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Try out PMC Labs and tell us what you think. Learn More. The sheep offers a unique model to study male sexual behavior and sexual partner preference. Rams are seasonal breeders and show the greatest libido during short days coincident with the resumption of ovarian cyclicity in the ewe. Threshold concentrations of testosterone are required for the acquisition and display of adult sexual behavior. In addition, estrogens produced from circulating testosterone by cytochrome P aromatase in the preoptic area are critical for the maintenance of sexual behaviors in rams. Sex differences in adult reproductive behaviors and hormone responsiveness are the result of permanent organizational effects exerted by testosterone and its metabolites on brain development.

Early exposure to ewes enhances ram sexual performance, but cannot prevent some rams from exhibiting male-oriented sexual partner preferences.

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Neurochemical and neuroanatomical studies suggest that male-oriented ram behavior may be a consequence of individual variations in brain sexual differentiation. Scientists have used laboratory animals primarily rats for many years to study physiological mechanisms underlying the regulation of behavior. The information acquired from this body of work has been pivotal. The rat has been a convenient model that provides preliminary information that, at least in part, can be applicable to other species, including humans. Therefore, we have a large repository of information about the natural history and physiology of the laboratory rat.

The rat, however, may not always be the best model for a particular research project. Recently the domestic sheep has become valuable as a tool for understanding sexual behavior, neural and endocrine systems related to reproduction. Although there is an abundance of information about domestic sheep, most of it is written from an animal husbandry perspective.

The purpose of this article is to review information about the natural history, behavior and physiology of the domestic ram for scientists who may be interested in using sheep as a model for their work in behavioral endocrinology and physiology. This paper will review our current understanding of the biological and social aspects of sexual behavior in domestic rams. Sheep were domesticated in southwest Asia around B. Mouflon are restricted mainly to Mediterranean islands. All wild type sheep can interbreed and are considered a single species.

Domestic rams can interbreed with wild type ewes if a wild ram is not present Ryder M. Scientists speculate that the Mouflon is the progenitor of all European Women want sex Bighorn Ryder M. All domestic sheep, as well as the wild Mouflon, have 54 chromosomes Vorontsov N. Domesticating sheep did not alter their new inheritance, but rather allowed for a greater range of variation to survive. The observations of variation led to selective breeding for preferred traits such as a wooly fleece, longer tails and no horns Ryder M.

Sheep breeders have used artificial selection by selective breeding over many generations. These selection criteria differ widely around the world and have resulted in numerous modern breeds. There is a critical period, that lasts only for a few hours following the birth of lambs, during which lambs develop a sensory image of their mother or substitute; for review on this topic see Women want sex Bighorn by Nowak et al.

The ewe learns to identify her own lamb during this same critical period. It is this ability to bond to humans during a critical period along with the inherent flocking behavior of this species that contributed to the early ecological relationships between humans and sheep Lay D. Reproductive efficiency is an important selection criterion for sheep. In a modern day sheep operation, females that fail to become pregnant are eliminated from the flock. Since the recommended stocking ratios for American sheep producers is between and rams to ewes, sheep producers must be certain that their rams are efficient breeders.

The serving capacity test was first developed by Mattner and colleagues in Australia Mattner et al. Rams can be classified as either sexually active or sexually inactive after their first test with females. Sexually active rams are ased an ejaculation score total of ejaculations in 30 minutes. Rams that are sexually active on their first test rarely become inactive. If they are tested repeatedly with females, they can be ased a serving capacity score, which is the average of ejaculations each ram achieves over repeated 30 min.

Rams classified as high libido show an average of 5—6 ejaculations within 30 min, whereas low libido rams perform less than 4 ejaculations. Among the sexually active rams, serving capacity scores are predictive of fertility success in pasture matings Price, At the U. Sheep Experiment Station in Dubois, Idaho serving capacity tests were routinely used to select potential sires and to identify individuals that fail to become sexually active. Hundreds of rams have been tested annually for the past 18 years.

There are many different reasons for poor performance during a serving capacity test. The first major observation made during the use of the serving capacity test is the tremendous variation in sexual behavior of rams. Some rams are immediately stimulated by the ewes and begin courtship and mounting within minutes of being Women want sex Bighorn into the testing pen. Other rams fail to even investigate the ewes and never direct courtship behaviors toward them. Some sexually inactive rams will begin to copulate when provided with additional opportunities.

These rams are typically called low sexual performers because they inseminate fewer females Perkins et al. Among the group of rams identified as sexually inactive, are rams that will not mount females but will mount male pen-mates. A ram that fails to become sexually active when exposed individually to at least three estrous females for 20 minutes on repeated occasions, and that mounts males exclusively in the presence of estrous females is classified as a male-oriented ram see Mate Preference.

Sheep are polygamous breeders. Rams use olfactory cues to detect estrous ewes Lindsay, If a receptive ewe is introduced into a pen containing a ram with prior copulatory experience, the ram will approach Women want sex Bighorn within several seconds. There are several stereotyped behaviors that the ram may engage in prior to his initial mount. These include sniffing the genital region of the ewe; pawing at her flank repeatedly with his foreleg while standing behind and at a small angle to her foreleg kick ; and nuzzling, licking and nibbling at her flank and ano-genital area.

The flehmen response draws non-volatile odors into the vomeronasal organ for detection by the accessory olfactory system. There is considerable variation among males in the frequency and duration of these precopulatory responses. It is not clear whether they play a functional role in stimulating the ewe or inducing her to stand for copulation.

A fully receptive ewe stands quite still after the initial approach by the ram and will often turn her head to one side and appear to watch him. There is also a characteristic wagging of the tail fanning that accompanies full receptivity and which may help disperse relevant olfactory cues.

Mounting behavior in rams is accompanied by a series of shallow pelvic thrusts. Rams usually mount several times prior to vaginal penetration and ejaculation, but an experienced ram may ejaculate on the first mount. Rams are capable of multiple ejaculations with a single ewe, although the intervals between successive ejaculations become progressively longer Bermant et al. Copulatory behavior can be measured in a serving capacity test where a ram is paired with 3—4 estrous ewes as described above, or in tests where an individual ram is paired with an individual estrous ewe.

Copulatory behavior tests are usually time-limited and last at least 10 minutes during which a of measurements can be taken. These include: mount latency, mount frequency, ejaculation latency, ejaculation frequency, and post-ejaculatory interval. Sheep in temperate climates are seasonally breeding mammals that are reproductively active after the summer solstice as the day length declines in the late summer and fall. Decreasing day length stimulates the release of gonadotropins, which drive gametogenesis and gonadal steroid hormone secretion in both males and females Martinet et al.

Seasonal activation of the reproductive axis initiates cyclic elevations of progesterone and estradiol that triggers the expression of estrus behavior in the ewe, and stimulates increased production of testosterone by the testis, which in turn triggers the expression of libido in the ram.

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Most domestic rams will mate out of season, but do not exhibit peak performance unless given regular exposure to estrous ewes Tulley and Burfening, ; Tilbrook and Cameron, Therefore, behavioral studies are best planned during the peak-breeding season in the fall and early winter. Seasonality of breeding in feral and wild populations of sheep is associated with segregation of the sexes for much of the year. Ewes are gregarious by nature and flock together for grazing, protection, and rearing of young lambs. Young rams up to 2 years old are present with the ewe flock in most wild populations.

Feral and wild adult rams tend to be more solitary although some breeds such as Soay and wild Mouflon form male groups. As the breeding season rut approaches, males congregate and often engage in fights that are believed to stabilize dominance hierarchies. During the rut, rams disperse and move through the flock in search of estrous ewes. The rut is usually spread over two or three weeks in mountain sheep, Soay and Mouflon breeds, but rams may stay with the ewes for up to eight weeks.

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After the breeding season has finished, rams re-establish a male group and move away from the ewe home-range areas. In contrast to wild populations of sheep, sexual segregation is enforced in most modern husbandry practices by exclusion of rams from ewe flocks, except during breeding. Lambing begins in April at the Field Station. Ewes and lambs are penned together for 2—6 weeks before being moved to summer rangeland. Male lambs are weaned and separated from ewes in August at 4 — 5 months of age. Young rams are kept separate from mature rams until 12 to 18 months of age.

This cycle of breeding begins again in the fall. Testosterone is essential for the development and maintenance of sexual behavior in rams. Sexual activity increases with elevated levels of testosterone during puberty Thwaites, ; Orgeur and oret, The expression of sexual behavior in rams at puberty can be suppressed by treatment with either a Women want sex Bighorn agonist Tilbrook et al. The importance and relationship to sexual behavior of testosterone has been demonstrated by castration and hormone replacement studies. Rams castrated before puberty show reduced or no sexual interest as adults Clegg et al.

Sexual behavior declines in sexually experienced adults after castration and may take up to 12 months before rams completely lose interest Clegg et al. On the other hand, treatment with testosterone stimulates sexual behavior in rams castrated either before puberty Clegg et al.

Likewise, the restoration of sexual behavior with hormone replacement therapy is not immediate but occurs after a few weeks of treatment. Rams that are sexually experienced before they are castrated have been found to sexual behavior more quickly following treatment with testosterone than rams that were castrated prior to puberty Clegg et al. Testosterone is converted to estradiol by cytochrome P aromatase within the central nervous system of rams and there is evidence that this metabolite of testosterone and not testosterone itself is responsible for maintenance of sexual behavior in rams.

Aromatase is enriched within brain regions important for the control of male reproductive behaviors Roselli et al. As was shown originally in rodents Damassa et al. There is no correlation between circulating levels of testosterone or other androgens and the level of sexual activity Knight, ; Schanbacher and Lunstra, ; Howles et al. Treatments with exogenous androgens neither initiate sexual activity in sexually inactive rams Knight, nor enhance behavior in sexually active rams Lincoln and Davidson, Thus, although circulating testosterone is an important physiological regulator of sexual activity in rams, it is apparent that other factors must also be involved.

Sex differences in adult reproductive behaviors and hormone responsiveness are the result of organizational effects that gonadal steroid hormones exert during discrete critical periods in early fetal life MacLusky and Naftolin, These early effects of gonadal steroids are permanent, in contrast with the reversible activational actions that steroids exert on behavior after puberty.

Sexual differentiation in mammals will follow the female pattern of differentiation unless the fetus is exposed to testicular hormones, which stimulate cellular programs that direct the development of the male pattern of differentiation MacLusky and Naftolin, Women want sex Bighorn The terms used to describe masculine differentiation are: masculinization, the production of male-typical copulatory behaviors; and defeminization, the suppression of female-typical sexual receptivity.

These terms can also be applied to other behaviors such as sexual partner Women want sex Bighorn and to patterns of gonadotrophin secretion, i. Gestation in the sheep lasts approximately days. Gonadal differentiation occurs between gestational day 25 G25 and G35 and the external genitalia begin to differentiate on G45 Clarke et al. The fetal testes synthesize elevated levels of testosterone starting around G35 Attal, ; Pomerantz and Nalbandov, and the testicular content of testosterone continues to increase from this time until birth.

Fetal males have higher circulating concentrations of testosterone at G65 to G70 than do fetal females Pomerantz and Nalbandov, Concentrations of testosterone in males decline between G70 and G90, and are not ificantly greater than in female until late in gestation and during postnatal life Pomerantz and Nalbandov, ; Roselli et al. Thus, it appears, in sheep, that testicular androgen is available to sexually differentiate males as early as the first trimester of pregnancy.

Short Short, administered testosterone implants to pregnant ewes on G20, G40, G60 and G80 and left the implants in place until parturition. Female lambs exposed to testosterone from G20 or G40 showed complete masculinization of external genitalia.

Those implanted with testosterone on G60 or G80 showed normal female external genitalia although the clitoris was enlarged. Female sheep exposed to testosterone from G20 to G60 until birth, did not display estrus behavior during adulthood defeminization and showed male-like mounting patterns masculinization Short, The suggest that masculinization of the internal and external genitalia in sheep occurs during the early phase of elevated fetal testosterone and behavioral masculinization occurs later. Clarke and colleagues Clarke et al. The greatest degree of genital masculinization was achieved in ewes exposed to testosterone over days G30 — G80, whereas the greatest behavioral masculinization and defeminization was seen in ewes exposed to testosterone over either G50 —G or G70 — G

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The Neurobiology of Sexual Partner Preferences in Rams