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Tropical and Subtropical Agroecosystems E-ISSN: 1870-0462 [email protected] Universidad Autónoma de Yucatán México

Lucio, R. A.; Cruz, Y.; Pichardo, A. I.; Fuentes-Morales, M. R.; Fuentes-Farias, A.L.; Molina-Cerón, M. L.; Gutiérrez-Ospina, G. THE AND ECOPHYSIOLOGY OF Tropical and Subtropical Agroecosystems, vol. 15, núm. 1, 2012, pp. S113-S127 Universidad Autónoma de Yucatán Mérida, Yucatán, México

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How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Tropical and Subtropical Agroecosystems, 15 (2012) SUP 1: S113 – S127

REVIEW [REVISIÓN]

THE PHYSIOLOGY AND ECOPHYSIOLOGY OF EJACULATION

[FISIOLOGÍA Y ECOFISIOLOGÍA DE LA EYACULACIÓN]

R. A. Lucio1*, Y. Cruz1, A. I. Pichardo2, M. R. Fuentes-Morales1, A.L. Fuentes-Farias3, M. L. Molina-Cerón2 and G. Gutiérrez-Ospina2

1Centro Tlaxcala de Biología de la Conducta, Universidad Autónoma de Tlaxcala, Tlaxcala-Puebla km 1.5 s/n, Loma Xicotencatl, 90062, Tlaxcala, Tlax., México. 2Depto. Biología Celular y Fisiología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510, México, D.F., México. 3Laboratorio de Ecofisiologia , Departamento de Fisiologia, Instituto de Investigaciones sobre los Recursos Naturales, Universidad Michoacana de San Nicolás de Hidalgo, Av. San Juanito Itzicuaro s/n, Colonia Nueva Esperanza 58337, Morelia, Mich., México * Corresponding author

ABSTRACT RESUMEN

Different studies dealing with ejaculation view this Diferentes estudios enfocados en la eyaculación, process as a part of the male copulatory behavior. consideran a este proceso como parte de la conducta Some of them explain ejaculation as the consequence copulatoria masculina. Algunos de ellos explican la of a neuroendocrine feedback loops or from a purely eyaculación como la consecuencia de una anatomical perspective. The goal of the present review retroalimentación neuroendócrina o desde una is to discuss the traditional and novel themes related to perspectiva puramente anatómica. El objetivo de la the of ejaculation. The text begins with the presente revisión es discutir los temas tradicionales y description of the behavioral motor patterns that lead novedosos relacionados con la biología de la to ejaculation. The anatomo-physiological mechanisms eyaculación. El texto inicia con la descripción de los are explained under the notion that ejaculation is more patrones motores copulatorios que conducen a la than genitals and an excurrent duct system; thus it is eyaculación. Se explican los mecanismos anátomo- also included the participation of the striated perineal fisiológicos considerando que la eyaculación es más musculature. Although ejaculation is a sexual spinal que genitales y un sistema de ductos excurrentes; reflex, it is inhibited tonically by supraspinal entonces también se incluye la participación de la structures. Such supraspinal modulation may explain musculatura perineal estriada. Aunque la eyaculación the prudent allocation, by which males adjust es un reflejo sexual espinal, está inhibido tónicamente the number of sperm per ejaculate while copulating por estructuras supraespinales. Tal modulación under distinct competitive scenarios. In some supraespinal puede explicar el reparto espermático , ejaculate components facilitate seminal conveniente, por el cual los machos ajustan el número , an adaptation that may increase the male de espermatozoides por eyaculado al copular en reproductive fitness. Finally, there is a reflection of the distintos escenarios competitivos. En algunos so-called ejaculatory disturbances, which from mamíferos, los componentes del eyaculado facilitan la an ecophysiolgical perspective could represent coagulación del , una adaptación que puede advantages instead of sexual malfunction as are incrementar el éxito reproductivo del macho. recognize under the medical view. Finalmente, se reflexiona sobre los llamados desórdenes eyaculatorios humanos, que desde la Keywords: Copulatory behavior; copulatory reflexes; perspectiva ecofisiológica podrían representar ventajas disorders of ejaculation; prudent sperm allocation; en lugar de disfunciones sexuales como son seminal characteristics; sexual reflexes; sperm reconocidas desde el punto de vista médico competition; sperm transport. Palabras clave: Conducta copulatoria; reflejos copulatorios; desórdenes de la eyaculación; reparto espermático conveniente; características seminales; reflejos sexuales; competencia espermática; transporte espermático.

S113 Lucio et al., 2012

INTRODUCTION during , an ex copula stimulation protocol has been devised in rats. During these tests, Ejaculation in mammals is a male sexual function are elicited by retracting the penile sheath while the design to inseminate the . This ephemeral but male is kept in a supine position (Hart, 1968). The ex essential process occurs when the male reaches the copula and in copula penile erections are similar in ejaculatory threshold during the copulatory encounter. physiological terms (Hart, 1968; Holmes et al., 1991). In the present text ejaculation is analyzed in an However, the temporal pattern of penile reflexes integrative view, from proximal mechanisms to differs between natural and ex copula erections (Hart, ultimate explanations. Then ejaculation is considered 1968). Three gradations of can be observed: form a behavioral to ecophysiological perspectives. a) tumescence and elevation of the penile body without glans erection, b) intense erection of the glans COPULATORY BEHAVIOR: THE “cup” and of the penile body, and c) anteroflexions of EJACULATORY PRELUDE the due to the straightening of the penile body. During copulation cup formation is necessary for Male sexual behavior comprises activities aimed at depositing the semen into the , where it inseminating the female and fertilizing her ova. In coagulates to form a solid seminal plug. Without this general, two components are accepted to constitute plug, much of the semen leaks out of the vagina and this behavior. The first component referred to as rarely occurs (Sachs, 1982). These penile sexual drive, , courtship or appetitive aspect responses are present in “neutrally” intact rat males involves the behavioral expression used by males to (Dusser de Barenne and Koskoff, 1932; Hart, 1968). gain access to the female (e.g., fighting for territory, Also, penile reflexes may be elicited from spinally advertising his physical attributes or providing food to transected (Zeitlin et al., 1957). This indicates ). The second component is known as that penile reflexes are organized substantially at the performance, potency or consummatory aspect, and spinal level. Reflexes are, nonetheless, subjected to corresponds when copulation occurs. Males spent considerable supra-spinal control (Beach, 1967). much more time and energy seeking for copulation than the actual time and energy used to copulate Seminal expulsion refers to the forceful discharge of (Sachs and Meisel, 1988). semen from the prostatic through the urethral meatus. Ejaculation is elicited by urethral distention Copulatory motor patterns and copulatory genital and results from the clonic contraction of the responses ischiocavernosus and bulbocavernosus muscles in response to the rhythmic firing of the cavernous . The male copulatory behavior is expressed as motor This response is called the urethrogenital reflex and it patterns commonly organized in series of mounts, can be observed in rats that have high spinal intromissions and ejaculation. In almost all mammals, transection. A cluster of serotonergic neurons in the the male mounts the female dorsally and from the rear. brain stem is implicated in the descending inhibition of Males’ mounts features pelvic movements (i.e., spinal sexual reflexes (Marson and McKenna, 1990). thrusts) and flank palpation (Sachs and Garinello, The urethrogenital reflex is used as a model to study 1978). Intromission occurs when the penis enters the penile erection and ejaculation (McKenna et al., vagina following a mount. Penile insertion may entail 1991). only a brief genital contact with immediate ejaculation (ungulates; Bermant et al., 1969; Lott, 1981), it may EJACULATION: THE MALE´S AIM consist of a single long connection (canids; Beach, 1969) or it may be an extended series of brief genital Ejaculation is defined as the expulsion of seminal fluid contacts as in before ejaculation is reached (rodents; from the urethral meatus. It involves coordinated Larsson, 1956). Ejaculation occurs when the inserted series of reflexes activated during its two phases: penis into the vagina expel seminal fluid via the emission and expulsion. urethral meatus. Ejaculation in male rats is the culmination of vigorous intravaginal pelvic thrusting Seminal emission refers to the secretion of seminal accompanied by the arching of the male’s spine and plasma from the accessory sexual glands as the results the lifting of his forepaws off the female prior to of the peristaltic contraction of their smooth muscles; withdrawal. After ejaculation, the male dismount is the transferring of seminal plasma and spermatozoa followed by penis auto-grooming (Orbach, 1961; located into the cauda into the urethra then Lucio and Tlachi-López, 2008). ensues. Thus, this process involves secretion of seminal plasma from epithelial cells and the accessory There are two genital responses during copulation, the sexual glands, as well as contraction of the vas penile erection that occurs during intromission and the deferens to move seminal plasma and spermatozoa to seminal expulsion observed during ejaculation. the proximal urethra. Simultaneously to these Because both reflexes are difficult to assess and study parasympathetic and sympathetic actions, the urethral

S114 Tropical and Subtropical Agroecosystems, 15 (2012) SUP 1: S113 – S127 smooth muscles contract until closing the bladder´s albuginea (Hsu et al., 2004 ). The three bodies arise preventing, under normal circumstances, from the root of the penis in which . structures and the completely surround smooth muscle structures; they intermingle Once emission is completed, the ejaculate is ready to with fibrous to form the sinusoids wall (Hsu et be expelled through the urethra. Seminal expulsion al., 2004).The distal portion of the spongiosum body is then occurs when the semen is rapidly and forcefully expanded and becomes the glans of the penis, covered advanced forward along the urethra and spring out by the . through the penile meatus. Adequate propulsion of semen requires the coordinated contraction of the The testes produce spermatozoa and achieve glandular external urethral sphincter and the bulbocavernosus, function secreting male sexual such as the striated muscles surrounding the urethra. (Setchell et al., 1994). In adulthood the Contraction of other perineal and pelvic muscles , surrounded by the cremaster, rest into the adjacent to the base of the penis, such as the . The epididymides are tubular coiled ischiocavernosus and pubococcygeus muscles also structures in close anatomical relation to the testes contribute during seminal expulsion (Shafik et al., tubules. There, spermatozoa are stored and 2005). In humans, ejaculation is associated with what periodically expelled to the deferent duct (Setchell et has been called ; a subjective pleasurable al., 1994). In primates, each is joined by feeling reported by men. Although we have no accessory gland ducts to form a common duct, the certainty of the existence of in other which opens into the urethra. mammals, there are some studies that suggest that ejaculation of others mammals is also associated with Accessory sexual glands secrete most of the seminal reward (Kippin and Pfaus, 2001). plasma expelled during ejaculation. Although there is a significant variation between mammals with respect Rats present several accessory glands (seminal to the range of them, most of the have vesicles, coagulant glands, prostate and bulbourethral and bulbourethral glands (Setchell et al., 1994). glands) whose secretion constitutes a significant fraction of the expelled semen during the ejaculation. The organs described above are mainly involved in During ex copula tests, seminal expulsion occurs semen storage and production. For the semen to be occasionally. In anaesthetized , however, placed into the female reproductive tract is necessary semen emission and expulsion may be elicited by to count with a propulsion system, strong and fast electrical stimulation of the intermesenteric enough to expel the fluid. The smooth and striated (Bernabe et al., 2007) or by systemic administration of muscle of the urethra fills this requirement. P-chloroamphetamine, an amphetamine derivative that releases catecholamines and serotonin from The urethra achieves urinary and reproductive monoaminergic nerve terminals (Clement et al., 2006). function. It is an elongated structure whose cranial With regard to the seminal expulsion from the urethra, region connects to the , the medial it has been suggested that the rhythmic contraction of region transverse the pelvic diaphragm and its distal the urethral striated musculature is induced by the portion ran along the corpus spongiosum of the penis. activation of the pressure urethral receptors. In The urethra is usually divided in four regions: agreement with this idea is the fact that increased prostatic, membranous, bulbar (diverticulum in rats) urethral pressure induced contraction of the and spongiosum or penile (Ciner et al., 1996). The ischiocavernosus and bulbocavernosus muscles in distal portion of the penile urethra expands to form the and in rats (McKenna et al., 1991). However, this external . In men the ejaculatory ducts notion is in conflict with evidence showing the discharge the semen into the while in triggering of expulsion in absence of seminal fluids other species such as the rat the ducts enter into the within the prostatic urethra or after urethral anesthesia dorsal wall of the cranial region of the membranous (Holmes and Sachs, 1991). urethra (Bierinx and Sebille, 2006; Lehtoranta et al., 2006). Ejaculatory structures and ejaculatory reflex Around half of the urethra is surrounded by striated In mammals, the male reproductive organs consist of muscles. In rats, the prostatic and membranous regions the penis, two testes, two epididymides, accessory are surrounded by the external urethral sphincter, a sexual glands with its ducts and the urethra. The penis muscle also named rabdosphincter and the bulbar is a copulatory composed of three sections; urethra is surrounded by the bulbocavernosus muscle , body and root of the penis. The body is (Pacheco et al., 2002). Adjacent to the made up of three cylindrical bodies of erectile tissue, bulbocavernosus muscle is the ischiocavernosus the paired corpora cavernosa and the centrally located muscle (McKenna and Nadelhaft, 1986). The spongiosum body, each one surrounded by the tunica contraction of these muscles compresses the bulb of

S115 Lucio et al., 2012 the corpus spongiosum and the penile crura. In men integration allows for a normal ejaculatory reflex as the external urethral sphincter in mainly composed of coordinated signals sequentially relayed to the muscles circular slow fibers (Gosling et al., 1981). In contrast, and to structures of the pelvic and enabling in rats most of the fibers are fast twitch (Bierinx and them to function in an orchestrated fashion. Because Sebille, 2006; Lehtoranta et al., 2006). Similarly to ejaculation can be observed in men and rats with high man, in rats the rostral fibers of the external urethral spinal transection, it has been suggested that the sphincter are circular. Other fibers nonetheless run neurons of the ejaculation generator are located in the diagonally and longitudinally (Cruz and Downie, (McKenna et al., 1991). Accordingly, 2005; Lehtoranta et al., 2006). This muscular tracing studies suggest that neurons of the spinal organization suggests that the external urethral ejaculation generator are located in the dorsal gray sphincter is a complex muscle whose contraction commissure and lamina X at the L3-S1 (neurons contributes to urethral continence and urine and semen labeled after injecting the prostate) and L5-L6 expulsion. (neurons labeled after injecting the bulbocavernosus muscle) spinal levels (Marson and Carson, 1999; Tang Spinal and supraspinal control of ejaculation et al., 1999).

The precise nature of the afferent stimuli that trigger Another group of neurons clearly related to the control the process of ejaculation is unknown. It is thought, of ejaculation has been identified in the central gray of however, that somatosensory stimulation of genital lumbar levels at L3-4, in lamina X and in the medial structures plays a chief role. The knowledge of the portion of lamina VII (Truitt and Coolen, 2002). These neural circuitry controlling the genital tract has been cells are referred to as lumbar spinothalamic cells mostly obtained from animal studies. (LSt) and are supposed to control ejaculation (Truitt et al., 2003). Lesion of these neurons disrupts the Although not all the neural pathways controlling ejaculatory behavior demonstrating that LSt cells are ejaculation have been identified, it is currently specific components of the ejaculation generator accepted that seminal emission and expulsion result (Truitt and Coolen, 2002). from the activation of afferent, efferent, , sympathetic and parasympathetic fibers (Clement et The spinal ejaculation generator is under excitatory al., 2006). Accordingly, axons innervating the penis, and inhibitory influence of supraspinal sites (Allard et foreskin and perineal are carried by the sensory al., 2005). Indeed, stimulation of the hypothalamic branch of the and proximal and distal medial and paraventricular nucleus perineal nerves (McKenna and Nadelhaft, 1986; facilitates ejaculation while the nucleus Pacheco et al., 1997; Pastelin et al., 2008). Somatic paragigantocellularis of the medulla in the brain stem afferents from the urogenital tract enter the spinal cord exerts a powerful inhibitory influence (Marson et al., via L6-S1 dorsal roots (Nadelhaft and Booth, 1984). 1992; Marson and McKenna, 1994). A relay center Disruption of this pathway suppressed induced between the hypothalamus and the ejaculation seems ejaculation (Clement et al., 2006). The efferent to be located at the because pathways of the ejaculatory reflexes controlling the lesions of this area block the reflex induced by the tone of the smooth muscle are conveyed by stimulation of the medial preoptic area (Marson, hypogastric nerves and sympathetic fibers arising from 2004). the lumbar paravertebral sympathetic chain (Nadelhaft and McKenna, 1987; Clement et al., 2006). The Finally, the ejaculatory reflex is predominantly sympathetic preganglionic neurons are located in the controlled by a complex interplay between central intermediolateral column and the dorsal central serotonergic and dopaminergic neurons with a autonomic nucleus of the lower thoracic and upper secondary involvement of cholinergic, adrenergic, lumbar segments (T13-L2) (Nadelhaft and McKenna, nitrergic, oxytocinergic and GABAergic neurons 1987). The posganglionic neurons seem to be located (Giuliano and Clement, 2005). in the major pelvic ganglia, the accessory ganglia and the pelvic plexus (Keast, 2006; Pastelin et al., 2011). THE ECOLOGY OF EJACULATION: The motoneurons of the external urethral sphincter, EVERYTHING MAKES SENSE ischiocavernosus and bulbocavernosus muscles are located in the dorsomedial and dorsolateral nuclei in After finishing reading the preceding sections, the L6-S1 spinal segments (Marson, 1997; McKenna and reader may find him/herself wondering on how comes Nadelhaft, 1986). that a few seconds of ultimate pleasure can be so important to define each male’s reproductive success. The peripheral and central signals are integrated into To understand this essential aspect of ejaculation, we the ejaculation center of the spinal cord, referred to as must take in consideration the cost of the ejaculation generator or ejaculation spinal production. Although conventional wisdom suggests pacemaker (Sachs and Garinello, 1979). This that the metabolic cost of producing spermatozoa is

S116 Tropical and Subtropical Agroecosystems, 15 (2012) SUP 1: S113 – S127 relatively low, recent evidence showing increased male’s guarding the inseminated females after longevity following impaired gamete production copulation). However, others strategies involve more argues otherwise. In addition, the fact that and directly ejaculation. Indeed, for some males it appears courtship also are associated with reduced lifespan sufficient to inseminate repeatedly a single female further support that wasteful sperm expenditure is during her reproductive period; a circumstance that costly for males (Fisher et al., 2006). Hence, males presumably ensures having the female’s genital tract must devise sexual and reproductive strategies aimed plenty of his sperm by the time (Gomendio at using prudently their reproductive resources, thus et al., 2006). Other males, however, do not avoid reducing the cost the semen wasting. confrontation and they seem to participate openly and happily in contests. These last Ecological control: Sperm competition and prudent males, however, have evolved a sperm saving sperm allocation ejaculatory strategy called prudent sperm allocation. In this case, males estimate the magnitude of intra-sexual For a male to use their reproductive resources competition or the levels of the female’s cautiously, he must judge a variety of ecological thus adjusting not only the amount and quality of the factors that may provide vital information on his semen ejaculated but also their sexual reproductive possibility of achieving successful paternity. The behavior (Gomendio et al., 2006; Engqvist and physical attributes of the female, the likeliness of a Reinhold, 2007). Therefore, if sexual/sperm female to be a good and the magnitude of competition or the risk of it is high, the amount and promiscuity of the female he is pursuing are just few quality of the semen ejaculated are reduced. examples of such factors. Predictions on the Copulatory behavior matches this response. Indeed if environmental elements such as food availability and the competitive context is high, the number of mounts climatic contingencies must also be foreseeing, since a and intromissions, as well as the ejaculatory latency, drastic change of them may jeopardize the survival of tend to decrease or are diminished significantly offspring and, therefore, the long term male’s inclusive (Figure 1). fitness. Another ecological aspect that deeply influences By far the best studied influence of a given ecological ejaculatory behavior is social rank. Indeed, ejaculatory process on ejaculatory behavior is a phenomenon latency is commonly shorter in subordinated than in called intra-sexual competition. It is long known that dominant males. Although the reasons for this sexually mature males confront each other in contests phenotypic difference are unclear, it is likely that in that provide to them with opportunities for displaying some instances it may reflect intrinsic phenotypic their physical attributes. Males that prevail over their distinctions. This possibility is supported by opponents are supposed to increase their chances to be observations showing a relationship between chosen by females to sire their offspring (a condition copulatory abilities, penile sensitivity and the levels of that not always occurs; Jennions and Petrie, 2000). aromatase activity and testosterone/estrogen receptors Male rivalry, however, does not stay at the organismal expression in the brain of male rats (Olivier et al., level. In many mammalian species, intra-sexual 2006). Short ejaculatory latencies displayed by competition is extended to the cellular level through subordinated males could also illustrate a behavioral promiscuity. Indeed, the majority of sexually active adaptation associated with sneaking-based females copulate sequentially with more than a single reproductive tactics. This copulatory strategy is male during her fertile period, a circumstance that frequently observed in subordinated males since they promotes sperm competition within their genital tract commonly are younger, with smaller body sizes, (Pizzari et al., 2008; Parker and Pizzari, 2010). The poorer sexual experience, less favored by females and ultimate prize of this competition is the possibility for constantly threatened by their dominant competitors. the males’ to fertilize the female’s (s). So they must take advantage when the opportunity to Taking in consideration this scenario, the reproductive copulate is given. The hypothesis that a short outcome for each competing male would depend, in ejaculatory latency is a behavioral adaptation is part, upon the number and mobility of the spermatozoa supported by the fact that the values of the testes/body ejaculated by him relative to those inseminated by his size index are regularly higher in subordinated than in competitors (Stockley, 2004; Pizzari et al., 2008). It is dominant males (Preston et al., 2001; Holt and Van precisely under this scenario where the possibility of Look, 2004), and by observations showing that wasting the male’s reproductive resources is greater if subordinated males, if provided with the chance of competition is not assessed adequately. changing their social status to a higher order rank, shift their reproductive tactic from the sneaking-based to a Males have evolved different strategies to reduce -based copulatory pattern (Rudolfsen et al., semen wasting while seeking improving their chances 2006); the latter pattern being characterized by longer of achieving paternity. Some of these strategies ejaculation latencies and increased numbers of mounts involve behaviors different from ejaculation (e.g.,

S117 Lucio et al., 2012 and intromissions that could last for over 30 minutes at semen ejaculated varies noteworthy among mammals least in rodents. (e.g. 1 ml in rams; 3 ml in men; 9 ml in dogs; 70 ml in and 250 ml in boars). The human ejaculate Ejaculation also plays a major role in enhancing clots and then lyses, whereas in many rodents a male’s self-sexual assertion, sexual sociability and seminal plug is formed following ejaculation (Luke reproductive success in various mammalian species. In and Coffey, 1994). male rodents, for instance, ejaculation (and probably the pleasurable orgasmic perception commonly The ejaculate is constituted by cells, the spermatozoa associated with it) is the most reinforcing component and by fluid called seminal plasma. The seminal of sexual behavior and induces a reward after plasma results from the mixture of secretions from the copulatory encounters (Phillips-Farfán and Fernádez- male accessory sexual glands. Among mammals, no Guasti, 2009; Tenk et al., 2009). Interestingly, other organs present such an anatomical and ejaculation-related sexual rewarding increases the biochemical diversity as these accessory structures. availability of metabolites in the male’s Indeed, while rats display , prostate, urine. The urinary presence of these metabolites coagulating and bulbourethral glands, dogs only have indicates that males are sexually experienced, a fact the prostate. Seminal vesicles are absent in carnivores that makes them preferable to females searching for a and are well developed in man, , rat and guinea reproductive partner. Finally, as an pig. Three distinct anatomical and histological lobes expression of ejaculatory behavior permits males to (dorsal, ventral and lateral) with different functions enhance their sexual behavioral responses, to reduce characterize the prostate in rats, whereas in dog and anxiety levels and to renew sperm stores in preparation man, the prostate appears as a single structure. A pair to forthcoming sexual encounters; this makes of bulbourethral glands are present in most terrestrial masturbatory behavior an adaptive process. Although mammals but are absent in the aquatic ones, and there masturbation has long thought to be essentially a are three pairs in some (Rodger and Huges, human, recent experimental data support that 1973). Such an impressive variation might reflect the masturbatory activity also occurs in other primates vast diversity of environments and reproductive (Hull et al., 2006). habitats in which mammals live (Luke and Coffey, 1994). In sum, from an ecological perspective ejaculation is much more than a physiological process involved in The semen and seminal plug male-to-female sperm transfer. It allows the male to preserve their reproductive resources, to socialize his The average volume of the human ejaculate is 3 ml sexual/reproductive behavior, to publish their sexual (ranging from 2 to 6 ml). The spermatozoa are present abilities, to gain sexual self-confidence and ultimately in the range of 100 million/ml and constitutes less than to increase his chances of being a father. This might 1 % of the total volume of the ejaculate. The major explain why male bodies have gone far to develop an volumetric contribution of the ejaculate comes from intricate system to control ejaculation and why altered the seminal plasma of which the seminal vesicles allot ejaculation could be so disturbing, as it will be 1.5 to 2 ml, the prostate 0.5 ml, and bulbourethral discussed. glands 0.1 to 0.2 ml. The seminal plasma provides a nutritive and protective medium for the spermatozoa THE EJACULATE: A sui generis FLUID during their deposition into the females’ reproductive tract. The importance of male accessory sexual glands The semen expelled during ejaculation is also known is highlighted whenever they become dysfunctional. as seminal fluid. It is typically translucent with a white, grey or even yellowish tint. The amount of

Figure 1. Male copulatory behavior under two different contexts. Non-competitive (open bar) and intra-sexual competition (closed bar). Mann-Whitney Rank Sum Test *P<0.015, **P=0.048

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The mammalian has two main Table 1. Seminal plasma components in different components, the head and the (or tail), species. which are bridged by the neck. The head contains the nucleus and acrosome surrounded by cytoskeletal Seminal plasma Function components and cytoplasm. The sperm nucleus constituents contains have of the genetic material including one or Cells the other of the sex (called X or Y); macrophages, Produce immune reaction chromatin in the spermatozoids nucleus is highly monocytes and against foreign bodies (man) condensed. The flagellum contains a central axonema polimorphonuclear surrounded by an outer dense fiber. In the anterior leucocytes flagellum there are mitochondria forming in a tight Peptides helix around the dense outer fibers (Eddy and O´Brien, spermadhesins Sperm (boar) 1994). Although all mammalian spermatozoa have calcitonin and Sperm motility (man) these general characteristics, there are species-specific carnitine differences in the size and shape of the head and semenogelin Seminal fluid coagulation length and relative size of the flagellum. (man) semenoclotin Copulatory plug formation When mammalian sperm are released from the (mouse) seminiferous , they are immature and phospholipases Sperm motility (bull) acquire forward motility and the ability to fertilize phospholipase Acrosome reaction (bull) as they pass through the epididymis, where they vitronectin Acromose reaction (man) undergo substantial changes in function, composition Poliamines and organization, the pattern and effectiveness of Seminal clot formation flagellar activity and the ability to bind to the zona (man) pellucida (Orgebin-Crist and Fournier-Delpech, 1982; and Seminal clot formation (rat) Robaire and Hermo, 1988). Changes in plasma membrane composition and organization contribute to Catecholamines functional modifications, and involve changes in adrenaline and Modulate immune activity in surface charge, lipid composition, composition noradrenaline the female reproductive tract and antibody binding (Eddy and O´Brien, 1994). (man) Eicosanoids The fluid portion of the ejaculate is the seminal Sperm defense (man) plasma. Its components vary across mammalian Alkaloids species (for a review Poiani, 2006; also Table 1). beta-endorphin Sperm defense (man) Poani (2006) has recently revised the role of the Reduce female mating seminal plasma in sperm capacitation, sperm receptivity (rat) competition and fertilization. Sperm capacitation is Salts any modification undertaken by spermatozoa bicarbonate Sperm motility through facilitating them to become capable of achieving control of pH (man) successful fertilization. Capacitation, on the other urate Protect spermatozoa against , is process that involves the acquisition of a coat oxidative damage in female of that form the glucocalyx. This is reproductive tract (man) necessary for the accomplishment of full capacitation Metals and fertilizing ability. Inhibit proliferation in female This is important since the outcome of sperm reproductive tract (man) competition (see below) and sperm viability is affected by spermatozoa speed and mobility (Birkhead et al., 1999) considering the female reproductive tract represents as a particularly hostile environment In humans, it is unresolved why the seminal plasma (Poiani, 2002). Seminal plasma could have presents coagulation and liquefaction. However, it is allospermicidal function, so the sperm of a competitor known that infertile men may have impairment of the male could be eliminated by a chemical attack (Poiani, liquefaction process. The coagulation and liquefaction 2006). In fact, seminal plasma of healthy men may of semen vary in different species, e.g. the semen of contain cytokines that potentially could damage the bulls or dogs do not coagulate, while semen of rats and sperm of others. In addition, contains leucocytes that guinea pigs ejaculate a firm pellet that does not not only could attack competitor sperm but also to liquefy. Human semen coagulates within 5 minutes remove defective sperm (Tomlison et al., 1992). after ejaculation into a semi-solid gel and upon further

S119 Lucio et al., 2012 standing for 5-20 minutes the clot spontaneously Esponda, 1992). The secretions of the prostate allow liquefies to form a viscous liquid (Tauber et al., 1975). the adhesion of the seminal plug to the vagina (Tlachi- López et al., 2011). The weight and size of the seminal In mammals, seminal vesicles secretions are involve in plug depends mainly on the secretions of the seminal coagulation and prostatic in the liquefaction. vesicles (Carballada and Esponda, 1992). The rostral The secreted by the seminal vesicles are end of the seminal plug forms a cup at the vaginal major proteins and enzymes involved in the rapid cervical junction holding the sperm under pressure clotting of the ejaculate. In man, the major clotting until transcervical transport is completed. Seminal protein has been termed semenogelin, and it serves as plugs are usually loosened by subsequent a substrate for prostate-specific enzymes that degrades intromissions by the same of different male. If plugs the clot (Aumuller et al., 1990). It is unknown why are dislodged in less than 6 minutes after an clotting and lysing mechanism is important to the ejaculation, the sperm transport is disrupted (Mathews reproductive process. and Adler, 1977). The length of time corresponds to the male rat´s postejaculatory interval. This interval Seminal plugs are found in some mammalian species prevents the male from reassume mating, and then particularly in those in which females copulate with allows complete sperm transport in the female genital different partners. Because multi-partners mating tract. However, a different male has the ability to results in sperm competition among males, the dislodge the plug reducing or avoiding the amount of of certain biochemical mechanisms enhances sperm delivered by the previous male, and deposit his seminal coagulation to copulatory plug formation own sperm and plug (Wallach and Hart, 1983). (Dixson and Anderson, 2002). The function of the copulatory plug is to prevent back-flow of semen Sperm transport in the male and female and/or to interfere with the ejaculates of other males. reproductive tracts The existence of a hard plug, which completely fills the lumen of the vagina of certain mammals, has been Sperm transport occurs not only into the female genital known for more than one hundred and fifty years. tract after copulation, but also in the male genital tract Many studies exploring the role of the seminal plug after . Sperm is transported passively have been done in rats. Copulation in rats includes 10 from the seminiferous tubules to the , and to 15 intromissions culminating in ejaculation. Upon then to the . These ducts become highly ejaculation sperm are expelled first, followed by convoluted as they reach the epididymis, which is a secretions from the accessory sexual glands that single, long and highly convoluted duct on the harden into the vagina to form the seminal plug. This posterior border of the testis. The epididymis is plug adheres to the and vaginal walls, and it is divided in caput, corpus and cauda. Peristaltic necessary for sperm transport (Blandau, 1945). movements of the epididymis propel the spermatozoa from the caput to the cauda. Transit through Primates, rodents and artiodactyls present the seminal epididymis is slow and constant in several species plugs. Among primates, and orangutans (Harper, 1994). present seminal plugs but are absent in gorillas and humans. This may be due to the relative lack of male- Therefore, during seminal emission the mature male competition during mating of gorillas and spermatozoa from the epididymis cauda are humans. Among rodents, guinea pigs, rats, hamsters, transported through the vas deferens and proximal and mice present seminal plug after ejaculation. Until urethra and then are mixed wiith the secretions of the now, among artiodactyls, the domestic pigs have a accessory sexual glands. Then the ejaculate (seminal copulatory plug after copulation. plasma and sperm) is expelled by the urethral meatus.

In general, it was recognized that Most male mammals deposit their ejaculates into the might continue after , and that rather than vagina. The pH of the vagina is ; this acidity is competing for partners, males compete for maintained by the presence of due to the fertilizations. The presence of a seminal plug is one of action of Doederlein bacilli on the vaginal secretions. the reproductive strategies to increase the male´s Seminal plasma serves as a buffer protecting sperm. possibilities to obtain more offspring. The vagina is a hostile environment to spermatozoa and those that are not rapidly entrapped in the cervical In rats, the hardness of the seminal plug depends on die and are voided to the exterior (Fox et al., the secretions of the coagulating glands. This secretion 1973). contains an called vesiculasa that coagulate the ejaculate. When coagulating glands are totally In primates, immediately after ejaculation, seminal removed, no seminal plug is formed after coitus, and plasma coagulates; the coagulum is broken down by sperm transport to the did not occur, therefore, proteolitic enzymes. In one hour, the material is males were completely sterile (Carballada and liquefied and spermatozoa are motile. The coagulum

S120 Tropical and Subtropical Agroecosystems, 15 (2012) SUP 1: S113 – S127 probably acts to retain spermatozoa in the vagina close (human and rats, Waldinger, 2002; horses, McDonnell, to the cervix, thus permitting maximal access for the 1992). As a result, it is now recognized that ejaculation spermatozoa to become entrapped in the cervical is normally preceded by semen emission and followed mucus. During coitus, intravaginal pressure is negative by an orgasmic perception in mammalian males but becomes positive during female orgasm. Then it is (Newman et al., 1991). We also are now aware that possible that, the vaginal pressure and the smooth when each or all of these phases “malfunction”, males muscle vaginal activity will also propel the develop sexual symptoms that have relevant spermatozoa into the cervix (Harper, 1994). The reproductive consequences. consistency, of cervical mucus forms the basis for the ovulation method (Billings) of naturally family control Precocious ejaculation, , delayed (Billings et al., 1972). ejaculation and retro-ejaculation

The women cervix has crypts; it seems that only A classification of ejaculatory disorders has also motile spermatozoa are lodged in these crypts. It has emerged as a result of these investigations. Emission been suggested that the cervical crypts serve as phase disorders are so far exemplified by retrograde reservoirs allowing a continued release of viable ejaculation. Ejaculation phase disorders conjunct spermatozoa approximately during hours (Harper, premature, deficient/partial and , 1994). The filtering action of the cervical mucus is a anejaculation, azoospermic ejaculation and urinary mechanism to guarantee that only the fittest incontinence. Orgasmic disorders include anorgasmia spermatozoa ascend toward the site of fertilization. and the so called postorgasmic illness syndrome Cervical mucus from infertile women contains (Jannini and Lenzi, 2005). Even though all these cytotoxic antibodies to their partner´s spermatozoa conditions may be conceived as disorders and in many inhibiting sperm motility (Marthur et al., 1988). Even cases could be associated with abnormal conditions, at though the cervix represents a major barrier to sperm least some of them might also reflect physiological ascent, many spermatozoa reach the uterus. In strategies to cope with sexual competition and/or contrast, in those mammals which ejaculates are promiscuity and may have psychogenic and organic deposited in the uterus, e.g. pigs, a great quantity of components (Lawrence, 1984; McDonnell, 1992). In sperm is found in uterus (Harper, 1994). Nevertheless, the following paragraphs we will speculate on this the uterotubal junction constitutes a barrier to sperm possibility by commenting on cases and ecological ascent. The uterotubal junction is between the uterus scenarios where a presumed ejaculatory dysfunction and the . During transit into the female tract, could have an adaptive value. sperm undergo the so-called capacitation, and is required for fertilization. This consists of a We will begin by considering . destabilization of the plasma membrane of sperm head Main stream urologists, sexologists and human without any visible morphological changes. reproductive biologists would probably coincide that premature ejaculation is undoubtedly the most In a few words sperm transport depends on several frequent ejaculatory problem encounter in their factors, not only of flagellar movement. In the male medical practice (Jannini and Lenzi, 2005)) tract depends on seminal plasma, the contraction of the Nevertheless, as mentioned before, short ejaculatory reproductive ducts and muscles of the perineum. This latencies are characteristic of subordinated males. In allows the expulsion of semen through the urethra. natural settings, this behavioral feature exemplifies a Once deposited the semen in the female, sperm reproductive strategy that allows males to increase transport depends on the pressure of the seminal plug their chances of having copulatory encounters (if applicable), changes of the intravaginal pressure avoiding the physical confrontation with dominant and activity of the oviduct to reach the site of males and the possibility of being harmed (Lawrence, fertilization. 1984). Also ejaculating faster would increase the males’ opportunities to copulate with more females. In this context, prematurely ejaculating males could well DISORDERS OF EJACULATION: FALLING represent an endo- that can be modified by HOPES WITH ADAPTIVE VALUE? sexual training or by changing social status, but it is never considered as an abnormal condition. Thus, Until a few years ago, the human medical community human males “suffering” of premature ejaculation considered ejaculatory disorders as having a purely might only represent a phenotypic variety associated psychological etiology. Fortunately, this concept with “unconscious” subordination. The observation changed over the past decade or so, springing the that premature ejaculation is diagnosed to a similar elaboration of a wealth of studies aimed at percentage (25 %) among male human populations characterizing the psychological and organic factors around the world regardless of credence and of that lead to “ejaculatory disorders” in human and non- economical or social status (Jannini and Lenzi, 2005), human mammalian species (e.g., rats, mice and horses) lends support to this notion.

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Human delayed ejaculation is also considered as an In many cases such “dysfunctional states” might only ejaculatory malfunction (Jannini and Lenzi, 2005). In be distinct functional traits that clearly reflect the male rodents, however, delayed ejaculation has an variability and plasticity of the mammalian sexual adaptive value since female rats require long-lasting phenotype. Unfortunately, biological evolution is not stimulation to reach the sexual excitement needed to driven by social precepts and does not necessarily increase their chances of getting pregnant (Toner and match social needs. Adler, 1986). This may explain why dominant male rats in the wild have developed a copulatory strategy that enables them to delay their ejaculation for CONCLUDING REMARKS approximately 30 minutes while providing adequate female ; if males succeed their Ejaculation constitutes a fundamental process in the inclusive fitness may increase (Pattij et al., 2005). males’ . The process requires efficient Once again, delayed ejaculation in humans may only propulsion system to ensure semen transport through reflect a phenotypic variation related with reproductive the male urethra and its expulsion into the strategies that could increases their possibilities of vaginocervical tract. In spite of one spermatozoon is fathering offspring, and do not necessarily reflect a required to fertilize an ovum, millions of them are dysfunctional state. expelled, presumable due to sperm competition. Great efforts have been made by mammalian males to evolve Mammalian males may show no ejaculation or intricate mechanisms essentially designed to avoid produce azoospermic ejaculates in spite of displaying wasteful use of semen (e.g., prudent sperm allocation). normal and persistent mounting and Although it is conventionally believed that males are thrusting. Although at first glance both circumstances always ready to copulate and ejaculate, the evidence might seem abnormal and non-sense since males discuss support that neuroendocrine mechanisms exert would decrease their inclusive fitness, self-assurance powerful inhibitory actions that must be overcome by and sexual interest while increasing their frustration the male to achieve ejaculation. And even then, subtle and aggressiveness (McDonnell, 1992), anejaculation mechanisms as yet poorly understood prevent males to and azoospermic ejaculation could also have an make unrestrictive use of their costly reproductive adaptive value in natural, ecologically meaningful resources under unfavorable copulatory contexts. The settings. In particular, if males are confronted with existence of different male copulatory , copulatory contexts of relatively high intra-sexual even those considered as ejaculatory disturbances in competition, they may choose during copulation to humans, may be considered as reproductive strategies remove the semen of their competitors that copulated evolved through evolution. before with the female (Ramm et al., 2005) while saving their own sperm stores for better opportunities. Even though under this scenario males would not win REFERENCES the competition, they would certainly impair the reproductive success of their competitor males. A Allard, J., Truitt, W.A., McKenna, K.E., Coolen, L.M. similar case might be casted for deficient or partial 2005. Spinal cord control of ejaculation. ejaculation since it could very well be the result of World Journal of . 23:119-126. physiological mechanisms modulating differential sperm allocation under high pressures associated with Aumuller, G., Seitz, J., Lilja, H., Abrahamson, sperm competition. T.A.,Vonderkammer, H., Scheit, K.H. 1990. Species-specificity and organ-specificity of The last example of “ejaculatory dysfunctional states” secretory proteins derived from human that might have an adaptive value when evaluated in prostate and seminal vesicle. Prostate. 17:31- natural setting is the so called anorgasmia (Jannini and 40. Lenzi, 2005). How can anorgasmia be adaptive at all for males? Ejaculation and orgasm are known to Beach, F.A. 1967. Cerebral and hormonal control of reinforce the couple´s bonding strength (Nelson and reflexive mechanism involved in copulatory Purdon, 2011). This, however, is opposite to the behavior. Physiological Reviews. 47:289-316. reproductive interests of males whose instincts are known to drive them to look after more than a single Beach, F.A. 1969. Locks and beagles. American female to fathering offspring. Clearly, if males avoid Psychologist. 24:971-989. the reinforcing effects of ejaculation and orgasm through anorgasmia, they could pursue more easily Bermant, G., Clegg, M.T., Beamer, W. 1969. their reproductive interests by creating lose bonds with Copulatory behaviour of the ram, Ovis aries their reproductive female partners. I: A normative study. Animal Behaviour. 17:700-705.

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Submitted September 09, 2011– Accepted October 25, 2011 Revised received November 09, 2011

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