strategies which make it a long read.

Hrdy, S.B., and P.L. Whitten. 1987. Patterning of sexual activity, pp. 370-384 in

Primate societies . Edited by B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W.

Wrangham, and T. T. Struhsaker, University of Chicago Press, Chicago.

This is a comprehensive analysis of a variety of primate reproductive cycles,

behaviours, characters, and their timeframes. Hrdy and Whitten obtain their

information from an assortment of researchers so there is a possibility for

inconsistencies in data collection and the quantification of observations.

However, this is a commonly cited source and continues to be viewed as highly

reliable almost a decade after its publication. Overall, this is an excellent resource

because of the large amount of detailed information on numerous primates.

Hutchins, M., D.G. Kleiman, V. Geist, and M.C. McDade. 2003. Grzimek's Animal

Life Encyclopedia - Mammals . 2 nd ed. Vol. 14. Gale Group, Farmington Hills.

This resource is ideal for anyone with little knowledge about individual primate

species. It provides an overview of each major family that includes a detailed

description of each group’s reproductive characteristics. In addition, this

encyclopedia provides a description of the several representative species from

each family with several specific details regarding their mating behaviours and

accompanying physiological manifestations of ovulation.

Manson, W.C. 1986. Sexual cyclicity and concealed ovulation. J. Hum. Evol. 15: 21-

30.

Manson discusses the possibility that human ovulation is not concealed and

reviews research regarding periods of sexual arousal, coital distribution, and

possible hormone correlates. Manson also suggests it is possible that the overt

sexual displays of non-human primates were lost as a result of the stance adopted

to facilitate bipedal locomotion. This resource was not used in this thesis, yet it

provides insight when considering the merits of Spuhler’s (1979) argument for the

influence of bipedal locomotion and continual sexual receptivity on the

concealment of ovulation.

Møller, A.P., and M.D. Jennions. 2001. Testing and adjusting for publication bias.

Trends Ecol. Evol. 16: 580-586.

This article investigates the possible influences of publishing biases through six

statistical methods of testing. Although a background in statistics is required to

understand the statistical methods offered, the article provides useful examples of

publication bias and suggestions regarding how to avoid frequent causes of bias.

Nunn, C. L. 1999a. The evolution of exaggerated sexual swellings in primates and

the graded signal hypothesis. Anim. Behav. 58: 229-246.

Nunn provides an extensive review of past research on sexual swellings in

primate species. He also addresses previous theories explaining the evolution of

sexual swellings, critiquing each and providing his own theory the graded signal

hypothesis. In his hypothesis Nunn posits that males are interested in maximally

swollen females as the swellings that they produce are a relatively reliable

indicator of fertility.

Palter, S.F., and D.L. Olive. 2002. Reproductive Physiology, pp. 159-168 in Novak’s

Gynocology 13 th ed . Edited by J.S. Berek. Lippincott Williams and Wilkins,

New York.

The physiology of the reproductive cycle is explored in this chapter of Novak’s

Gynocology . The information provided is most useful in its explanation of the

different phases of the reproductive cycle. Since the menstrual cycle has no true

start or end, confusion can occur; therefore, clear divisions of the reproductive

cycles and the events occurring in each are critical to ones understanding. The

information presented is well detailed, yet succinct enough that someone without

a background in human reproduction could comprehend the menstrual cycle.

Additionally, numerous useful diagrams are presented in this chapter. These

diagrams serve to reinforce the text and as an aid for clarification.

Pawlowski, B. 1999. Loss of oestrus and concealed ovulation in human evolution.

Curr. Anthropol. 40: 257-275.

Pawlowski provides a description of possible factors that may have led to the

development of concealed ovulation in humans. The possibility of pheromones as

a form of communication is considered as well as the influence of the menstrual

cycle on mating frequency. Pawlowski’s article is most useful as a resource to

find other relevant articles, both theorizing about the advantages and evolution of

concealed ovulation, as well as on other related topics such as pheromones.

Schröder, I. 1993. Concealed ovulation and clandestine copulation: A female

contribution to human evolution. Ethol. Sociobiol. 14: 381-389.

In this article it is argued that females concealed their ovulation to allow them

enhanced success in EPCs. In contrast to Benshoof and Thornhill’s (1979)

arguments, Schröder suggests that females chose to mate with subordinate males

to promote their status within groups where dominance was highly dependant on

the relationships among kin. Schröder’s arguments are interesting; however,

some aspects of her theory are confusing due to several inconsistencies in her

argument.

Sievert, L.L. & Dubois, C.A. 2005. Validating signals of ovulation: do women who

think they know, really know? Am. J. Hum. Biol. 17: 310-320.

The participants of this study are all ovulating females who believe that they can

discern their periods of fertility without the assistance of hormonal assay. Sievert

and Dubois test the knowledge of participants through the use of hormonal assay

finding that approximately 14% of the population would be correct in identifying

their time of ovulation.

Sillén-Tullberg, B., and A.P. Møller. 1993. The relationship between concealed

ovulation and mating systems in anthropoid primates: A phylogenetic

analysis. Am. Nat. 141: 1-25.

In this article the evolution of concealed ovulation is investigated based on

phylogenetic reasoning. The possibility that mating systems were the primary

force influencing the development of concealed ovulation is considered

extensively and several evolutionary trees are provided as a means to rationalize

how many times estrous was lost in groups with differing mating systems. Based

on the trees constructed it is determined that ovulatory signs were lost 0-1 times

under monogamy and 8-11 times in other mating systems (placed into one group).

Therefore, it is concluded that concealed ovulation developed in a non-

monogomous context and it is implied that the loss of ovulatory signals may have

served as a factor influencing the development of mating systems. An

understanding of phylogenetics is useful when reading this article as sometimes

the reasoning used relies heavily upon the principles employed in this field of

science. This article was a useful resource in providing information about the

mating systems and degrees of sexual swelling in many species of primates.

Song, F., A.J. Eastwood, S. Gilbody, L. Duley, and A.J. Sutton. 2000. Publication

and related biases. Health Technol. Assess. 4: 1-115.

These authors examine the probability of publication bias in medical research

finding that it is notably present. Eight factors are identified as either the cause of

publication bias or as issues that lead to the enhancement of bias. This resource

provides many examples of publication bias and their influences on the research

they are present in. Additionally, this article proposes several courses of action

that could safeguard against bias.

Speroff, L., and M.A. Fritz. 2005. Clinical Gynecologic Endocrinology and Infertility

7th ed . Lippincott Williams and Wilkins, New York.

This text provides detailed information about the hormonal changes throughout

the menstrual cycle. In addition, it discusses the role of each hormone and its

impact on the physiological changes occurring throughout the menstrual cycle.

Steklis, H.D., and C.H. Whiteman. 1989. Loss of estrus in human evolution: Too

many answers, too few questions. Ethol. Sociobiol. 10: 417-434.

Steklis and Whiteman provide a brief overview of past theories and then address

possible confounds that have impacted our research. As well, our perception of

our own species is investigated and Steklis and Whiteman attempt to discern why

the human-animal dichotomy exists.

Strassmann, B.I. 1981. Sexual selection, paternal care, and concealed ovulation in

humans. Ethol. Sociobiol. 2: 31-40.

Strassmann’s article expands on the arguments of Alexander and Noonan (1979).

However, Strassmann suggests that it would have been unlikely that successful

male polygynists would have changed reproductive strategies to favour one that

would lessen their reproductive success. Instead she argues that concealed

ovulation evolved in response to females opting for enhanced paternal care over

superior genes and thus males who wanted any reproductive success had to

conform and provide parental care, thus depleting their ability to acquire multiple

mates.

Strassmann, B.I. 1996. Menstrual hut visits by Dogon women: A hormonal test

distinguishes deceit from honest signaling. Behav. Ecol. 7: 304-315.

Although this research was not extensively investigated in this thesis it is an

interesting body of work. In Dogon society females are forced to honestly

displacy their fertility by visiting a menstrual hut during menses to decrease

chances of adultery and the conception of illegitimate children. Strassmann finds

through hormone analysis that females are honest in the reports of menses 86% of

the time. This is particularly useful study as it examines an African population

that has retained most of their traditional aspects of life and has been only slightly

influenced by external Westerners.

Tarín , J.J., and V. Gómez-Piquer. 2002. Opinion: Do women have a hidden heat

period? Hum. Reprod. 17: 2243-2248.

This article investigates past research examining the possibility of the phases of

the menstrual cycle influencing coital rates and attractivity, as well as the effect of

pheromones on human sexual behaviour. The information provided in this article

is useful as it summarizes most of the significant research conducted in the areas

listed above. However, the article is not critical of any of the reported studies,

assuming the complete validity of each which may be incorrect in some cases.