Human Sperm Competition: Copulation, masturbation and infidelity

Douglas

About the Authors

Robin Baker

Born in Wiltshire, England, in 1944, Robin Baker grew up in the small village of Manningford Bruce in the Vale of Pewsey. After obtaining a First Class Honours degree in Zoology (1965), then a PhD, at the University of Bristol (1968), he lectured in Zoology for over 25 years at the Universities of first Newcastle-upon-Tyne and then Manchester. At Manchester he was Reader in Zoology in the School of Biological Sciences from 1981-1996. In 1996 he left academic life to concentrate on his career in writing and broadcasting. A best-selling author in the field of sexual biology, his books (6 academic, 4 popular science, and 3 novels) have been translated into 28 different languages. He has also published around 100 scientific papers and articles and his work and ideas on the evolution of human behaviour have been featured in many radio and television programmes around the world. Since 2002 he has lived in the foothills of the Spanish Sierras with his partner and their family. He has six children and three grandchildren.

Mark A. Bellis

After working for many years on the evolution of human behaviour, Mark turned his behavioural research to the improvement of population health. Since then he has led national and international research programmes to tackle alcohol and drug misuse, improve sexual health and prevent violence. He has published over 140 academic papers primarily on the relationships between human behaviour and health, and as Professor of Public Health at Liverpool John Moores University established and directed one of the UK's largest public health research departments. Professor Bellis is now Director of Policy, Research and Development for Public Health Wales; leading developments in public health policy nationally and working internationally with bodies including the World Health Organization and other arms of the United Nations. Mark is visiting Professor of Public Health at Liverpool John Moores University and holds honorary chairs in the Schools of Medicine at both Cardiff and Swansea Universities.

Dedications

RRB

To Liz, for being open-minded, and

to Nathanial, for being the first flowback baby

MAB

To my wife Georgie and my children Aaron, Jack and Molly

– my whys and the wherefores

Table of Contents

About the Authors

Dedications

Table of Contents

Frontispiece

Preface to Digital (2014) Publication

Preface to Original (1995) Publication

Acknowledgements

1 Introduction

2 Sex, coyness and promiscuity: the evolution of sperm competition

2.1 Introduction

2.2 Evolutionary inheritance: a programme for a lifetime

2.3 Human sexuality: the basics

2.3.1 Sex, gender and the sex ratio

2.3.2 Urgent males and coy females

2.4 Polyandry and sperm competition: a pre-vertebrate legacy

2.4.1 Polyandrous females

2.4.2 Sperm competition and double-mating

2.4.3 Spermatogenesis and male sperm storage organs

2.4.4 Mate-guarding by males

2.5 Sperm competition theory

2.5.1 The lottery principle

2.5.2 Sperm size and competitiveness

2.5.3 Sperm warfare and the Kamikaze Sperm Hypothesis

2.5.4 Restraint in sperm ejaculation

2.5.5. How many sperm should be ejaculated?

2.5.6 Females should promote sperm competition

Boxes for Chapter 2

Box 2.1 A suggested history of the different facets of human sexuality

Box 2.1a A suggested course for the human lineage during its pre-vertebrate phase of evolution (adapted from Margolis 1981).

Box 2.2 Reproduction: the currency of natural selection

Box 2.3 Sexual reproduction

Box 2.4 Anisogamy and the male-female phenomenon

Box 2.5 Evolution and maintenance of a 1:1 sex ratio

Box 2.6 A nationwide survey (1989) of the level of polyandry and other sexual behaviour of British females

Box 2.7 Urgent males; coy females

Box 2.8 Polyandrous females: modes of sexual activity

Box 2.9 Minimum time intervals between successive copulations with two different males by females at different levels of sexual experience

Box 2.10 Sperm production and storage (In part adapted from Johnson and Everitt, 1988)

Box 2.11 The efficiency and evolution of mate-guarding by males

Box 2.12 Sexy sons, sexy daughters and handicaps: the successful child principle in the evolution of female sexual behaviour

3 Legacies from the age of reptiles: copulation, flowback and the female orgasm

3.1 Introduction

3.2 Internal fertilization and sexually transmitted diseases

3.3 The male: copulation, seminal fluids and copulatory plugs

3.3.1 Intromittent organs and copulation

3.3.2 Seminal fluids

3.3.3 Copulatory plugs

3.3.4 The antiquity of copulation and insemination in the human lineage

3.4 Forced copulation

3.5 The female: sperm storage organs, flowbacks and copulatory orgasms

3.5.1 Sperm storage organs in the female

3.5.2 The flowback: female ejection of sperm

3.5.3 Female copulatory orgasm

3.5.4 The antiquity of sperm storage and manipulation by females of the human lineage

Boxes for Chapter 3

Box 3.1 A suggested course for the human lineage during its premammalian phase of vertebrate evolution. (Adapted from Pough et al., 1990.)

Box 3.2 In vitro fertilization (IVF) and embryo transfer (ET)

Box 3.3 The behavioural ecology of rape

Box 3.4 The reproductive tract of the human female

Box 3.5 Cervical mucus

Box 3.6 The evolution of sperm storage organs in females

Box 3.7 Written instructions for the collection of flowback samples

Box 3.8 A direct study of whole ejaculates and flowbacks

Box 3.9 The subjective estimation of flowback volume

Box 3.10 Frequency distribution of number of sperm in whole inseminates (collected by condom) and ejected in flowbacks

Box 3.11 Ejection of flowback by female Grevy’s zebra

Box 3.12 Course and timing of female copulatory orgasms in humans

4 The mammalian inheritance: maternal care, family planning, and sperm polymorphism

4.1 Introduction

4.2 Maternal care, viviparity and lactation

4.2.1 Maternal care and lactation

4.2.2 Viviparity and pregnancy

4.3 The female tract: the arena for sperm competition

4.4 Family planning and contraception: the female perspective

4.4.1 Contraception: avoiding copulation

4.4.2 Contraception: prepuberty and menopause

4.4.3 Contraception: avoiding ovulation from puberty to menopause

4.4.4 Contraception: copulation at infertile stages of fertile menstrual cycles

4.4.5 Contraception: short-lived eggs

4.4.6 Contraception: sperm longevity in the female tract

4.4.7 Contraception: the timing of ovulation

4.4.8 Contraception: control of sperm numbers

4.4.9 Avoiding pregnancy: failure to implant

4.4.10 Avoiding development: polyspermy

4.4.11 Avoiding birth: spontaneous abortion

4.4.12 Avoiding maternal care: infanticide

4.4.13 Optimizing family structure: influencing the sex ratio

4.4.14 Optimizing family structure: influencing paternity after insemination

4.4.15 Optimizing family structure: producing helpers

4.4.16 Antiquity of female family planning

4.5 Male genitalia: size and location of testes

4.5.1 Testis size

4.5.2 Testis location

4.6 Sperm polymorphism

4.7 Ordered ejaculates

Boxes for Chapter 4

Box 4.1 A suggested course for the human lineage during its mammalian phase of evolution (Redrawn and adapted from Novacek, 1992)

Box 4.2 The behavioural ecology of parental care

Box 4.3 Maternal care in the animal kingdom

Box 4.4 Lactation, breasts and nipples

Box 4.5 Viviparity, pregnancy and the placenta

Box 4.6 Ovulation and menstruation: the menstrual cycle

Box 4.7 Energetics of female reproduction: fat distribution, body weight and nutrition

Box 4.8 Variation in copulation rate

Box 4.9 The duration of maternal care and the evolution of puberty

Box 4.10 Anovulatory menstrual cycles

Box 4.11 Longevity of mammalian sperm

Box 4.12 Spontaneous and induced ovulation in mammals

Box 4.13 Spontaneous abortion

Box 4.14 Sex ratio of offspring as a function of social status: the Trivers-Willard hypothesis

Box 4.15 Parental manipulation

Box 4.16 Down’s syndrome: sterile helpers?

Box 4.17 Male-male variation in testis size, rate of sperm production and involvement in sperm competition

Box 4.18 Testis location

Box 4.19 Sperm shape and polymorphism in humans and other mammals

Box 4.20 A study of sperm in the different spurts of the human ejaculate

5 The mammalian inheritance: masturbation, homosexuality and push buttons

5.1 Introduction

5.2 Orgasms in a lifetime

5.3 Types of non-copulatory orgasms

5.3.1 Spontaneous (nocturnal) orgasms

5.3.2 Self-masturbation

5.3.3 Heterosexually stimulated non-copulatory orgasms

5.3.4 Homosexually stimulated non-copulatory orgasms

5.4 Interaction between copulation and the different types of non-copulatory orgasm

5.5 The distribution of non-copulatory orgasms through the menstrual cycle in females

5.6 The function of non-copulatory orgasms

5.6.1 Behavioural polymorphism

5.6.2 Male self-masturbation and nocturnal emission

5.6.3 Female self-masturbation and nocturnal orgasm

5.6.4 Orgasm crypsis

5.6.5 Homosexuality

5.7 ‘Push-buttons’: the clitoris, nipples and masturbation

5.7.1 Push-button power

5.7.2 The evolutionary history of male nipples

5.7.3 The evolutionary history of the human clitoris

Boxes for Chapter 5

Box 5.1 Variation with age in incidence of ejaculation (males) and orgasm (females) (USA, 1940s)

Box 5.2 Frequency with which first lifetime orgasm is non-copulatory or copulatory (USA, 1940s; UK 1980s)

Box 5.3 Variation with age in the incidence and frequency of homosexual, nocturnal and self-masturbatory ejaculations (males) and orgasms (females) (USA, 1940s)

Box 5.4 Influence of intercopulation interval on probability of males and females experiencing a non-copulatory orgasm (self-masturbatory or nocturnal) between copulations

Box 5.5 Mean time interval between different sexual events for males and females

Box 5.6 Mean time interval from copulation to first non-copulatory orgasm of different types

Box 5.7 Distribution of different types of non-copulatory orgasm experienced by females during different types of menstrual cycle

Box 5.8 Variation with age in daily sperm production and rate of ejaculation (USA)

Box 5.9 Relationship between daily sperm production, mean ejaculation interval and proportion of time spent with partner between copulations (Manchester, UK)

Box 5.10 Relationship for females between frequency of copulation and frequency of non-copulatory orgasms (UK)

Box 5.11 Lack of influence of orgasm at last copulation on probability of self-masturbation or nocturnal orgasm before next copulation at three different intercopulation time intervals (females, Manchester, UK

Box 5.12 Reproductive success of bisexual and heterosexual women at different ages (UK)

Box 5.13 Index of differences between women with and without lesbian experience when controlled for age (UK)

Box 5.14 Distribution during the menstrual cycle of male-associated events experienced by females with and without lesbian experience

Box 5.15 Variation with age in differences in risk of genital tract problems for women with and without lesbian experience (UK)

Box 5.16 The clitoris

6 The primate inheritance: paternal care, sexual crypsis and the façade of monandry

6.1 Introduction

6.2 The primate inheritance: parental and mating systems

6.2.1 Paternal care

6.2.2 Systems of biparental care: monogamy and polygamy

6.3 The primate inheritance: infidelity

6.3.1 Female infidelity

6.3.2 Male infidelity

6.4 The primate inheritance: male contraception

6.4.1 Spiteful copulation

6.4.2 Withdrawal

6.5 The hominid inheritance: female sexual crypsis

6.5.1 The behavioural ecology of sexual swellings

6.5.2 The evolution of sexual crypsis and monandry

6.5.3 Infidelity’s accomplice: the behavioural ecology of sexual crypsis

6.6 How cryptic is female fertility in humans?

6.6.1 Ancient beliefs, modern knowledge

6.6.2 Menstruation and sexual crypsis

6.6.3 Cervical mucus and sexual crypsis

6.6.4 Pheromones and sexual crypsis

6.6.5 The pain of ovulation?

6.6.6 Menstrual synchrony: no threat

6.6.7 Copulation during pregnancy: the final touch

6.6.8 How successful is sexual crypsis by human females?

6.7 The hominid inheritance: permanently pendulous breasts

6.8 The hominid inheritance: penis size, shape and function

6.8.1 Penis size and shape

6.8.2 Plugs and penises

6.8.3 The piston penis

6.8.4 The evolution of plugs in primates

6.8.5 Thrusting and copulation duration

6.8.6 Copulatory position

6.8.7 The human penis: an evolutionary sequence

Boxes for Chapter 6

Box 6.1 A suggested course for the human lineage during its primate and hominid phases of evolution

Box 6.2 The evolution of paternal care

Box 6.3 Monogamy and polygamy

Box 6.4 Human mate choice

Box 6.5 The behavioural ecology of infidelity

Box 6.6 Why is infidelity so subtle and sophisticated?

Box 6.7 Some taxa of anthropoid primates with sexual swellings

Box 6.8 Some taxa of anthropoid primates with sexual crypsis

Box 6.9 The relationship between cervical mucus symptoms and ovulation

Box 6.10 The timing of in-pair (IPCs) and extra-pair copulations (EPCs) in relation to fertility during different phases of the human menstrual cycle

Box 6.11 Female activity in relation to fertility during the human menstrual cycle

Box 6.12 Penis size, shape and structure in primates

Box 6.13 The human penis as a suction piston for sperm removal

Box 6.14 Summary of two major phylogenetic sequences in the evolution of level of female sexual crypsis, penis structure and function, and copulation behaviour in the anthropoid primates

Box 6.15 Copulation position and juxtaposition of penis and cervix during copulation

7 The modern scenario: contraception, fecundity and the illusion of conscious control

7.1 Introduction

7.2 Modern embellishments

7.2.1 Modern contraception

7.2.2 Reduced fecundity

7.2.3 Elevated infertility: clinical and behavioural

7.3 Conscious and subconscious sexual strategy

7.4 Natural selection on modern humans

Boxes for Chapter 7

Box 7.1 Modern contraceptives

Box 7.2 Female fecundity in various countries (c. 1980)

Box 7.3 The demographic transition and use of contraceptives in the UK

Box 7.4 Family size in relation to life expectancy and use of contraceptives in various countries

8 Levels of human sperm competition

8.1 Introduction

8.2 Sperm competition: where and for how long do sperm live in the human female?

8.2.1 Sperm competition and the flowback

8.2.2 The fate of sperm which remain in the female tract

8.2.3 Differences of opinion

8.3 How often, how many, how long: the statistics of double-mating

8.3.1 What proportion of males place their sperm in competition?

8.3.2 What proportion of females generate sperm competition?

8.3.3 Double-mating, contraception and sperm competition

8.3.4 Do females promote sperm competition?

8.4 The pay-off

8.4.1 What proportion of children are the result of sperm competition?

8.4.2 Which male does best: first or last, extra-pair or in-pair?

Boxes for Chapter 8

Box 8.1 The relationship between Basal Body Temperature (BBT) curves and ovulation

Box 8.2 Variation in human double-mating rate with age and sexual experience (UK)

Box 8.3 Association between double-matings, contraceptive use, and fertility (UK)

Box 8.4 Studies of paternal discrepancy

9 Optimizing inseminates: ejaculate adjustment by males and the function of masturbation

9.1 Introduction

9.2 Variation in number of sperm inseminated during in-pair copulation (IPC)

9.2.1 Male response to risk of sperm competition

9.2.2 ‘Topping-up’ the partner

9.2.3 Male response to female value

9.3 Number of sperm inseminated during extra-pair copulation (EPC)

9.4 Masturbation: features and function

9.4.1 Numbers and circumstance

9.4.2 Time since last ejaculation

9.4.3 Differences between males

9.4.4 The function of masturbation

9.5 Seasonal variation in the number of sperm ejaculated

9.5.1 Masturbatory ejaculates

9.5.2 Copulatory ejaculates

9.6 Long-term changes in the number of sperm ejaculated (1938-1990)

9.7 Why do males show restraint in size of inseminate?

9.7.1 Is there an advantage in saving sperm for a future copulation?

9.7.2 Is restraint an advantage or disadvantage at the current copulation?

9.7.3 Restraint: conclusion

9.8 When and how do males adjust sperm number?

Boxes for Chapter 9

Box 9.1 Predicting the number of sperm ejaculated during IPC and masturbation

Box 9.2 Number of sperm inseminated during IPC varies according to the risk of sperm competition and testis size.

Box 9.3 Topping up the female: number of sperm inseminated during IPC varies with inter-IPC interval

Box 9.4 Association between number of sperm inseminated during in-pair copulation and male and female stature

Box 9.5 Predicted and observed number of sperm inseminated during in-pair copulation, extra-pair copulation and double-mating

Box 9.6 Variation in number of sperm ejaculated during masturbation in relation to sociosexual situation.

Box 9.7 Influence of male self-masturbation on the number of sperm inseminated (by the male) and retained (by the female) at the next copulation

Box 9.8 Seasonal variation in number of sperm ejaculated during masturbation

Box 9.9 Lack of correlation in the number of sperm a male ejaculates during masturbation and copulation

Box 9.10 Seasonal variation in the number of sperm inseminated during copulation as a function of probability of conception

Box 9.11 Long-term changes (1938—90) in the number of sperm ejaculated during masturbation

Box 9.12 Ejaculation and potential stages for adjusting the number of sperm in the ejaculate

10 Ejaculate manipulation by females and the function of the female orgasm

10.1 Introduction

10.2 Male and female influences on sperm retention

10.3 Human flowbacks: general features

10.4 Oral contraceptives, pregnancy and flowbacks

10.5 Are male strategies generally successful?

10.6 The female orgasm and sperm retention

10.6.1 The poleaxe hypothesis: falls down

10.6.2 The upsuck hypothesis: taken up

10.6.3 Masturbatory, nocturnal and other intercopulatory orgasms

10.6.4 Blocking sperm?

10.6.5 Undoing the block: the basis of female strategy

10.7 Menstruation and sperm retention

10.8 Female orgasm, sperm retention and sperm competition: the female strategy

10.8.1 In-pair copulations and monandry

10.8.2 In-pair copulations and polyandry

10.8.3 Extra-pair copulations

10.9 How does the female orgasm influence sperm retention? A hypothesis

10.9.1 Copulatory orgasms

10.9.2 Non-copulatory orgasms

10.10 The cryptic mating game: male—female conflict and cooperation over sperm

10.10.1 Ejaculate manipulation by females in the absence of sperm competition

10.10.2 Ejaculate manipulation in the presence of sperm competition

10.10.3 Sperm retention and mobilization in the absence of fertilization

10.10.4 Individual variation in female strategies

Boxes for Chapter 10

Box 10.1 Separating male and female contributions to sperm retention

Box 10.2 Equation to calculate the number of sperm retained during in-pair copulation in different sociosexual situations

Box 10.3 Some general features of flowbacks

Box 10.4 The average success of male strategies

Box 10.5 A test of the upsuck hypothesis: female orgasm and sperm retention

Box 10.6 Intercopulatory orgasms and the retention of sperm at the next copulation

Box 10.7 The influence of sperm from one copulation on the retention of sperm from the next copulation

Box 10.8 Orgasm regimes and sperm retention levels

Box 10.9 Female sperm retention strategy in monandry and polyandry: data from a UK Nationwide survey

Box 10.10 Seasonal variation in level of sperm retention by females in relation to probability of conception

Box 10.11 Females faking orgasms

11 Sperm polymorphism and the Kamikaze Sperm Hypothesis

11.1 Introduction

11.2 The evolution of sperm size and shape

11.2.1 The functional anatomy of human sperm

11.2.2 Is sperm size, shape and behaviour determined by the male or the sperm?

11.2.3 Sperm size

11.2.4 Sperm shape

11.2.5 Sperm polymorphism

11.3 Kamikaze sperm: four hypotheses

11.3.1 Sperm with coiled tails: an ageing block

11.3.2 Macros and micros: hares and tortoises in the human ejaculate?

11.3.3 Oval-headed sperm: seek-and-destroyers?

11.3.4 Tapering and pyriform sperm, male stress and spiteful insemination

11.3.5 Kamikaze sperm: a summary

11.4 How do males adjust level of polymorphism?

11.4.1 Morph differentiation during spermatogenesis and maturation

11.4.2 Ontogenetic transformation

11.4.3 Selective reabsorption and/or phagocytosis

11.4.4 Varying the size of the ejaculate

11.4.5 Environmentally induced transformation

11.5 The kamikaze sperm hypothesis: an evaluation

11.6 The ejaculate as a male organ

Boxes for Chapter 11

Box 11.1 Swimming performances of four different tail morphs

Box 11.2 An empirical test of the hypothesis that the main ‘blocker’ sperm are sperm with coiled tails

Box 11.3 The swim-up process and Human Tubal Fluid Medium (HTFM) used in experiments on live sperm

Box 11.4 The proportion of sperm with coiled tails increases as sperm age

Box 11.5 Variation in retention by the female of sperm of different morphologies

Box 11.6 Variation in the number of coiled tail sperm inseminated during copulation in relation to risk of sperm competition

Box 11.7 Oval-headed sperm: influence of head size on swimming performance, longevity and retention by the female.

Box 11.8 A study of sperm behaviour and survival when in the presence of sperm from another male

Box 11.9 Summary of results from mixing experiments: the response of sperm to encountering sperm from another male

Box 11.10 The acrosome reaction

Box 11.11 The MTP ratio, male fertility, stress and male family planning

Box 11.12 Male control of sperm polymorphism: the time and the place

12 Human fertility and infertility: the kamikaze perspective

12.1 Introduction

12.2 How many egg-getters?

12.2.1 What is an egg-getter?

12.2.2 So how many human sperm in an ejaculate are egg-getters?

12.2.3 How many egg-getters reach the oviduct?

12.2.4 Which morph is the egg-getter: the macro credentials

12.3 Maturation, ejaculation, capacitation and fertilization: three views of sperm ontogeny

12.3.1 The standard view: a steady trickle of ripe sperm

12.3.2 Cohen’s view: a tale of two sperm

12.3.3 The kamikaze view: a job for all ages

12.4 Kamikaze sperm and differences in fertility

12.4.1 Ejaculates and fertility: gross associations

12.4.2 Fertility indices: ‘normality’ evaluation vs MTP ratio

12.4.3 Sperm morphology and polyspermy

12.4.4 Sperm for assisted conception: masturbation vs copulation

12.4.5 Kamikaze sperm in competition

12.4.6 Kamikaze problems in fertility

Boxes for Chapter 12

Box 12.1 Two hypotheses for the nature of egg penetration in eutherian mammals

Box 12.2 The MTP ratio of the ejaculate as a predictor of success in IVF and AID-assisted conception treatment

13 Final thoughts

References

Suggested search terms

Frontispiece

The two sequences show facets of sperm behaviour unfilmed before 1994.

(A1-A3) An apparently normal and still alive sperm ‘metamorphoses’ into a coiled-tail sperm in a single (unmixed) ejaculate. The sequence shown took about 20 seconds. In a further five minutes the sperm was as coiled as the sperm in the top left of A3. Both sperm were still moving.

(Bl-3) Possible ‘seek-and-destroy’ behaviour by modal oval-headed sperm in a heterospermic mix of ejaculates from two different males. The pair of sperm (diad) were filmed for 30 minutes attached at the head. Both were active when first seen but by B1 the left-hand sperm was inactive, apparently dead. The surviving sperm, attached at the head tip, spent 15 minutes rotating on its long axis (B1-B2) before eventually breaking free and swimming off (B3).

Sequences taken from a video film made by Suzanne Jackson, Robin Baker, Chris Bainbridge and Karin Halliday, School of Biological Sciences, University of Manchester, using equipment provided by the British Broadcasting Corporation Natural History Unit, Bristol, and Nikon

Preface to Digital (2014) Publication

This book was written 20 years ago in 1993-94 and published in 1995. Yet despite its age we consider it to be as relevant now as it was two decades ago. Perhaps even more relevant, because since our demonstration that Human Sperm Competition could actually be studied in a variety of ways a number of research groups have taken up the challenge where we left off. Gratifyingly, most of these groups have obtained results that have built firmly upon our early work. A few others have created important dialogues. None though have destroyed any crucial part of the foundation that we first lay down in this book. But the main way in which our book remains relevant to this day is that for various reasons – some cultural, some procedural, and yet others due to sheer opportunity – we were able to do a number of experiments that others since have not had the opportunity to repeat. And the results of those unique experiments of ours are presented in this book and nowhere else. For these different reasons we have been under pressure for some time from students in the fields of human sexuality and human sperm competition to make our book more generally available. But until now, copyright issues have prevented us from doing so, and even now an e-book is the only avenue open to us.

When this book was first published in hardback by Chapman and Hall, London, e-books were only just being mooted and not yet a standard item on authors’ contracts – which in this particular instance is probably just as well. Like most academic authors at the time we signed away control of just about everything concerning our book in the initial contract. Not least was the price, which over the years has soared to a point where no sensible individual would buy it. Yet we know from a succession of requests, even pleas, that there are many people who would like to read our work but simply cannot, not only because of the price but also because library waiting lists often stretch into months. But early in 2014 The Susijn Agency Ltd (RRB’s agent) managed to clarify the position with regard to digital rights with the current hardback publishers (Springer). This cleared our way to proceed with this digital edition and to publish at a student-friendly price over which we have made sure we retain some control.

Those familiar with the print edition will notice that some changes in layout have been necessary to accommodate the digital medium. Boxes containing figures and tables have needed to be moved from their original position in the text. However, Hyperlinks to each Box have been added for easy navigation, and those readers using devices with a Back button can then easily return to the page of the main text that they were reading. Although the publishers have made sure that everything in the original version is included and legible, the reader may at times need to change the size of an image on their screen, depending on the reading device being used.

This edition is intended to be simply a digital version of our original 1995 publication. Tempting though it was to add data collected since (not only by us but also and mainly by others) and to open new dialogues we have resisted. Maybe a revised and updated edition will come later, but here we have restricted ourselves to correcting the few typographical errors in the original and adding the odd clause of clarification (probably no more than five in the whole book). There is one matter though that we feel we have to address here, because clear though we thought we had been in our original publication, this issue seems to have caused unexpected confusion in some quarters.

In the days before machines could do the job much, much faster, all of our studies of sperm morphology were carried out by eye down the microscope. Sperm were categorised morphometrically, by shape, not micrometrically, by measurement. We followed the World Health Organization classification of sperm types as given in the Human Semen Manual (Belsey et al., 1987) – see Box_4.19 for details. In all of our data, therefore, any oval-headed sperm with a head longer than 5 μm and wider than 3 μm was recorded as a Macrocephalous sperm. We were well aware that a small proportion of these were actually yet-another sperm-type with a diploid chromosome content and hence infertile, but in our data we could not separate these out from the majority of Macrocephalous sperm that are haploid and potentially fertile. Nor did we see any pressing reason to do so – because the presence of this diploid, infertile subset in our Macro data makes no difference to any of the conclusions we reach, much as it may amuse some people to suggest that it does.

Robin Baker

Mark Bellis

May 2014

Preface to Original (1995) Publication

The romantic and traditional view of sexual reproduction is as the one phase of an animal’s life when it cooperates totally with another individual (a member of the opposite sex) for their mutual benefit (the production of offspring). In contrast, behavioural ecologists see reproductive cooperation as a brief period when the biological interests of a male and female just happen to coincide. Even then, each sex is continuously vigilant for ways of promoting its own fitness at the expense of its partner’s. According to this view, reproduction is a mating game; a subtle mixture of conflict and cooperation between the sexes.

By definition, most mating by monogamous species is in-pair copulation (IPC). However, an apparently universal feature of such species is that from time to time both sexes engage in extra-pair copulation (EPC). Although their own infidelity may be advantageous to both males and females, either may suffer through their partner’s infidelity. Males risk cuckoldry or loss of the female to another male. Females risk reduced paternal care or loss of the male to another female. In response to these disadvantages, behavioural ploys have evolved in both sexes to attempt to reduce levels of partner infidelity.

The mating game does not only occur at the level of overt behaviour. Equally powerful aspects are played out cryptically within the female reproductive tract. For example, a special category of EPC is double-mating (the female mating with a second male while still containing competitive sperm from one or more previous males). The result is ‘sperm competition’ as the sperm from different males compete to fertilize the female’s egg(s).

Models of sperm competition tend to view the female tract as a passive receptacle in which males play out their sperm competition games. Females have the potential, however, to influence the outcome of the contest in several different ways. Not least, females may physically eject more sperm from some inseminations than others.

Throughout most of his hominid evolution, the major part of the human population seems to have been ‘monogamous’ but with a range of subtle and sophisticated forms of infidelity. Many past and present populations show levels of EPC that indicate an evolutionary history of double-mating and sperm competition. We estimate that in Britain in the late 1980s, about 4% of children were conceived via sperm competition (i.e. were conceived while their mother contained within her reproductive tract competitive sperm from two or more different males).

Male humans respond to separation from a female partner by inseminating more sperm at their next copulation. Female humans, although not as blatant as some mammals, eject seminal fluid from their vagina after copulation. In view of the relative ease with which their ejaculates and relevant information can be collected, humans appear to be ideal subjects for the study of the cryptic mating game that takes place in the reproductive tract of female mammals. Yet, when we began our studies of human sperm competition in 1988, it was transparently clear that academically the area was virgin territory. We now know why.

The study of human sperm competition has led us into areas that many people consider to be taboo and to be unseemly as topics for academic consideration. An understanding of sperm competition demands information on patterns and levels of sexual behaviour, particularly levels of infidelity and double-mating. It also demands information on, and understanding of, such emotive and personal facets of human sexual behaviour as frequencies of copulation, rape, patterns of female orgasm, and levels of both male and female masturbation.

On the whole, our publications and lectures have been greeted worldwide with a gratifying level of interest. Most academics have responded with excitement and the question ‘why has nobody done this before?’. Perhaps in answer to this question, we have also met our share of people who, from the perspective of their own particular hang-up, view us as nothing better than scientific (or actual) voyeurs who have violated others at a most intimate and personal level.

In carrying out our research, we have two major aims. Our first is a purely scientific understanding of the reproductive behaviour of humans and other animals. As our approach is novel, the type of understanding we are promoting is novel.

Our second aim is medical. About 10% of couples are, at some time, clinically defined as infertile and many expensive treatments for infertility have, and are being, devised. A 1985 estimate calculated the cost of infertility to the USA alone to be $64 billion for infertility investigations and treatment of around 2 million infertile couples with only 14% success. Many of these treatments are lacking information from basic research, particularly on the factors that influence the fertility of sperm. In all modesty, we feel our research could revolutionize the medical approach to infertility.

In writing this book we have but one objective. In the space of just six years we have seen in our research implications for a wide range of disciplines, from sociobiology on the one hand to medicine and veterinary science on the other. Although we shall continue to publish papers in appropriate journals, we could never give the overview that we feel is the main strength of this work. In a book, such an overview is possible.

Although this book is concerned primarily with the sexual behaviour of humans, throughout we take the opportunity of placing human behaviour in the context of that of other animals. At the same time, we point out the implications of the work for the medical understanding and treatment of infertility.

We make no apology for open discussion in these pages of the mechanics and consequences of human infidelity, copulation, rape, masturbation and orgasm. In our view, the result is a better understanding of the way males and females are programmed to behave in sexual matters. If, as a consequence, each sex manages better to understand the behaviour and motivations of the other, we shall feel that our whole project has been more than worthwhile.

Acknowledgements

Our studies have depended on the voluntary cooperation of many people who have had the courage to allow us to examine some of the most intimate aspects and products of their sexual behaviour. We are grateful to them all.

We also thank all those students who played a part in organizing and distributing questionnaires (Emma Creighton, Dominic Shaw, Viki Cook and Jo Moffitt), or in counting and typing sperm (Jo Bell, Jill Bownass, Jill Brundie, Jill Chew, Penny Cook, Tiffany Derwent, Cheryl Durkin, Katie Ellisdon, Helen Fisher, Kath Griffin, Debbie Haynes, Louise Heywood, Dave Johnson, Andy Lang, Steve Lockley, Naomi Matthews, Heather Newton, Alex Norman, Richard Oliver, Simon Pearson, Liz Shields, Mary Southall, Katy Turner and Paul Wilson).

In publishing our nationwide questionnaire, Gill Hudson and Company magazine gave us access to a mine of information on female sexual behaviour. Jo Bell, Kath Griffin, and Phil Wheater helped with the mammoth task of transferring the questionnaire data onto computer. Drs Keith and Anna Richardson provided considerable medical guidance and Andrew Burdett provided the same guidance in the field of veterinary medicine. A number of other friends and colleagues have also made invaluable contributions to various aspects of our work (Dr Matt Gage, Rachel Alcock, Jayne Burdett and Deborah and Sean Cochrane).

We are extremely grateful to St Mary’s Hospital, Manchester for their help and collaboration over the past few years, particularly Dr Phil Matson and his staff at the IVF clinic and Anne Atkinson and her staff at the AID clinic.

Our work on sperm competition has been funded in part by the Science and Engineering Research Council; our work on menstrual synchrony by the Leverhulme Trust. We also thank Durex for their kind donation of condoms.

We have both benefited considerably over the years from discussions with the father of sperm competition, Professor Geoff. Parker (one of us, RRB, ever since 1962 when we began our undergraduate days together at the University of Bristol). If he had not started the whole study of sperm competition in 1970, we should not have enjoyed ourselves half as much since 1988 when we first decided to study the phenomenon in humans.

The manuscript was greatly improved by the typical and critical attention of Jack Cohen. More than anything, we benefited from his incredibly wide knowledge of all things reproductive and particularly through his eyes from seeing our book from the perspective of a non-behavioural ecologist.

Finally, we particularly thank both Dr Tamsin Peachey, for advice on all matters biochemical and for her part in developing our model for the function of the female orgasm, and Elizabeth Oram, for drawing our attention to the potential value of studying flowbacks and for her role in developing the techniques of flowback collection. Without this single development, a major part of the work reported in this book might never have begun.

1 Introduction

It is probably fair to say that both traditional biological and current medical doctrines tend to interpret the characteristics of human ejaculates as features essential to the process of fertilization. However, such traditional doctrines find it difficult to explain why, for example, at each insemination a human male ejaculates around 350 million sperm (apparently enough to fertilize all of the women in America) to fertilize a single egg.

Over the past two decades, behavioural ecologists, one of the most recent subgroups of the biological sciences, have begun to question this traditional view. They suspect instead that most of the conspicuous aspects of animal ejaculates are more the evolutionary product of a phenomenon known as sperm competition than the result of selection for the efficiency of fertilization. Indeed, they have even begun to suspect that some characteristics of mammalian ejaculates evolved for the purpose of sperm competition may even be detrimental to the fertilization of eggs (Baker and Bellis, 1993a).

Sperm competition is the competition between sperm from different males for the ‘prize’ of the fertilization of the egg(s) produced by a single female. In internal fertilizers, such as humans, such competition naturally takes place within the reproductive tract of a single female. The risk of sperm competition is thought to have influenced many aspects of sexuality, not only concerning sperm and the ejaculate but innumerable other aspects of male and female anatomy and physiology. Thus, sperm competition may be argued to promote not only highly competitive ejaculates but also to shape anatomical devices such as the penis and vagina and to generate a whole array of copulatory behaviour.

The importance of sperm competition in the shaping of sexual behaviour and anatomy was first pointed out for insects by Parker (1970a). Since then, however, behavioural ecologists have come to realize that sperm competition is a virtually universal phenomenon that has shaped the sexuality of nearly all animal lineages (see collection of papers in Smith 1984a). They suspect that every male of nearly every animal that exists today, including every male human, is the descendant of many generations of male ancestors who have either successfully avoided contests or whose sperm have been successful in contests with sperm from other males. It is not surprising then that the stage has been reached when interpretation of human ejaculates as well as human sexual behaviour demands an understanding of the dynamics of human sperm competition.

Fertilization of an egg places relatively simple demands on the behaviour and physiology of both the sperm and the male who produces them. By contrast, sperm competition places enormous and complex pressures on males, their ejaculates, and on the females in whose reproductive tracts the contests take place. Thus, males do best who produce competitive ejaculates. Females do best who provide an internal environment that is optimally selective for the competitiveness of the sperm from different males.

As an analogy, let us compare a person ( = DNA) leisurely driving a car (= a sperm) uncontested from A (= vagina) to B (= site of fertilization) with the same person in a rally car racing to arrive at B ahead of numerous other hostile competitors from one or more opposing teams (= sperm competition). In both cases only the car which arrives at B at precisely the right moment will receive a prize (= egg). However, the requirements, resources and strategies necessary to attain a prize in the second scenario are infinitely greater than in the first even though in the first the person may stand a better chance of completing the journey.

If this analogy seems whimsical, consider the bull whose semen is fully fertile when artificially inseminated on its own but fails to gain any fertilizations when mixed with semen from another bull (Beatty et al., 1969). Little wonder, therefore, that behavioural ecologists suspect that when they look at ejaculates, or any other aspect of sexuality, they are seeing requirements for success in sperm competition rather than for success in simple fertilization. Although the latter is there, and obviously important, it is obscured by the former. The single tree of fertilization is difficult to find in the forest of sperm competition.

Since 1970, behavioural ecology has made tremendous progress in understanding the nature of animal sexuality. At the same time, other biological and medical disciplines have been unravelling the cellular and biochemical complexities of ejaculate structure. The complete picture, however, has been appreciated by only a limited and esoteric audience. By and large, the combined implications have escaped the attention of the wider interested audience of lay biologists, students in all branches of biological science, and medical and veterinary scientists.

This book is an attempt to correct that situation. Its message is simple and straightforward. Human sexuality, in all its anatomical, physiological and behavioural detail, owes more to sperm competition (both in the present and in the immediate and distant evolutionary past) than it does to simple fertilization. Acceptance of this fact revolutionizes one’s view of all aspects of male and female sexuality and brings old enigmas into new perspective. As we hope this book will show, the medical and veterinary implications of this new perspective are enormous.

2 Sex, coyness and promiscuity: the evolution of sperm competition

2.1 Introduction

Each living human is the modern representative of a continuous evolutionary lineage stretching back from the present day through an unbroken sequence of generations to the origin of life on planet Earth some 4000 million years ago. During the course of these generations, the human lineage ‘picked up’ through evolution a variety of anatomical, physiological and behavioural characteristics that today constitute human sexuality.

In this and the next four chapters, we discuss the evolution of various facets of human sexuality. Throughout, we point out the pivotal role of sperm competition. Our approach is broadly chronological, considering each facet roughly in the order in which we think it appeared in the human lineage and since when it will have been a continuous feature of our ancestors’ sexuality (Box_2.1; Box_2.1a).

Each section in this and the next four chapters deals with a particular facet of human sexuality and is organized according to the following convention. First, if necessary, we define the terms associated with the aspect of sexuality to be discussed. Next, we describe the characteristics of this aspect as manifest by humans. Finally, we briefly place the characteristic in the perspective of other animals before making a ‘best guess’ at its antiquity (i.e. when it first evolved in the human lineage).

We assume that many people who read this book will not have received formal training in behavioural ecology and thus will not be familiar with those basic hypotheses that have been formulated to explain the evolution of sexual behaviour. For those among such readers who would like a deeper understanding of the arguments in this book, we describe these hypotheses when they are appropriate. However, to avoid disrupting the flow of the main text, these descriptions have been separated into Boxes and collected together at the end of each chapter.

2.2 Evolutionary inheritance: a programme for a lifetime

The earliest life-forms were probably simple, replicating molecules with relatively few heritable elements (‘genes’ etc.). Over a time scale of 4000 million years, however, the influence of mutation, breakage and recombination of heritable material has generated more, and more diverse, heritable elements.

Perhaps the first step in complexity was the greater reproductive success of individuals with a ‘coat’ that hindered other such molecules from ‘stealing’ their chemical building blocks (Dawkins, 1976). With the general increase in genetic complexity has come an increase in complexity of the coat. In a sense, the human body serves the same function; a ‘coat’ to protect its genes. It is the properties of this ‘coat’ that determine the chances of the germ cells meeting others in order to reproduce (Cohen, 1977).

So many heritable elements are now needed for the human (or rat, butterfly or tree) to function that the combination of elements are nearly infinite. However, despite the potential for infinite individual variation, populations are dominated numerically by heritable characteristics possessed by most individuals. For example, almost every human is programmed to reproduce sexually. With the certainty of mathematics, such widespread characteristics are those that over past generations have imparted the greatest production of offspring to their possessors.

The currency of natural selection is not survival but reproduction (Box_2.2) and the two are by no means always linked. For example, a dominant male gains no genetic benefit from his greater size, fitness and perhaps longevity if he is impotent (e.g. swine; Sumption, 1961). Inevitably, the genetic programmes that shape the behaviour of the majority of modern individuals are made up of a range of heritable characteristics, each of which in past generations was found in those ancestors who generated most descendants (i.e. had the greatest reproductive success).

Programmed behaviour does not equate to inflexible behaviour. The best artificial intelligence programmes are designed to change their response for the better as a result of their own experiences (Schank, 1990). However, even such dynamic intelligence is still simply a series of algorithms; a programme. Of course, some types of animals in some types of environment may gain greatest reproductive success from inflexible, unvarying behaviour though it is difficult to think of any unequivocal example. Without doubt, the majority gain from behavioural flexibility. Individuals whose behaviour changes with each change in circumstance, perhaps in part according to previous experience, will achieve greater reproductive success than those whose behaviour does not, or changes inappropriately. Nevertheless, which behaviour is shown in which circumstance and how, how quickly and to what extent behaviour changes with experience, will be part of the inherited programme. Humans, like other mammals, may be programmed to be extremely flexible. Nevertheless, the basis of the flexibility is still just a programme, a collection of interacting chemicals. Change the chemical balance inappropriately even in a human (for instance by alcoholic intake) and behaviour may become inappropriate and maladaptive (e.g. excitability, euphoria, aggression and unconsciousness; Littleton, 1981).

2.3 Human sexuality: the basics

2.3.1 Sex, gender and the sex ratio

Almost every modern human is programmed to reproduce sexually via the production of gametes which fuse to produce a zygote. Individuals are programmed to be either male or female producing, respectively, either sperm or eggs.

At a global level, the population consists of males and females in a roughly 1:1 sex ratio. However, at conception (primary sex ratio) males may out-number females 1.3:1 with much of this bias disappearing by birth (secondary sex ratio) and males faring worse than females in all subsequent stages (Singer, 1985). Perhaps most importantly, there is some evidence that a balanced 1:1 ratio may be reached at the age when male and female humans begin sexual exploration (Crew, 1952).

In these terms, basic human sexuality is indistinguishable from that of virtually all other mammals, the vast majority of other vertebrates and probably the majority of invertebrates. As far as sex ratio is concerned, a few animals do depart from a 1:1 ratio (Hamilton, 1967) and humans do show a bias toward producing male or female offspring depending on the mother’s circumstance (Crew, 1952). However, further discussion of these subtle departures from a 1:1 ratio in humans is left until Chapter 4. For the moment, the important point is that sex ratios more often than not are nearly 1:1.

Theories explaining the evolution of these basic facets of sexuality are relatively well established (Box_2.3, Box_2.4, Box_2.5). Thus, it seems likely that sexual reproduction has been a continuous feature of the human lineage ever since the appearance of the simplest organisms, soon after the origin of life (3500-2500 million years ago; Box_2.1). Gametes and zygotes seem likely to have been a continuous feature since at least the appearance of the first eukaryotes (1200 million years ago; Box_2.1). The male:female phenomenon with a 1:1 sex ratio, however, although possibly orginating at about the same time may not have been firmly established until the explosive evolution of metazoans (around 800-600 million years ago; Box_2.1) (Parker et al., 1972; Knowlton, 1974; Bell, 1978).

2.3.2 Urgent males and coy females

Surveys consistently show that human males claim to have inseminated more females than females claim to have been inseminated by males (Anderson et al., 1991; Morris, 1993). Mathematically, of course, with a 1:1 sex ratio, mean (though not median) number of partners must be identical (Gurman, 1989). Recent analysis of the discrepancy suggests that almost the whole difference lies in the ‘tail’ of the distribution, in the claims made by the sexually most active males and females (Morris, 1993).

Two explanations for the discrepancy are normally given. Either: (1) more males than females have multiple partners (a few females being inseminated by many males) but most surveys are too small or too biased to contain a representative proportion of the few very active females; or (2) males tend to exaggerate, and/or females to underplay, their sexual activity, especially at the most active end of the spectrum.

The first of these two explanations has, in the past, generally been the more favoured (Johnson et al, 1990). If this were the case, however, the larger the sample the greater the chance of including the putatively few very active females and hence the smaller the difference between male and female claims. Unfortunately, any evidence for this interpretation has recently been undermined by the findings of two very large surveys of 20,055 men and women in France (ACSF investigators, 1992) and 18,876 in England, Wales and Scotland (Johnson et al, 1992, 1994). Even though both surveyed over 10,000 females, the total numbers of claimed lifetime partners for males and females were, respectively, 11 and 3 in France and 10 and 3 in Britain. Both sets of figures are similar to the claims of 11 and 3 based on the first 1000 respondents in the UK survey (Maddox, 1989; Johnson et al., 1990). There is no indication of a decrease in this anomaly with increase in sample size.

Aspects of the British and French 1992 surveys suggest that the second of the above interpretations is the more likely: males tend to exaggerate, and/or females to underplay, their sexual activity once number of partners becomes large (Morris, 1993). Of these two elements, the more potent seems to be the tendency for females to underestimate their past number of partners. For example, in the British survey (Johnson et al., 1992, 1994), the mean number of partners claimed by females showed an unlikely decrease with age. Of course, such a trend could be attributable to age cohort differences. The past few decades could have seen such an increase in number of partners that young women now have more partners in their first eight years of sexual activity than older women did in their entire lifetime. However, the data for males shows the expected increase in number of partners with age. Even allowing for age differences in the selection of partners by males and females and an undoubted tendency for males to exaggerate, the most powerful factor still seems likely to be female understatement. Such understatement could be the result of a genuine lapse of memory or it could be due to subconscious deception (of self as well as others) and/or conscious secrecy. Self-deception as a female strategy is discussed in Chapter 6.

Both of the 1992 French and British surveys were carried out by interview, either by phone (in France) or by direct contact (Britain). Our own survey (females only) was by mail (Box_2.6) and produced claimed numbers of lifetime partners for females far more comparable to the number claimed by males in these other studies. Whether this higher claimed number of partners/female in our study reflects greater accuracy due to our less personal methodology or whether the women in other surveys really had fewer partners/female must remain a moot point. In favour of the former possibility, however, is the fact that in our study women did show the expected increase in number of partners with increased sexual experience.

Important though it is in its own right, the eventual detailed explanation for the male/ female dichotomy in claimed number of partners does not matter in the present context. What matters here is that the discrepancy reflects an important difference between the sexual programming of human males and females: males are generally more urgent, indiscriminate and overt over sexual matters; females are generally more coy, cautious and secretive. This difference was graphically illustrated in a survey of Californian students in which males were significantly more likely than females to say that they would have sex with an anonymous partner (Symons and Ellis, 1989).

The greater urgency of males and their relative indiscrimination sometimes translates into enormous levels of reproductive success. For humans, the most offspring credited to a single male is 888 (achieved by an ex- emperor of Morocco). By contrast, the most offspring ever credited to a single female is 67 (in 29 pregnancies) (The Guinness Book of Records). The tendency for males to be more indiscriminate and urgent than females over sexual matters is almost universal among animals and the theoretical basis of the phenomenon is relatively clear (Box_2.7).

The number of offspring produced by a population is determined by the females, not the males. It is the rate at which females convert time and energy into children that is critical, not their rate of sexual encounter with males. For males, however, it is the rate at which they fertilize eggs that is important to their individual reproductive success. In a classic experiment by Bateman (1948), equal numbers of male and female fruit flies, Drosophila melanogaster were placed in bottles. The number of matings and offspring produced by each individual was scored, using genetic markers to determine parentage. For males, reproductive success went up with number of matings, for females it did not (beyond the first mating).

The few animal lineages characterized by females who are more urgent and competitive than males are associated with ecological situations in which it is the male who limits reproductive output, not the female (Clutton-Brock and Vincent, 1991). Thus, in the Panamania poison-arrow frog, Dendrobates auratus, the male offers protection and transport to the tadpoles on his back. The male thus guards the offspring during their early development (Wells, 1981). In some birds (e.g. phalaropes), females are in a food-rich environment and are not limited in the number of eggs they produce. The limitation to their reproductive output is in finding males to incubate the eggs that they produce (Cramp, 1983). In both frog and phalarope, the females are the more urgent sex and males the more coy and cautious. Females compete (often aggressively) with each other for sexual access to males.

Urgent males and coy females have probably been a feature of the human lineage for as long as there have been mobile, metazoan