Doi:10.1016/j.mehy.2004.10.020

http://intl.elsevierhealth.com/journals/mehy Male reproductive physiology as a sexuallyselected handicap? Erectile dysfunction iscorrelated with general health and healthprognosis and may have evolved as a markerof poor phenotypic quality Alessandro Cellerinoa,*, Emmanuele A. Janninib a Scuola Normale Superiore, Laboratorio di Neurobiologia, c/o Isituto di Neuroscienze del CNR,via Moruzzi 1, 1-56100 Ghezzano (Pisa) Italyb University of Aquila, Italy Received 22 October 2004; accepted 29 October 2004 Many extravagant physical traits are selected because they are used as cues for mate choice (sexual selection). Why is mate choice driven by costly ornaments? A theory of sexual selection posits that extravaganttraits are preferred because are reliable indicators of superior (heritable) phenotypic quality. In particular, thepreferred traits can be expressed only in individuals with superior conditions because are handicaps which imposea high cost to the carrier.
The human penis achieves its reproductive function by the complex neuro-vascular mechanisms that controls erection. Surprisingly, erectile dysfunction and infertility, two condition which nearly annihilate fitness, arewidespread medical conditions which affect millions of people of any age worldwide. The very high incidence oferectile dysfunction appears as an evolutionary paradox. Impotence is associated with all major systemic diseasesas well depression and stress. Stress is also one of the causes of infertility. Therefore, male reproduction appearsto be extremely sensitive to internal and external stressors. Moreover, erectile dysfunction is a predictor ofmyocardial infarction and stroke, whereas men with regular sexual activity have lower risk of death due tocoronary disease. This large body of medical literature makes erection the best case for a fitness indicator in thehuman male. We suggest that the fragility of male sexual physiology observed in modern society is the specificconsequence of an evolutionary process driven by the handicap principle.
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Many animal species posses physical traits, such as Tel.: +39 3381077548; fax: +39 050 3153212.
the peacock’s tails, which do not have any obvious c 2005 Elsevier Ltd. All rights reserved.
physiological function. It is well established that support the correlation of FA or sexual dimorphism mate choice and differential reproductive success with male fertility or health parameters in modern drives the evolution of extravagant physical traits and the trait are present because individuals withwell-developed ornaments are preferred as sexualpartners (sexual selection, Moreover, the traitswhich are needed for reproduction often reduce survival of the carrier One model of sexualselection posits that sexually selected traits are In species with internal fertilisation, female choice markers of heritable fitness Mating with orna- and differential mating success can represent a mented individuals is rewarded by a higher pheno- strong selective force for the evolution of genital typic quality of the offspring. An association anatomy and reproductive physiology. Penises between sexually selected traits and heritable fit- were defined as ‘‘internal courting devices’’ ness was detected in some experimental paradigms and can therefore be shaped by female choice.
(e.g. In order to reflect individual fitness, One of the consequences of female choice, is that expression of sexually selected traits need to be genital anatomy tends to diverge rapidly during condition-dependent. Signals which impose a high cost to the carrier (handicaps) can only be ex- The human male genital anatomy and reproduc- pressed by individuals of superior phenotypic qual- tive physiology differ in some traits from those of other Primates. The human penis lacks the bacu- lum, a bony structure found in the penis of most as ‘‘the handicap principle’’.
Is mate choice in the human species influenced the retractor penis muscle . As a consequence, by fitness indicators? In females, body-mass index erection in humans is achieved exclusively by vas- (BMI) is a good predictor of whole body attractive- cular mechanism and cannot rely on an osteo- ness . BMI is associated with general health and also specifically with hormonal function and ments, combined with large size of the human fertility. Women with too low or too high BMI are penis, arguably make intromission comparatively prone to a series of hormonal dysfunction and more difficult than in related Primate species. reports the mean duration of copulation of is reasonably close to optimal BMI in terms of several Old-World Primate species. With the nota- reproductive physiology, perception of female ble exception of the monogamous orang-utans, it body attractiveness could be biased by an inborn is evident that the time needed for a human male to ejaculate is considerably longer than in many other Primates and once ejaculation occurs, it is Up to now, no good indicators of male pheno- followed by a long refractive period. It can be con- typic quality have were identified. Fluctuating cluded that the ability to obtain an erection and asymmetry (FA) and facial sexual dimorphism were maintain it for a period sufficient to reach ejacu- lation is a comparatively stronger prezygotic selection factor in humans than in most other between BMI and fertility, no strong medical data Duration of copulation and inter-copulation intervals Intromission duration and inter-ejaculation intervals in some Primate species. Modified from p. 118 and p. 105.
Male reproductive physiology as a sexually selected handicap? is clearly an evolutionary paradox. A large bodyof epidemiological data are available as to the aeti- The difficulties posed by these anatomical and neu- ologies of ED which can be of help in defining rological constraints are demonstrated by the prev- alence of erectile dysfunction (ED), the chronic The incidence of ED increases with age and ED is impossibility to have or to maintain a full erection a sure marker of aging. While 60% of men are po- in the presence of proper erotic stimuli, which is a tent in their fifth decade, only 33% are able to widespread symptom affecting about 20 million of achieve erection at 70 years . However, the patients in the US only . The very high preva- large current prevalence of ED cannot be simply lence of ED is further confirmed by the 20 million explained with the increase of life expectancies patients worldwide having received sildenafil (Via- in modern society. ED is a frequent symptom of gra) in the first few months after marketing .
many diseases which affect all the age classes.
Many men do not seek medical advice for ED, how- ED can be caused by specific damage of vascular, ever, and men reporting some kind of erectile endocrine and neural mechanisms which control problem range from 13% in Italy , to 74% in Fin- erection, but is also dependent on general body land A synopsis of the reported incidence of erectile dysfunction is reported in .
with several widespread diseases. Nine of the 10 Although, the reasons for the high variation in inci- major causes of a possible taxonomy of ED aetiolo- dence are not clear and can be partly due to cul- gies presented in are natural, and between tural differences in admitting impotence, it can the most frequent, illnesses. In general, erection is be safely estimated that at least 1 man out of 3 lost in all severe systemic diseases which affect all has unsatisfactory erection worldwide. In an evolu- ages (cancer, AIDS, lung and kidney insufficiencies, tionary perspective, ED would cause a severe infective diseases). To provide some quantitative reduction of fitness and the high prevalence of ED examples, chronic renal failure and chronic uremia Prevalence of erectile dysfunction per country Braun M, Wassmer G, Klotz T, Reifenrath B, Mathers M,Engelmann U. Epidemiology of erectile dysfunction: results ofthe ‘Cologne Male Survey’. Int J Impot Res 2000;12:305–11 Giuliano F, Chevret-Measson M, Tsatsaris A, Reitz C, Murino M,Thonneau P. Prevalence of erectile dysfunction in France:results of an epidemiological survey conducted on arepresentative sample of 1004 men. Progr Urol 2002;12:260–67 Nazareth I, Boynton P, King M. Problems with sexual function inpeople attending Lond general practitioners: cross-sectionalstudy. Br Med J 2003;327–423–29De Boer BJ, Bots ML, Lyclama A, Nijeholt AA, Moors JP, PietersHM, Verhej TJ. Erectile dysfunction in primary care: prevalenceand patient characteristics. Int J Impot Res 2004;16:358–64 Medeira ED, Abdo CH, Torres EB, Lobo CF, Fittipaldi JA.
Prevalence and correlates of erectile dysfunction: results of theBrazilian study of sexual behavior. Urology 2001;58:583–88 Tan JK, Hong CY, Png DJ, Liew LC, Wong ML. Erectiledysfunction in Singapore: prevalence and its associated factors– a population-based study. Singapore Med J 2003;44:20–6 Levine LA. Erectile dysfunction: a review of a common problemin rapid evolution. Prim Care Update Ob Gyn 2000;7:124–29 Morillo LE, Diaz J, Estevez E, Costa A, Mendez H, Devila H,Medero N, Rodriguez N, Chaves M, Vinueza R, Ortiz JA, GlasserDB. Prevalence of erectile dysfunction in Colombia, Ecuador,and Venezuela: a polulation-based study. Int J Impot Res2002;14(Suppl. 2):S10–8 Taxonomy of the 10 major causes of erectile dysfunction Cancer, leukemia, chronic renal failure, liver insufficiency, peptic ulcer,infective and parasitic diseases Hypogonadism, hyperprolactinemia, hypo- and hyper-thyroidism, acromegaly Diabetes mellitus, hyperlipidemia, obesity, zinc deficiency Stroke, temporal lobe epilepsy, Parkinson’s and Alzheimer’s diseases, multiplesclerosis, Arnold-Chiari and Guillain-Barre Peyronie’s disease, priapism, pelvic and penile trauma Alcohol, illegal drug abuse, antihypertensives, antidepressants,antipsychotics, anxiolytics, H2 antagonists, antiandrogens, digoxin,chlofibrate, . . .
are associated with ED in 40% and 90%, respec- Erection also correlates with psychic well-being.
tively, of the patients; 64% of men with myocardial ED is robustly associated with conditions of psycho- infarction are impotent and up to 59% of diabetics logical stress and anxiety with depression suffer for ED . The strict correlation between being one of the major causes of hypoactive sexual ED and proper function of the circulatory system is further demonstrated by the observation that tantly in an evolutionary perspective, ED is strongly the probability of developing ED is directly corre- associated with traits correlated with submissive lated with hypertension and inversely correlated with HDL cholesterol (the probability of complete All these pathophysiological data clearly demon- impotence increases of 16% as HDL cholesterol de- strate that erectile function is correlated with ac- creases from 90 to 30 ng/ml). In general, cardio- tual organic and psychological health, with the level of physical and psychological stress, with peripheral and coronary artery diseases, myocar- life-style and with the risk of developing major dial infarction, hypertension, hyperlipidemia, and life-threatening diseases. In general terms, erec- diabetes mellitus all increase the probability of tile function can be strictly defined as a condi- ED even when corrected for age. Also chronic neu- rodegenerative diseases (Parkinson’s and Alzhei-mer’s diseases, multiple sclerosis) are majorcauses of ED (for a more complete review of theaetiology of ED see ED not only correlates with current health but, more importantly, with health prospects. Recentresearch has demonstrated that ED is a predictor If erection physiology can represent a strong of myocardial infarction and stroke. More specifi- selection mechanism at a pre-copulation stage, cally, vascular ED, the most frequent aetiology of spermatogenesis and sperm quality is a strong impotence, was shown to be highly predictive of post-copulatory selection mechanism. Sexual con- a major vascular accident in the next few years flict often results in cryptic female choice and evolution of female genitalia that perform a sexual activity have lower risk of death by coronary post-copulatory sperm selection by a variety of hearth disease In general, ED appears as an mechanisms which impair sperm vitality and egg early indicator of dysfunction in the circulatory sys- accessibility . Although, the prevalence of tem. Finally, erectile performance is correlated sperm competition in humans remains to be as- with general levels of physical activity (and possi- sessed, reduced fertility is the second major male bly physical condition): sedentary life style is an health concern in modern society. Literature re- important risk factors for the development of ED view demonstrates that the current infertility prevalence is one infertile couple every 50 individ- Male reproductive physiology as a sexually selected handicap? uals in the population and that the prevalence of pressed only by individuals of high phenotypic qual- subfertility is about 10% Roughly half of ity. The fragility of erection is clearly a handicap, these cases are estimated to be due to male fac- at least in contemporary males, and might simply tors. Male fertility is sensitive to environmental represent a general limitation of human physiol- stress. Stressful conditions are in fact known for ogy. However, the strict association between male affecting the quality on semen . Although sexual function and health suggest that this fragil- the medical evidence is not as strong as for the ity evolved as a specific fitness indicator under the case of ED, male fertility might as well represent a condition-dependent trait, in particular can becorrelated to the resistance of the organism toenvironmental and psychological stress.
This work was partially supported by Italian Minis- 2003062953 and SNS03 grant from Scuola NormaleSuperiore.
In animal species where both sexes invest in raisingthe offspring, the same individual can adopt differ-ent mating strategies. In long-term mating strate- gies, mate quality depends from a trade-offbetween parental investment and heritable fitness.
[1] Andersson M. Sexual selection. Monographs in behaviour In short-term mating strategies mate quality is and ecology. Princeton, NJ: Princeton University Press;1994.
determined exclusively by heritable fitness and [2] Araujo AB, Johannes CB, Feldman HA, Derby CA, McKinlay JB.
mate choice is more sensitive to sexually selected Relation between psychosocial risk factors and incident physical traits. This general evolutionary model erectile dysfunction: prospective results from the Massa- was often invoked to explain variation in the wo- chusetts male aging study. Am J Epidemiol 2000;152: men perception of male physical attractiveness [3] Benson GS. Mechanisms of penile erection. Invest Urol during the menstrual cycle. In the ovulatory phase, women are more responsive to presumed indicators [4] Birkhead TR. Sperm competition: evolutionary causes and of phenotypic quality Gangestad, 2001; #269; consequences. Reprod Fertil Dev 1995;7:755–75.
. Short-term mating strategies are also based [5] Boyle P. Epidemiology of erectile dysfunction. In: Carson on a limited (or even one single) copulations. Effi- RS, Kirby RS, Goldstein I, editors. Textbook of erectiledysfunction. Oxford: ISIS; 1999. p. 15–24.
cient erection and good semen quality are then [6] Carr BR. Disorders of the ovaries and female reproductive especially relevant in the context of occasional ex- tract. In: Wilson JD, Foster DW, Kronenberg HM, Larsen PR, tra-pair relationships when they would critically editors. Williams textbook of Endocrinology. Philadel- decide the probability of insemination.
phia: WB Saunders; 1998. p. 751–817.
[7] Corona G, Mannucci E, Mansani R, Petrone L, Bartolini M, Giommi R et al. Aging and pathogenesis of erectiledysfunction. Int J Impot Res 2004;16:395–402.
[8] Derby CA, Mohr BA, Goldstein I, Feldman HA, Johannes CB, McKinlay JB. Modifiable risk factors and erectile dysfunc-tion: A large body of medical evidence makes penile [9] Dixon. Primate sexuality. Oxford: Oxford University Press; erection one of the best cases for an honest indica- tor of phenotypic quality in the human male. If the [10] Eberhardt WG. Sexual selection and animal genitalia. Har- pattern observed in modern western society is still vard: Harvard University Press; 1985.
representative of human biology in ancestral envi- [11] EHSRE. The ESHRE Capri Workshop Group: social determi- ronments, the sensitivity of erection physiology nants of human reproduction. Hum Reprod 2001;7:1518–26.
[12] Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, and fertility to internal (organic and psychological) McKinlay JB. Impotence and its medical and psychosocial and external (environmental) conditions must have correlates: results of the Massachusetts male aging study. J reduced the reproductive success of individuals with low phenotypic quality. Sexual selection the- [13] Feldman HA, Johannes CB, Derby CA, Kleinman KP, Mohr ory posits the existence of ‘‘honest’’ fitness indica- AB, Araujo AB et al. Erectile dysfunction and coronary riskfactors: prospective results from the Massachusetts male tors in the form of handicaps, i.e., phenotypic aging study. Prev Med 2000;30:328–38.
traits that are specifically selected because they [14] Flier JS, Foster DW. Eating disorders: obesity, anorexia reduce individual fitness and can therefore be ex- nervosa, and bulimia nervosa. In: Wilson JD, Foster DW, Kronenberg A, Larsen PR, editors. Williams texbook of [29] Montorsi P, Montorsi F, Schulman CC. Is erectile dysfunc- endocrinology. Philadelphia: WB Saunders. p. 1061–97.
tion the ‘‘tip of the iceberg’’ of a systemic vascular [15] Goldstein I. The mutually reinforcing triad of depressive disorder?. Eur Urol 2003;44:352–4.
symptoms, cardiovascular disease and erectile dysfunction.
[30] Morley JE, Korenman SG, Kaiser FE, Mooradian AD, Viosca SP. Relationship of penile brachial pressure index to [16] Grafen A. Biological signals as handicaps. J Theor Biol myocardial infarction and cerebrovascular accidents in older men. Am J Med 1988;84:445–8.
[17] Grafen A. Sexual selection unhandicapped by the Fisher [31] Parazzini F, Menchini Fabris F, Bortolotti A, Calabro A, process. J Theor Biol 1990;144:473–516.
Chatenoud L, Colli E et al. Frequency and determinants of [18] Grammer K, Fink B, Moller AP, Thornhill R. Darwinian erectile dysfunction in Italy. Eur Urol 2000;37:43–9.
aesthetics: sexual selection and the biology of beauty. Biol [32] Penton-Voak IS, Little AC, Jones BC, Burt DM, Tiddeman Rev Camb Philos Soc 2003;78:385–407.
DI, Perrett DI. Female condition influences preferences for [19] Grumbach MM, Styne DM. Puberty: ontogeny, neuroendi- sexual dimorphism in faces of male humans (Homo crinology, physiology and disorders. In: Wilson HR, Foster sapiens). J Comp Psychol 2003;117:264–71.
HM, Kronenberg HM, Larsen PR, editors. Williams textbook [33] Penton-Voak IS, Perrett DI, Castles DL, Kobayashi T, Burt of endocrinology. Philadelphia: WB Saunders; 1998. p.
LK, Murray LK et al. Menstrual cycle alters face prefer- [20] Hartz AJ, Barboriak PN, Wong A, Katayama KP, Rimm AA.
[34] Promislow DE, Smith EA, Pearse L. Adult fitness conse- The association of obesity with infertility and related quences of sexual selection in Drosophila melanogaster.
Proc Natl Acad Sci USA 1998;95:10687–92.
[35] Rhodes G, Chan J, Zebrowitz LA, Simmons LW. Does sexual [21] Johnston VS, Hagel R, Franklin M, Fink B, Grammer K. Male dimorphism in human faces signal health?. Proc R Soc Lond facial attractiveness – evidence for hormone-mediated B Biol Sci 2003;270(Suppl. 1):S93–5.
adaptive design. Evol Hum Behav 2001;22:251–67.
[36] Smith GD, Frankel S, Yarnell J. Sex and death: are they [22] Johnstone RA. Sexual selection, honest advertisement and related? Findings from the Caerphylly cohort study. Br Med the handicap principle: reviewing the evidence. Biol Rev [37] Steers W, Guay AT, Leriche A, Gingell C, Hargreave TB, [23] Klinge E, Sjostrand NO. Contraction and relaxation of the Wright PJ et al. Assessment of the efficacy and safety of retractor penis muscle and the penile artery of the bull.
Viagra (sildenafil citrate) in men with erectile dysfunction Acta Physiol Scand(Suppl. 420):1–88.
[24] Koehler N, Simmons LW, Rhodes G, Peters M. The relationship between sexual dimorphism in human faces [38] Thornhill R, Gangestad SW. Facial attractiveness. Trends and fluctuating asymmetry. Proc R Soc Lond B Biol Sci [39] Tovee MJ, Maisey DS, Emery JL, Cornelissen PL. Visual cues [25] Koskimaki J, Hakama M, Huhtala H, Tammela TL. Effect of to female physical attractiveness. Proc R Soc Lond B Biol erectile dysfunction on frequency of intercourse: a popu- [40] Tovee MJ, Reinhardt S, Emery JL, Cornelissen PL. Optimum body-mass index and maximum sexual attractiveness.
[26] Krane RJ, Goldstein I, Saenz de Tejada I. Impotence. N Engl [41] Watson JP, Davies T. ABC of menthal health: psychosexual [27] Kubin M, Wagner G, Fugl-Meyer AR. Epidemiology of problems. Br Med J 1997;315:239–42.
erectile dysfunction. Int J Impot Res 2003;15:63–71.
[42] Zahavi A. Mate selection-a selection for a handicap. J [28] Lewis RW, Mills TM. Risk factors for impotence. In: Carson RS, Kirby RS, Goldstein I, editors. Textbook of erectile [43] Zahavi A. The cost of (honesty further remarks on the dysfunction. Oxford: ISIS; 1999. p. 141–8.
handicap principle). J Theor Biol 1977;67:603–5.

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