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Chapter 17: Seasonal regulation of reproduction.

CHAPTER OBJECTIVES

* Discuss the importance of harmony between an animal's reproductive activity and the environment.

* Describe the major strategies of seasonal reproduction in mammals.

* Describe the major environmental variables underlying seasonal reproduction.

* Describe how mammals use annual rhythms in photoperiod and rainfall as cues to initiate and terminate reproductive activity.

* Describe the physiologic mechanisms whereby environmental stimuli affect reproduction.

BACKGROUND

As noted in Chapter 1, the success of a particular species depends on the ability of individual members of the species to survive and reproduce viable offspring. In order to accomplish this, an organism must have the ability to cope with its environment. Most mammals live in environments that change with the season. Under these circumstances, natural selection favors individuals that can cope with seasonal changes in variables such as ambient temperature and food availability. With respect to reproduction, natural selection promotes adaptations that restrict reproductive activity to times when environmental conditions favor pregnancy and rearing of young. Therefore, it should come as no surprise that most mammals exhibit some degree of seasonal variation in their reproductive activities. In the most extreme cases, the so-called seasonal breeders, reproduction is restricted to only part of the year. In less extreme cases, animals will show reproductive activity throughout the year, but the intensity of activity varies with season. In females that breed seasonally, expression of ovarian cycles is confined to a particular time of year. At other times these animals experience a complete cessation of estrus and ovulatory cycles. In seasonally breeding males, testicular size, testosterone production, and spermatogenesis decrease at certain times of the year. The degree of this decrease in testicular function can vary between complete infertility to reduced fertility.

REPRODUCTIVE STRATEGIES AND THE ENVIRONMENT

The reproductive characteristics of individual members of a species constitute the species' reproductive strategy. A reproductive strategy is a function of an individual animal's genotype, but the particular genes responsible for these traits are expressed because of natural selection. When considering how an animal's environment causes changes in its reproductive activity, it is useful to think in terms of ultimate and proximate causes. You have already encountered these concepts in reference to the causes of sexual behavior. Ultimate causes of environment-induced changes in reproductive activity are evolutionary processes that shape the annual reproductive cycle of a species. In contrast, proximate causes refer to the physiologic mechanisms that mediate the effects of various environmental stimuli on individuals. The relationship between food availability and reproductive activity in seasonal breeders such as sheep illustrates the difference between ultimate and proximate factors. Over the eons, seasonal changes in availability of food imposed selection pressure that favored lambing and suckling of lambs during a time of year when food is abundant (i.e., during spring and summer). It is not the availability of food per se that drives seasonal patterns of reproduction in sheep. Rather these animals use annual fluctuations in photoperiod as cues to predict when food availability is generally greatest. In this case, food availability is an ultimate cause of seasonality. This is not to say that food availability doesn't exert direct effects on reproduction. The restriction of food intake resulting from a lack of adequate food supplies suppresses fertility in all mammals by depriving them of the amount of calories required to support reproductive processes. This direct effect of food intake on the physiologic mechanisms regulating reproduction is an example of how food availability acts as a proximate cause of variations in reproductive activity.

The focus of this chapter will be on the ultimate causes of environmental effects on reproduction in mammals; that is, mechanisms regulating seasonal breeding. It is not possible to provide detailed accounts of the numerous ways mammals have adapted to seasonal fluctuations in their environments. Therefore, we will examine only a few of the most thoroughly documented examples. As we study these cases, it is important to keep in mind that the seasonal components of a species' reproductive strategy are shaped by both intrinsic and extrinsic variables. Intrinsic variables include: life span, ultimate body size, length of the female's reproductive cycle (from puberty to weaning of offspring), feeding strategy, and the presence of some seasonal survival mechanisms, such as hibernation. Extrinsic variables include: the nature, severities and timing of climatologic changes, dietary challenges, competition for resources, and predator pressure.

Strategies for Seasonal Breeding

Mammals cope with seasonal changes in environment via two basic strategies: 1) reacting directly to variations in an environmental variable and 2) reacting to environmental cues that predict periods that are favorable to reproduction. In the first case, reproduction is not linked to seasonal cues such as annual patterns of day length. Mammals that rely on this strategy are facultative seasonal breeders, meaning that seasonal fluctuations in reproductive activity occur only when there are seasonal fluctuations in some variable that is necessary for reproduction (e.g., adequate food). The reproductive strategies of facultative seasonal breeders can be viewed as opportunistic. In other words, they will breed at opportune times. A good example is the house mouse (Mus musculus). Under field conditions these animals reproduce between April and November in northern temperate climates. However, when living commensally with humans (i.e., in their dwellings with abundant food), they will reproduce throughout the year. In general, facultative seasonal breeders are small and have high reproductive rates due to rapid development, short gestation periods, and short postpartum periods. These characteristics allow these animals to produce large numbers of offspring for as long as conditions support the reproductive processes.

Larger mammals will also express seasonal fluctuations in reproductive activity when living in environments where there are marked fluctuations in food supply. For example, hunter-gatherer societies living in regions where there are marked fluctuations in food availability (e.g., the !Kung people of the Kalahari desert in Africa) exhibit seasonal fluctuations in pregnancy rate among women. In each of these examples, food availability is affecting reproductive activity via altering the number of calories available for reproduction; that is, it produces immediate beneficial or detrimental effects on the reproductive fitness of an individual.

Obligatory seasonal breeders rely on environmental cues to predict when conditions will be favorable for successful reproduction. These animals are typically larger, and live longer than the majority of facultative seasonal breeders. They also have lower reproductive rates due to slower rates of sexual maturation, longer gestation lengths, and longer postpartum periods. Because of their longer gestation periods, mating occurs at a time that precedes birthing by several months. These mammals rely on mechanisms to ensure that breeding occurs at a time that results in offspring being born when the mothers have adequate food to support lactation. The domestic sheep is arguably the most familiar and most thoroughly studied example of this type of seasonal breeder. In temperate climates, the ewes of most breeds express a period of seasonal anestrus. Although the length of this anestrous period varies among breeds, it typically occurs during long days (between April and September in the northern hemisphere). Figure 17-1 shows the average seasonal fluctuation in expression of estrous cycles for several popular breeds of sheep when maintained in temperate climates (e.g., latitude 45_N). Recall that the gestation length of sheep is approximately 5 months. Thus mating during the first part of the breeding season results in lambs being born in late February and early March when food availability is beginning to increase. Unlike facultative seasonal breeders, sheep and other obligatory seasonal breeders cannot take advantage of sudden increases in food supply during the anestrus season. Increased feeding does not overcome seasonal anestrus in these animals.

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The sheep is an example of a short-day breeder. In other words, breeding is restricted to a time of year when photoperiod is short. Not all seasonal breeders are short-day breeders. For example, horses are long-day breeders. Figure 17-2 illustrates the major stages of seasonal reproduction in mares in northern, temperate climates. Mares begin to express estrous cycles as early as February, but ovulation is variable until May (spring transition period). Maximum fertility of mares occurs between May and September. Ovulation continues in a variable manner during the autumn transition to anestrus (October through December). Because of their 12-month-gestation length, this breeding season ensures that foals are born in the spring and summer, a time when there is likely to be enough food to support lactation.

ENVIRONMENTAL FACTORS UNDERLYING SEASONAL BREEDING

The previous discussion has established that virtually all mammals have the capacity to express seasonal changes in reproductive activity. In this section, we will consider what aspects of the environment influence the patterns of reproduction in these animals. As noted in the previous section, food availability is a major driving force in this regard. Reproduction, like all other physiologic processes, is an energy-consuming process. Thus a deficit in energy consumption can suppress reproductive activity in an animal. Reduced reproductive activity can also result from an increase in use of energy for other vital processes, including cellular maintenance, thermoregulation, locomotion, and so on.

Food

As noted earlier, food can affect reproductive activity in both a proximate and ultimate way. Our concern in this section is with the proximate effects of food on reproduction. There is an abundance of information concerning the effects of food intake on reproductive activity of mammals. Most of this work has dealt with the effects of food restriction on sexual development and onset of puberty in females. Restriction of food intake delays age at first ovulation in all species studied. Figure 17-3 illustrates this effect in heifers. Other effects of food restriction on female reproductive activity include disruption of estrous cycles and reduced milk production. Pregnancy appears to be quite resistant to food deprivation, at least in large mammals that have large energy stores. In these cases, females draw on their own body stores of energy to maintain pregnancy. However, feed restriction during pregnancy can result in lower milk production and a longer postpartum anestrous period.

Restriction of food intake also disrupts reproductive activity in males. In adolescent males food restriction will impair steroidogenesis and delay sexual maturation. Severe and prolonged food restriction will disrupt both spermatogenesis and steroidogenesis in adult males.

Most studies have not been directed at identifying the particular nutrient deficiencies that are responsible for impaired reproduction during restricted feed intake. However, it is generally accepted that many of the detrimental effects of food restriction on reproduction can be attributed to a lack of dietary energy. Nevertheless a deficiency in particular nutrients (vitamins, minerals, amino acids, and fatty acids) can also disrupt reproduction in males and females.

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Energy Metabolism and Reproduction

Food intake is only one of several variables that affect the amount of energy available for reproduction (Figure 17-4). The extent to which a particular amount of dietary energy can sustain reproductive activity depends on how much energy is consumed by other physiologic processes as well as how much energy the animal can mobilize from its storage depots. Major energy-consuming processes in adult mammals include cellular maintenance, thermoregulation, locomotion, growth, and lactation. During times of feed deprivation an animal offsets its deficit in dietary energy by mobilizing energy substrates from adipose tissue, muscle, and the liver. Whether or not an animal reproduces depends on a delicate balance among food intake, rate of energy consumption, and mobilization of energy substrates.

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Ambient Temperature

Mechanisms regulating body temperature consume a considerable amount of energy. Mammals are homeotherms; that is, they maintain their body temperatures within narrow ranges in spite of fluctuations in ambient temperature. An animal does not have to expend energy to maintain its body temperature when ambient temperatures are within its thermoneutral zone (Figure 17-5). When ambient temperatures rise above or fall below this zone, the animal makes metabolic and behavioral adjustments that allow it to maintain body temperature. The adjustments mammals make in order to maintain constant body temperature in high and low temperatures are widely different among species.

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Low Temperature

Coping with low ambient temperatures requires an increase in food intake, whereas adjusting to high ambient temperature does not. One of the most important ways a mammal prevents a drop in its body core temperature during low ambient temperatures is to generate heat by increasing its rate of metabolism. This raises the energy requirement of the animal, which it meets by increasing its food intake. The metabolic response to cold temperatures varies considerably among mammals, depending on how well they prevent heat loss. For example, small animals with large surface area-to-volume ratios and animals with poor insulation (due to lack of blubber or thick pelage) respond more robustly to a drop in temperature than larger animals that are well insulated. At any rate, when considering the effects of food intake on reproduction it is important to take into account the ambient temperatures that prevail during times of low food availability. Figure 17-6 illustrates this concept based on studies with rats. It is clear from this example that the effects of reduced food intake are exacerbated by low ambient temperatures. The important implication from these results is that the decrease in reproductive activity expressed by facultative seasonal breeders is probably attributed to the combined effects of a decrease in food intake as well as an increase in dietary energy requirements.

High Temperature

Ambient temperatures that exceed the thermoneutral zone of an animal can also suppress reproductive activity, but such effects are not entirely due to reduced availability of energy substrates. Elevated ambient temperatures disrupt reproductive processes via two major mechanisms; reduced appetite and hyperthermia (elevated body temperature). Figure 17-7 summarizes these effects in the dairy cow, which has been the focus of study for many years. As noted in the previous chapter, females typically experience a period of negative energy balance early in the postpartum period. Heat stress during this period results in a reduction in feed intake thereby prolonging this period of metabolic insufficiency. In addition to reducing milk production, the reduced caloric intake suppresses pulsatile release of gonadotropin-releasing hormone (GnRH)/ luteinizing hormone (LH). This can disrupt follicular maturation (i.e., deviation), estrus, and ovulation resulting in ovulation of poor-quality oocytes, or under severe cases, extending the length of the postpartum anestrous period. Hot temperatures can also disrupt reproduction via behavioral mechanisms. Under such conditions males and females become lethargic and are less likely to express appropriate reproductive behaviors. This may prevent mating, or promote poor timing of insemination relative to ovulation.

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Elevation of an animal's body temperature (hyperthermia) can exert direct (independent of reduced caloric intake) effects on reproduction. The physiologic mechanisms mediating the inhibitory effects of high temperature on reproduction have been studied extensively in livestock, but most of the work has focused on the female. In general, hyperthermia disrupts spermatogenesis in males and reduces conception rates in females. The major effect of heat stress in females is a compromised uterine environment.

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However, there is also evidence that maternal hyperthermia exerts direct effects on the embryo. The combined effects on the uterus and embryo result in increases in embryo mortality.

Other Factors

Seasonal variations in the reproductive rates of mammals are influenced by variables other than food availability and ambient temperature. Our discussion of nutrition and reproduction has been narrowly focused on the importance of energy substrates. However, it is also likely that other nutrients can influence reproductive activity. Certainly deficiencies of vitamins, minerals, essential amino acids, and long-chain fatty acids can have negative effects on reproduction. Unfortunately, we lack detailed information concerning the roles of the substances in expression of seasonal patterns of reproduction. Three additional factors are likely to play a role in regulation of seasonal breeding are: 1) competition for limited resources, 2) predation pressure, and 3) social interactions. Each of these can act as ultimate causes of seasonal breeding. Selection pressure from competition with or predation by other species could favor a breeding season that is either synchronized with or out of synchrony with those of competitors or predators. With respect to competition, the latter strategy would avoid over-consumption of resources. In the case of predation, synchrony between predator and prey reproduction might enhance the fitness of the prey species by satiating the predators. On the other hand, asynchrony between reproductive activities might provide some adaptive advantage to prey by reducing loss of very young offspring. Social interactions can act either as proximate or ultimate causes of seasonal breeding. An example of a proximate cause would be the so-called ram effect in ewes. Ewes that have been isolated from a ram for several weeks during seasonal anestrus will express estrus and ovulate upon exposure to a male. The mechanism involves an increase in frequency of LH pulses, which promote development of a preovulatory follicle. On the other hand, social cues can serve as a means to predict periods that are favorable to reproduction. In this case, social cues act as ultimate factors. Examples of this phenomenon will be described in the next section.

Before we leave this discussion of how the environment can cause seasonal changes in reproductive activity it is important to emphasize that none of the aforementioned factors acts alone. Rather, the pattern of reproduction expressed by members of a species reflects the combined actions of food availability and ambient temperature.

REGULATION OF SEASONAL BREEDING BY ENVIRONMENTAL CUES

As noted earlier, some mammals rely on seasonal cues to regulate the time of reproductive activity. These mechanisms are typically viewed as time-keeping mechanisms. In other words, they allow the animal to keep track of the time of year such that it can prepare metabolically for seasons that are either conducive or hostile to successful reproduction. Of course such mechanisms are only advantageous in climates where there are reliable annual cycles in climate and/or availability of nutrients. They would offer little advantage when climatic and dietary conditions are more variable. In this case opportunistic mating strategies offer an advantage.

Photoperiodic Control of Seasonal Breeding

Photoperiod appears to be the most important environmental cue regulating seasonal reproduction in mammals. In latitudes north and south of the equator there are annual cycles in day length that do not vary from year to year. Figure 17-8 illustrates the annual cycle of photoperiod in the northern hemisphere (e.g., latitude 45_N). Twice during the year, the length of the light and dark periods is the same; i.e., the spring and autumn equinoxes. The longest day of the year occurs on the summer solstice, whereas the shortest day occurs on the winter solstice. Day length increases between the winter solstice and summer solstice, then decreases between the summer solstice and winter solstice. This pattern of photoperiod suggests three strategies whereby photoperiod can be used to regulate seasonal reproduction. First, a critical day length may both induce and terminate reproductive activity. For example, the spring equinox might induce gonadal activity, whereas the autumn equinox might terminate gonadal activity. Such a strategy would allow animals to reproduce more than one time each year. A second strategy is that a particular day length either stimulates or inhibits gonadal activity. For example, reproductive activity might begin at the spring equinox and continue for some predetermined length of time. This too would permit animals to reproduce more than once each year. Note, however, that this approach requires some type of internal timer that measures length of the breeding or nonbreeding season. The third strategy involves synchronization between an internal and external rhythm. In this case, the annual cycle of reproduction is driven by an endogenous circannual rhythm, which somehow becomes synchronized (entrained) with the external cycle of photoperiod. Although all of these strategies are possible, only the second and third have been documented in mammals. Syrian hamsters (Mesocricetus areatus) employ the second strategy, whereas the domestic sheep uses the third strategy. Each of these examples will now be considered.

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Photoperiod and Reproduction in the Syrian Hamster

Gonadal activity in the Syrian hamster is at a minimum between November and January (Figure 17-9). In late winter (February) the gonads begin to recrudesce (become active again) and reach full activity around the time of March. Gonadal activity remains high throughout the spring and summer, but then diminishes beginning in late summer. This seasonal pattern of gonadal activity is produced via the following mechanisms. First, gonadal regression is induced when day length becomes less than 12.5 hours. The gonads remain inactive for 4 to 5 months, but then begin to recrudesce because the animal becomes refractory to the short day lengths. They will remain active throughout the summer, but then regress due to decreasing day length. It is clear that in the Syrian hamster, short days signal the end of the breeding season and that an internal interval timer, involving refractoriness to the inhibitory effects of short days, times the duration of the breeding season.

Photoperiod and Reproduction in the Sheep

The photoperiodic regulation of reproductive activity in the ewe has been studied extensively and intensively for decades. As noted earlier, sheep are short-day breeders. In temperate zones, ewes begin exhibiting estrous cycles in late summer and will continue to do so until early spring, if they are not mated (Figure 17-10A). If ewes are maintained under a constant photoperiod for several years, they will continue to show recurring cycles of reproductive activity (Figure 17-10B). However, these cycles will eventually become unsynchronized (i.e., not all ewes at the same stages at the same time) and will not coincide with natural cycles of day length (reproductive activity does not necessarily occur during short-day lengths) because the periods of these cycles are less than 1 year. This response illustrates the existence of an endogenous cycle of reproductive activity (circannual rhythm). When sheep are exposed to natural fluctuations in photoperiod, their internal rhythms in reproductive activity become entrained by the external rhythm of day length.

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The synchrony between the ewe's annual cycle of reproduction and the annual cycle of day length is evolutionarily significant in two ways. First, this strategy synchronizes the estrous cycles of ewes. Second, it causes lambing to occur at a time when food availability favors lactation and survival of young lambs.

Other Environmental Cues

How might animals predict opportune times for breeding when photoperiod is not a reliable indicator of environmental conditions? For example, due to dynamic weather conditions, photoperiod is not a reliable predictor of the onset and termination of plant growth in high-altitude environments such as the one found in the American Rocky Mountains. The montane vole appears to rely on the emergence of some types of grass as a predictor of availability of green grass. The stimulus appears to be a compound that is present in high concentrations in fresh green shoots. Other plant compounds may act as predictors of environmental conditions in other species.

NEUROENDOCRINE MECHANISMS MEDIATING THE EFFECTS OF ENVIRONMENT ON REPRODUCTION

The interface between an animal's external environment and its reproductive activity involves neuroendocrine mechanisms. In other words, the ability of an external stimulus to influence gonadal activity requires detection of the stimulus by the central nervous system, generation of a neuronal signal, and transformation of the neuronal signal into an endocrine signal that effect changes in reproductive activity. Our understanding of interfaces between the environment and the reproductive system is most complete with respect to how changes in photoperiod and feed intake affect gonadal activity. There is also a fair amount of information concerning how social cues influence reproduction.

Food

The importance of adequate nutrition in developing and maintaining reproductive activity is well documented. One of the more familiar examples is the relationship between nutrition, growth and onset of puberty. As noted earlier, growth rate during the prepubertal period is inversely related to age at puberty. It is also well known that infertility occurs when adults lose significant amounts of body weight. For example, amenorrhea and anovulation are common in women who engage in intensive athletic training or who suffer from various types of anorexia. A nutritional anestrus is also well documented in livestock. The vast majority of studies dealing with the relationship between food intake and reproduction have involved females. However, there is sufficient evidence to support the idea that food restriction reduces fertility in both males and females and involve essentially the same neuroendocrine mechanisms.

Several hypotheses have been developed to explain how nutrition influences gonadal activity. According to the first hypothesis, a so-called critical amount of body fat is required for normal reproductive activity. In spite of the popularity of this hypothesis, there is no empirical data to support it. There is support for modifications of this hypothesis. There is a growing consensus that some sort of metabolic signal, rather than body fat, mediates the effects of food intake on reproduction (Figure 17-11). According to the first version of this hypothesis, metabolic hormones (insulin, growth hormone, etc.) that reflect different metabolic states act as signals that regulate the reproductive system. Alternatively, the availability of metabolic fuels (e.g., glucose, fatty acids, and amino acids) acts might act as signals mediating the effects of nutritional status on reproductive activity. In either case, metabolic signals that reflect feed restriction might act to suppress pulsatile LH secretion, whereas signals that reflect the well-fed state might enhance pulsatile LH secretion. There are ample data showing that feed restriction reduces LH pulse frequency by suppressing the pulsatile release of GnRH. Such decreases in LH secretion impair gonadal function by disrupting steroidogenesis and gametogenesis.

Photoperiod

In order to understand how photoperiod regulates seasonal breeding, it is important to consider the following issues: 1) How do animals keep track of seasonal changes in day length? and 2) How are signals that provide information about these changes transformed into signals that affect the reproductive system? The most complete answers to these questions come from work with the ewe. The answer to the first question requires an understanding of the neuronal pathways that monitor photoperiod. The retina is the only photoreceptor in mammals and is therefore the most likely candidate for detection of photic stimuli. Information about daylight is transmitted from the retina into the central nervous system via the retino-hypothalamic tract (Figure 17-12). Neurons from the retinal photoreceptors innervate the suprachiasmatic nuclei and impinge upon other neurons that project to the superior cervical ganglion via the accessory optic tract. Neurons of this tract interact with ganglionic neurons, which re-enter the brain and terminate at the pineal gland and endocrine gland that produces melatonin. This hormone is released into the blood (the pineal gland is a circumventricular organ and is not protected by a blood-brain barrier) as well as the cerebrospinal fluid. Melatonin then acts on the hypothalamus to regulate seasonal changes in the pattern of GnRH release, which effects changes in gonadal function.

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The role of the pineal gland is to provide information about daily photoperiod. Melatonin is secreted in a circadian pattern; that is, secretion is minimal during light and maximal during darkness. Thus the pattern of melatonin release provides an accurate depiction of the daily light-dark cycle (Figure 17-13).

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The precise role of melatonin in regulation of seasonal breeding patterns in sheep is unclear. However, reproductive biologists agree that melatonin itself does not stimulate or inhibit reproductive activity. Its role appears to be more of a time-keeping signal than a driver of the seasonal transitions between gonadal activity and quiescence. One well-accepted hypothesis is that patterns of melatonin mediate the synchronization between an endogenous circannual rhythm in reproductive activity and the external annual rhythm in day length.

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Although our understanding of how melatonin regulates hypothalamic release of GnRH is limited, there is a good deal of information regarding the effects of photoperiod release of gonadotropins. The pulsatile pattern of LH release appears to play a central role in mediating the effects of photoperiod on gonadal activity. Much of our understanding of these effects comes from work with ewes. We have already considered the regulation of the ovarian cycle of ewes in Chapter 10. Recall that estrus and ovulation require development of a pre-ovulatory follicle, which emerges from a wave of follicle growth. During seasonal anestrus, ewes exhibit waves of follicle growth, but dominant follicles fail to attain the pre-ovulatory stage of development. This is due to the fact that LH is released in a low-frequency pattern during anestrus. In sheep, exposure to long days results in a decrease in LH pulse frequency. This is the result of steroid-dependent and steroid-independent mechanisms. The steroid-dependent mechanism involves an increase in responsiveness to estradiol negative feedback, a state that resembles the pre-pubertal period. Figure 17-14 summarizes the current theory for the hormonal control of seasonal breeding in the ewe.

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Social Factors

There are no studies to support the idea that social factors can serve as cues to regulate seasonal breeding in mammals. However, such cues can and do affect reproductive activity in ways that can dramatically alter seasonal patterns of reproduction. One of the more dramatic examples is the so-called ram effect in ewes. Introduction of a ram to ewes that have been isolated from males for several months induces high-frequency patterns of LH release during anestrus. The response is attributed to a pheromone that is secreted by glands located near the horn pits and becomes dispersed in the fleece. Because such an increase in LH secretion is necessary for estrus and ovulation, it appears that introduction of a ram to ewes might disrupt the anestrous period.

Similar male pheromone-mediated effects on reproductive activity have been well documented in rodents. The estrous cycles of female mice kept in a group and isolated from males will become synchronized following exposure to a male mouse (Whitten effect). Moreover, exposure of newly-mated female mice to a novel male will block implantation of embryos (Bruce effect). These effects are caused by pheromones present in the male's urine that presumably disrupt the reproductive activity of females by acting on the hypothalamic-pituitary system.
BOX 17-1 Focus on Fertility: Effects of Space Travel on Reproduction

When biologists speak of environmental effects on
the reproductive physiology of animals it is
generally assumed that the environment being
considered is the one here on Earth. What about
the extraterrestrial environment? During the past
40 years space travel has become common. The
International Space Station is continually inhabited
by humans and is viewed by some as a step
toward the colonization of space. The colonization
of space will require that humans, and possibly
other animals, spend long periods of time away
from Earth. Under these circumstances it is
inevitable that procreation will be attempted.
What are the chances that life forms that evolved
within the Earth's 1 x g gravitational field can
reproduce successfully in hypogravity (>1 x g)?
No one really knows, but there is a growing
number of studies to address this question. At this
time there is only one report documenting the
mating of a mammalian species during a spaceflight.
In this case a male rat was reported to
mate with several female rats, but no pregnancies
resulted. Investigators speculated that the
embryos were resorbed, but it is also possible that
the lack of pregnancies was attributed to
infertility of the males and/or females.

Very few studies have involved assessment of
fertility during or after actual space flights. Due to
the expense and difficulty of conducting long-term
studies in space, many investigators rely on models
that simulate spaceflight. One model involves
confining humans to bed rest with a 6-degree
head-down tilt. The resultant shift in body fluid
and reduced resistance placed on muscles
reproduces major symptoms of hypogravity. A
similar approach has been developed for rats. In
this case the animal is suspended from the base of
its tail to achieve a 30-degree head-down
position.

Based the results of experiments conducted
during actual or simulated spaceflights it is
reasonable to conclude that hypogravity affects
reproductive traits in both males and female.

There is general agreement that actual and
simulated spaceflight have negative effects on
testicular function in males. Male rats experience a
reduction in testes weight and a decrease in circulating
concentrations of testosterone regardless of
the experimental model. In most, but not all,
cases these effects are accompanied by reduced
spermatogenesis. Men subjected to 60 to 120 days
of bed rest with head-down tilt express altered
sperm morphology and a reduced number of motile
sperm. The physiologic basis for these results is
unclear. However, it is worth noting that unlike
the human, the inguinal canals of rats does not
close. Therefore, the reduced sperm count in rats
exposed to actual or simulated hypogravity may be
attributed to retraction of the testes into the
abdominal cavity. Recall that body temperature is
detrimental to spermatogenesis.

More recent studies have focused on the
effects of hypogravity on sperm activity. Bovine
sperm subjected to 360 seconds of freefall and sea
urchin sperm sent on space shuttle missions
exhibited higher velocities than sperm kept at
1 x g. The impact of these effects on fertility
remain unclear at this time.

Our knowledge of the effects of hypogravity
on female reproduction is even less than that for
males. There is no information on the effects of
low gravity on the ovaries of nonpregnant females,
but weights of ovaries and numbers of preovulatory
and atretic follicles in postpartum rats that
were in space between days 9 and 20 of pregnancy
were no different from those of rats that remained
on Earth during the same time period. Finally,
of the three experiments involving female rats
carried on spaceflight mission, only one showed
detrimental effects of hypogravity on pregnancy.
In this case, rats exposed to spaceflight during
gestation had reduced weight gain, prolonged
parturition and gave birth to lighter pups that
showed lower perinatal survival rates. There is no
information concerning the effects of actual
spaceflight on the menstrual cycle of women
because female astronauts are required to
suppress ovarian cycles with the birth control pill.
Studies involving women exposed to simulated
spaceflight conditions are limited and
inconclusive.

Whether or not humans can eventually colonize
space depends on whether the physiologic
processes that regulate our reproductive processes
will function properly under the conditions that
prevail in extra-terrestrial environments.
Microgravity is one such condition. However, there
are other environmental variables that might also
pose barriers to mammalian reproduction. In
addition to hypogravity, people who travel in
space will be exposed to various types of
electromagnetic radiation as well as periods of
hypergravity, each of which can exert their own
effects on reproductive processes.


SUMMARY OF MAJOR CONCEPTS

* Reproductive success depends on the ability of an animal to coordinate its reproductive activity with environmental conditions that are conducive to successful reproduction.

* Harmony between an animal's reproductive state and favorable environmental conditions can be achieved by responding directly to food availability, or by using environmental cues to predict when food availability is sufficient to support reproduction.

* The extent to which sufficient calories will be available to support reproduction depends on food availability, ambient temperature, and energy stores.

* The annual rhythm in photoperiod is highly repeatable and therefore serves as the most common environmental cue to synchronize reproductive cycles with food availability.

* Photoperiod and metabolic status influence reproductive activity via neuroendocrine mechanisms that regulate pulsatile LH secretion.

DISCUSSION

1. It is generally agreed that changes in food availability cause changes in reproductive activity. Differentiate between food as a proximate factor and food acting as an ultimate factor affecting reproductive activity. Give an example of each case.

2. Imagine that you are observing two groups of ewes. One group is allowed to consume feed on an ad libitum basis during the anestrous season, whereas the other group is maintained on a diet that is below maintenance (i.e., the animals lose approximately 20 percent of their body weight during anestrus). Would you expect each group to begin showing estrous cycles at the same time in the late summer/early autumn? Explain your answer.

3. Bos taurus (domestic cattle) are not seasonal breeders in the sense that cows will express regular estrous cycles throughout the year if they are provided with adequate nutrition. What would you expect the reproductive patterns of cows to be when they are maintained strictly under range conditions in temperate climates? Explain your answer.

4. When female rats with good body condition (ample fat stores) are given a drug that blocks the metabolism of glucose, they continue to show estrus and ovulate. However, if the same treatment is administered to thin females, they will fail to express estrus and ovulation. Explain these results.

REFERENCES

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De Rensis, F. and R.J. Scaramuzzi. 2003. Heat stress and seasonal effects on reproduction in the dairy cow--a review. Theriogenology 60:1139-1151.

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Keith K. Schillo, PhD

Department of Animal and Food Sciences

University of Kentucky

Lexington, Kentucky
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Author:Schillo, Keith K.
Publication:Reproductive Physiology of Mammals, From Farm to Field and Beyond
Geographic Code:1USA
Date:Jan 1, 2009
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