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.
c 2005 Elsevier Ltd. All rights reserved.
Many animal species posses physical traits, such as
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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.
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Ophthalmology Residency Indiana University School of Medicine, Department of Ophthalmology, Indianapolis, IN Medical Internship Transitional Year Program, Indiana University School of Medicine, Indianapolis, IN Doctor of Medicine Loyola University Chicago Stritch School of Medicine, Maywood, Chosen and served as one of only two student interviewers and voting members of the C