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Reproductive Processes

Reproductive processes

Mammalian reproduction

Reproduction is pivotal to the continuation of life. From an evolutionary standpoint, there is no single factor that has more impact on the development of species. The impetus to reproduce shapes morphology, physiology, life history, and behavior of all animals, mammals included. From the egg-laying platypus (Ornithorhynchus anatinus) to the wildebeests (genus Connochaetes) that have neonates that can run mere seconds after birth, a wide variety of strategies have evolved to successfully bear offspring in a multitude of environments.

Fundamentals of mammalian reproduction

Mammals reproduce sexually, and both sexes must unite to conceive offspring. The physical contact of both sexes does not constitute reproduction, but instead, it is the union of the sexual cells or gametes produced by each sex that constitutes the first step to reproduction. In females, the gamete is the egg or ovum. In males, the gamete is sperm. Each gamete contains one copy of each of the parental chromosomes, and thus, when the gametes unite, they form a zygote, the first complete cell of a new animal. Division of this first cell will result in the development of a full-grown animal. But before the two gametes can be united, several events must occur, all contributing to the phenomenon of mammalian reproduction. First, animals must find and choose mates. This very basic step will allow for a variety of adaptations to conquer, convince, attract, or seduce mates of the other sex. Second, mammals must get their gametes together, and this will be discussed under copulation and fertilization. Third, offspring growth and development to adulthood will be discussed under ontogeny and development. Because several aspects of development will be affected by the role of the two sexes, the importance and implications of mating systems will be discussed as well as strategies of reproduction and associated life history. Finally, some of the peculiar reproductive strategies present in mammals, and their role in the evolution and development of mammalian reproductive processes will be explored.

Mate choice

For a mammal to reproduce it must unite its gametes with the gametes of a member of the other sex. Because each gamete provides half of the genetic material of the offspring, the choice of mate has direct implications on the resulting genotype (genetic makeup) of the offspring. For this reason, animals do not mate randomly and instead choose mates. Mate choice is among the most important pressures affecting the evolution of species because failure to be able to select a "good" mate results in poor offspring quality (offspring that may be less adept to survive or reproduce), or worse yet, no offspring. Animals that fail to reproduce disappear from the gene pool, so mate choice is a critical factor.

In mammals, both sexes produce gametes of different size. Females produce relatively large eggs, and, typically, in limited number. In contrast, males produce tiny, cheap (from an energy standpoint), and extremely abundant sperm. Thus, from the outset, females adopt a "quality" strategy whereas males adopt a "quantity" strategy. This very basic difference in the size of gametes and parental investment in gamete production will trickle down and affect almost all subsequent reproductive processes. The larger initial investment of females will also result in females taking care of growing embryo(s). Production of offspring in mammals involves placental growth (monotremes and marsupials are exceptions—see below), and this is performed by females. Once born, young are nursed with milk, also produced by the mother. So although the genetic contribution of each sex in the offspring is equal, the investment of females in offspring is greater. Thus, females have more to lose from bad mating decisions. This asymmetry in investment between sexes will be reflected throughout most sexual adaptations, and will lead to females being almost invariably the most selective in mate choice.

Sexual selection and the evolution of species and their attributes

The pressures caused by females choosing males will lead to two types of evolutionary selection: inter-sexual selection (adaptations to win members of the other sex), and intra-sexual selection (adaptations to win access to mates over members of the same sex). Both vary in importance according to species and environments.

Inter-sexual selection leads to the development of adaptations, morphological, physiological, or behavioral, to seduce

mates. Typically, females are choosers, so most of the inter-sexual selection targets males. Adaptations resulting from inter-sexual selection are meant to reveal genetic quality, so males will harbor features, or perform behaviors that indicate quality. Examples of inter-sexual selection are numerous in mammals, and the best known morphological examples are probably the growth of horns in ungulates such as giraffe (Giraffa camelopardalis), or bighorn sheep (Ovis canadensis).

In contrast to inter-sexual selection, which arises from pressures imposed by the other sex, intra-sexual selection leads to adaptations as a result of pressures imposed by the same sex. Displays of strength or resources may serve to indicate dominance and establish hierarchy among males, allowing better individuals to access more mates. Best examples in the mammals are the sparring competitions of ungulates such as deer (genus Odocoileus), or the banging of heads in musk oxen (Ovibos moschatus). In these examples, some of the morphological attributes such as large antlers may be used for both inter-sexual selection (seduction of mates), intra-sexual selection (indication of dominance), and even individual selection (defense against predators). But multiple functions do not lessen their attractiveness as large antlers indicate that the males that harbor them are able to find resources to grow and carry heavy antlers, and thus indicate that they are in good health and have good genes. The extinct Irish elk possessed the largest antlers ever. They were up to 6 ft (1.8 m) in length. However, the purpose of these was not to fight. It is unlikely they could be used for this purpose as they were too big. These massive antlers seem to have evolved because of runaway sexual selection. Females prefered males with larger and larger antlers, so the antlers got bigger and bigger.

Sperm and egg formation

Sperm cells are made in the testes of males. Through a process of cellular division called meiosis, sperm-producing cells with regular genetic material (diploid cells, meaning they posses two copies of each chromosome) undergo division with the end product being two cells each with only one copy of each chromosome (haploid, half of the parent cell). Because sperm production is optimal at temperatures slightly colder than average body temperature, testes are housed in a pouch

of skin just outside the body, the scrotum. But not all species have scrotal testes year-round, and some species such as bats have testes that are kept internal for most of the year and become external prior to breeding. Other species such as aquatic cetaceans (whales and dolphins) or sirenians (dugong and manatees), as well as terrestrial armadillos, elephants, and sloths retain internal testes even during reproductive season; interestingly, sperm production readily occurs at normal body temperatures in these species.

Once formed, the sperm cells are stored in the epididymis where they remain until sperm is ejaculated. Not surprisingly, the mating system of species is often correlated with the size of testes, and many species with promiscuous mating systems will have larger testes simply because copulations are more frequent and males require more sperm, for example lions. Sperm production in humans is constant throughout reproductive life, but in seasonally breeding animals it only occurs immediately prior to the reproduction period as sperm made too far in advance degrades with age. Because millions of sperm are released with each ejaculate, the number of sperm produced by a male during a lifetime is astronomically high.

In females, the process is much different. At birth, females already possess in their ovaries all the eggs they will ever produce. Eggs are stored as follicles, and they will start developing into fully functional eggs once sexual maturity is reached. As follicles mature, they expand in size on the surface of the ovary until ovulation is triggered by release of luteinizing hormone. Peaks of this hormone occur either as part of the estrous cycle or are triggered by physical stimuli in induced ovulators such as cats (Felidae) and rabbits (lagomorphs).

Copulation and fertilization

Once eggs are released from the female ovaries, they migrate down into the uterus. Eggs are not self-propelled, and migration occurs passively by gliding over cells that have minuscule sweepers (cilia). In contrast, sperm cells each have a long flagellum that provides mobility. But for sperm to reach the egg or eggs, copulation must first occur.

Copulation in most terrestrial species occurs as the male straddles the female from behind. Typical examples of this type of copulation occur in deer, elephants, mice, and cats. Most animals remain in this position, but some, especially dogs (Canidae), may then turn 180 degrees and continue a prolonged copulation in a copulatory lock, where the penis points 180 degrees away from the head, and both animals face in the opposite direction. Another situation occurs in Cetaceans (whales and dolphins) where copulation occurs as

both animals lay or swim belly to belly. In primates, including humans, copulation positions are more flexible but most often consist of the ventral-dorsal mount or the ventralventral position.

The position assumed during copulation helps transfer the gametes from the male to the female tract, and physical constraints of size and position necessitate the use of a gamete-transfer organ, the penis. Depending on challenges faced by each species, characteristics of the penis such as size, length, or structure will vary. But all penes have the same function: to facilitate the transfer of the sperm cells from the male body to the female reproductive tract. Unlike fishes, which can release their sperm in water, mammalian sperm loses its mobility when exposed to air and internal copulation and fertilization maximizes the chances of successful transfer of viable sperm.

Both sexes have evolved adaptations to facilitate every step of reproduction, and copulation is no different. For example, females that come into heat will often produce thick vaginal secretions that not only attract males, but that also serve to lubricate the reproductive tract in preparation for copulation. Males also produce a lubricant via their bulbourethral glands to help facilitate copulation. In some species, including humans, the vaginal tract is highly acidic to serve as a barrier against diseases or microbial infections that may occur in or on the reproductive organs of males. To neutralize the acidity of the female tract that could damage or affect the motility of sperm cells, males have a prostate gland that secretes an alkali buffer to bring the pH of the female tract closer to neutral (pH = 7) so that sperm mobility and survival is optimized.

Once sperm cells reach the egg, a single sperm cell fuses with the egg cell. An enzyme then allows penetration of the genetic material of the sperm into the egg cell. Once this is done, the membrane of the egg becomes sperm proof to prevent inclusion of additional genetic material that would unbalance the process and possibly render the zygote non-viable.

Although this process seems simple, males release millions of sperm in each ejaculation so obviously not all sperm reach eggs. Sperm mobility may be affected by external conditions (such as acidity in the female tract), but also by their age, and older sperm become less mobile as they age. Strength and mobility of sperm cells is crucial, especially if females copulate with numerous males, and in these cases, sperm of multiple males may be present at the same time, forcing males to compete again for the available eggs, this time via sperm wars within the female's reproductive tract.

Sperm competition

Gametes evolved to different sizes. Females by definition are the sex that produces larger gametes. Once they've deposited their smaller gametes, males are in the advantageous position to limit energetic input (e.g., leave). The females are then left with the decision to raise offspring or not, and this decision has important energetic implications. But males also have one evolutionary uncertainty to overcome: the certainty of paternity. If males release millions of sperm and can father multiple litters within a single reproductive season (by breeding with several females), the certainty of paternity is seldom assured, and the uncertainty of paternity may well be the greatest challenge that mammalian males face when it comes to reproduction. Not surprisingly, a myriad of adaptations has evolved to overcome this uncertainty—from mate guarding and mate defense to strategies inside the reproductive tract such as sperm competition. Also, if there are fights to prevent other males from mating, these males will fight to overcome barriers put in place by previous males. One could argue that when males fight, females ultimately win because whichever male succeeds probably has better genes or the kind of genes that will enable her male progeny (i.e., son) to produce more children (i.e., increased fitness).

Mate guarding and defense following mating is a simple way for a male to reduce the odds of another male copulating with a female. However, the trade-off is obvious: staying with one mate precludes males from courting others, and strategies that allow males to protect their paternity without being present would yield great advantages. Sperm competition is one such process that can be simply summarized as any event that leads to sperm of two or more males being present at once inside the reproductive tract of a female. Males that release seminal fluids with greatest number of sperm, and sperm with the greatest mobility are thus more likely to fertilize female eggs.

Other strategies also exist for males to ensure paternity. In some species of primates such as the Senegal bush baby (Galago senegalensis) or ring-tailed lemur (Lemur catta), males have a penis that is highly spinuous, and the function of these spines is to alter the reproductive tract of the mated female so that she become less receptive to subsequent mating from other males. In carnivores such as wolverines (Gulo gulo) or American mink (Mustela vison), the penis bone may also play a role in causing enough stimulation for females to abort the first set of fertilized eggs, thus allowing males with larger penis bones to father more offspring. This also would allow females to compare male quality via the size of males' penis bones inside the reproductive tract instead of by classic displays.

In many species of rodents such as brown rats (Rattus norvegicus), primates, or bats, some of the seminal fluids will form a copulatory plug. This plug is formed soon after copulation and it appears that its main function is to prevent leakage of sperm from the female reproductive tract following

copulation. The longer the sperm stays inside the female, the better the odds of fertilization by maximizing the amount of sperm and hence number of sperm cells active in the female tract. Interestingly, the tip of the penis (the glans) is used by males to remove sperm plugs deposited by other males.

Ontogeny and development

Mammalian ontogeny and development can, from a physiological standpoint, be separated into three general strategies. First, the monotremes such as platypus and echidnas are oviparous, meaning that they conceive young via copulation, but give birth to young inside an eggshell. After a short period of development in the egg, young hatch and then suckle the mother's milk as it leaks into the fur and not through a nipple as monotremes do not have nipples.

In contrast, marsupials and placental mammals are viviparous, meaning they give birth to live young. But their respective strategies differ, especially with regards to level of development of the young at birth. Marsupials give birth to live young, but they have a short gestation and produce young that are extremely altricial, i.e., very early in their development stage. Marsupial offspring are born blind and naked, and with underdeveloped organs except for a pair of extremely well-developed and strong front limbs. The young are also minuscule in size compared to adults. They spend most of their growth phase outside of the female reproductive tract but securely attached to the maternal nipple for nourishment, often, but not always, in a pouch. Kangaroos for example give birth to tiny young which then crawl to the pouch (with the strong front limbs) and find a nipple. Attachment to the nipple ensures that the blind and naked young does not fall off the mother and always remains close to its source of nourishment.

Placental mammals constitute the largest group of mammals. In these species, which includes, cats, dogs, horses, bats, rats and humans, fertilized ova migrate to the uterus where they implant and fuse with the lining of the uterus called endometrium, which then leads to the creation of a placenta, a highly vascular membrane that acts as the exchange barrier between embryo(s) and mother. Young develop inside the female tract to varying degrees, but even the most altricial of placental mammals (polar bears Ursus maritimus, for example) still are more developed at birth than marsupials. Internal development can be extremely advanced and lead to birth of young that are able to stand and run almost immediately after birth. Wildebeests, elephants and guinea pigs all have precocial young (offspring born fully developed) in this category.

Milk and lactation

At birth, the young no longer can rely on the direct exchange of nutrients through the placenta (or in monotremes, through nutrient stored in the egg). Thus, nutrition of young requires an additional process, and milk is the nutrient that serves that purpose. Milk is unique to mammals, and all species of mammals are capable of producing milk. Milk production occurs in the mammary glands, which resemble sweat glands in form but become mature only following parturition or birth of young. The milk is delivered through nipples or teats (except in monotremes), and typically the number of teats is roughly twice the average litter size. Although males have fewer and smaller teats that are vestigial, only females produce milk and consequently they have larger teats. All rules have their exception and in mammals, there is one species in which males can also produce milk and nurse young, the Dyak fruit bat (Dyacopterus spadiceus).

Sexual maturity

Sexual maturity in many species occurs when body size reaches adult size. However, there are some notable exceptions: male least weasels (Mustela nivalis) often seek maternity dens of females and will copulate the newly born females, as soon as 4 hours after birth. At that time, neonates still have their eyes and ears closed, are pink and hairless. This strategy enables females to have a first litter within weeks of birth (least weasels do not exhibit delayed implantation), and then again before the end of their first year. Another example of early sexual maturity is in musk shrews (Suncus murinus) in which mating and repeated ejaculations from males induce puberty and ovulation in virgin females.

Mating systems

Depending on the environment, mammals will adopt various mating strategies. In some species such as beaver (genus Castor), the maintenance of a pond, lodge, and dam to maintain water level and insure security of the offspring requires the efforts of both parents, and thus both sexes must combine efforts to raise young to adulthood successfully. In such species, the sexes not only combine gametes, but also efforts and they remain together throughout the mating season, or for life. The term monogamy describes such systems, where animals remain with one mate either annually or permanently. Only 3% of mammals are monogamous but monogamy is found within nearly all mammalian orders and predominates in some families, for example in foxes, wild dogs and gibbons. Some examples of seasonal monogamy would be in red foxes (Vulpes vulpes), in which males provide parental care, but where couples break-up after rearing of young. Permanent monogamy would be best exemplified in North American beavers that mate for life (Castor canadensis). Generally speaking, monogamy occurs in species where the support from the males is instrumental to the rearing of young, and males gain more from limiting the number of offspring (by staying with one female) and investing instead in the growth of their offspring. However, many so-called monogamous males will opportunistically attempt breeding with other females, paired or not, to increase their genetic fitness, and true monogamy occurs rarely when lack of potential mates occurs, or under pressures from the environment.

Polygynous mating systems occur when males do not provide paternal care, and hence pursue matings with numerous females. Such are probably best exemplified in ungulates and pinnipeds, where males maintain access to several females simultaneously. In these harems, males try to control female breeding by asserting their dominance over other males, and if successful, winning males sire offspring from several females, whereas females only breed with a single male.

Not all females accept a single male, and in some species, both males and females will mate with numerous individuals. Promiscuity describes such a system, and is probably best exemplified in wide-ranging carnivores such as mink or wolverines. In these species, females cannot compare mates because they are spatially widely scattered, so females may mate with numerous individuals, and rely on other mechanisms to choose mates such as sperm competition. Promiscuous females also occur in certain social structures where uncertainty of paternity in males prevents them from killing the offspring of the female (infanticide). Such a social structure occurs in prides of lions (Panthera leo).

Finally, a mating system exists where male alliances may form to care for the offspring and allow females to spend most of their energy producing, and not caring for, offspring. This system, called polyandry, may occur in mammals under extremely biased sex-ratio in adulthood where males are extremely abundant, and females extremely rare, as for example with the African wild dog or the naked mole rat, with one "queen" and all else workers. This scenario is much less common but occurs in some human cultures.

Life history strategies

Just like gamete production, offspring production can follow the same two strategies: quantity or quality. The quality strategy is best exemplified in African elephants (Loxodonta africana), the largest living land animal. African elephants produce one young, rarely two, after a gestation of 22 months. Young are born precocial, and can stand up and follow the mother within 15–30 minutes. They are nursed for 2–3 years (sometimes up to 9 years), and reach sexual maturity at 8–13 years of age. In their lifetime of 55–60 years, female elephants average four calves, with a range of one to nine.

In contrast to the "quality" strategy of elephants, numerous rodents and lagomorphs have multiple litters each year, each with numerous young, and spend little time investing in

offspring growth (quantity strategy). Obviously, a continuum exists between the two extremes and typically these life history strategies are influenced by the size and life span of the animal and the environment. For example, small rodents grow faster, and live shorter lives, and thus invest in "faster" reproduction such as earlier age at maturity, and smaller but more numerous neonates. In contrast, larger mammals such as ungulates, elephants, and whales have relatively larger but fewer neonates, and attain sexual maturity much later. The latter species are typically longer-lived, and thus spread their reproductive efforts over a longer time span than smaller mammals.

Reproduction in monotremes

Three species of mammals differ completely from the more common placental animals: the short-beaked echidna (Tachyglossus aculeatus), the long-beaked echidna (Zaglossus bruijni), and the duck-billed platypus (Ornithorhynchus anatinus). Monotremes differ from placental mammals mostly because development of the offspring occurs outside of the female reproductive tract. Monotreme females conceive young via copulation, but fertilized ova then move to a cloaca (a common opening of urinary and reproductive tract) where they are coated with albumen and a shell, and eggs are laid after 12–20 days. Female echidnas carry the egg into a pouch whereas platypus lay the eggs into a nest of grass. At hatching, young echidnas remain in the pouch and subsist on the milk that drips from the fur (monotremes lack nipples). Once large enough, young are deposited in a nest where they are nursed until weaning. In contrast, female platypus lay their eggs in a grass nest inside a burrow, incubate them until hatching 10 days later, and then nurse the young in the den. Young emerge from the burrow when fully furred and approximately 12 in (30 cm) in length.

Reproduction in marsupials

In marsupials, ova are shed by both ovaries into a double-horned or bicornate uterus. The developing embryos remain in the uterus for 12–28 days, and most of the nourishment comes from an energy sac attached to the egg (yolk sac). There is no placenta (except for one groups of marsupials, the bandicoots, that have an interchange surface that resembles a true placenta). Gestation is thus short (less than one month), and much of the development of the young will occur outside of the female reproductive tract.

At birth, the offspring are extremely altricial (poorly developed). In many marsupials such as kangaroos, offspring will migrate to the nipples where they attach. This will ensure that they remain in contact with their nourishment sources, and also probably serve to secure the young and prevent them from falling off the mother at an age when they do not have the strength to hold on by themselves. In red kangaroo (Macropus rufus), the largest of all marsupials, young climb unaided to the pouch within a few minutes of birth, remain on the nipple for 70 days, protrude from the pouch at 150 days, emerge on occasion at 190 days, and permanently leave the pouch at 235 days, but is fully weaned only after a year.

Marsupials have the tiniest young in relation to adult size. In the eastern gray kangaroo (Macropus giganteus), young at birth weigh less than 0.0001% of the female mass. Put into context, this would be similar to a 150 lb (68 kg) human female giving birth to individual babies that would each weigh 0.0048 lbs (22 g), or 0.08 oz. But extreme altriciality is not a disadvantage in evolutionary terms. In fact, many scientists believe that this is instead a great advantage as the small investment in each neonate allows females to minimize investment in young and be more flexible and responsive to environmental conditions. Mechanistically, if environmental conditions become too tough to raise young successfully, starvation would terminate the production of milk and lead to rapid death of young, thereby saving energy lost (versus placental mammals that have a greater energy investment). This would give marsupial females a competitive advantage over animals with internal pregnancy (placental mammals) in unpredictable environments.

Some marsupials such as the eastern gray kangaroo also display other reproductive oddities. Pregnancy following copulation does not affect the cycle and the female can become pregnant again as her first young (litter size usually is one) move to the pouch. The second fertilized egg undergoes diapause (halt in development) until the first young either reaches adulthood or dies. In this case, the diapause is facultative or changes length depending on circumstances such as food availability or season. Then, the second egg immediately resumes development so that birth occurs as soon as the mother's pouch is available. So at any one time, the female can have three young: one in the placenta, one in the pouch, and one joey out of the pouch and still suckling.

Placental mammals

Placental mammals constitute the largest group of mammals. In placental mammals, fertilized eggs migrate to the uterus or to the uterine horns where they implant and begin to develop. In the process, a placenta is grown to act as the interface between mother and offspring. The highly vascular placenta then connects to growing embryos via the umbilical cord, and exchanges of nutrients and waste between mother and fetus occur in the placenta as fluids are not shared between mother and fetus in the womb.

Not all placental mammals have the same reproduction scheme. Most females have estrous cycles with well-defined "heat" periods and will only accept mates and breed during this period. The estrous period often is fairly conspicuous and recognized by mates through hormonal, pheromonal, or behavioral cues. Most mammals fit in this category, and best known examples may include deer, dogs, and otters.

Primates are recognized by many as the most advanced mammals, possibly because of advanced cognitive skills and a larger brain relative to body size. Many primates including humans do not have an estrous cycle, but instead a menstrual cycle. The menstrual cycle typically leads to more frequent ovulation (every 28 days on average in humans) and considerable bleeding associated with breakdown of the endometrial lining in the uterus (menstruations). Moreover, females of advanced primate species including humans do not show clear sign of ovulation and in many females, ovulation fits into a process called the menstrual cycle. In this cycle, the uterus is prepared prior to ovulation, the egg or eggs are released several days later, and if fertilization does not occur, the lining of the uterus degenerates and is shed during a period called the menstruations. The combination of regular but hidden ovulation in females probably allow primates to evolve promiscuous mating systems because males cannot assess when ovulation occurs, and thus mate guarding either occurs throughout the year (monogamy in many human societies), or uncertainty of paternity leads to child care in large promiscuous groups (chimpanzees) and lessens the risk of infanticide.

Peculiar mechanisms: Induced ovulation

Induced ovulation occurs when release of eggs in females is triggered by a stimulus, most often physical such as copulation, but also behavioral or pheromonal such as the vicinity of males. In contrast to spontaneous ovulators, or species where the release of eggs depends on the seasonal photoperiod

signal, species with induced ovulation develop ova that are ready for release but require a stimulus for release.

Induced ovulation occurs in many species, but is best understood in mammalian carnivores. Examples of species with induced ovulation include cats (Felidae), bears (Ursidae), and numerous Mustelidae such as wolverine (Gulo gulo), striped skunk (Mephitis mephitis), and North American river otter (Lontra canadensis). For species with induced ovulation, it appears that a certain level of stimulation is required for eggs to be released, and thus it has been hypothesized that females may use the ability of a male to induce her ovulation as an indicator of male vigor, hence male quality. In these species, females may not be able to compare males simultaneously and because of the severity of the environment, may not be sure of her ability to find mates. In this case, the best strategy for the females would be to mate with all males encountered, and bear offspring from the male that induces the greatest stimulus. Evidence in black bears (Ursus americanus) of multiple paternity within single litters suggests that induced ovulation may be used by females as a mate choice strategy within the reproductive tract. For males, inducing ovulation may be a method of ascertaining paternity when pair bonds must be short to allow for encounters with other females. It is also possible that induced ovulation evolved as a strategy against sexual coercion in carnivores. In this case, females forced into copulation by males of lesser quality could abort eggs if they subsequently bred with a better quality male that provided a greater stimulus. Although the complexity of induced ovulation is still being investigated, it appears that benefits may exist for both males and females of species living in highly seasonal environments.

Peculiar processes: Delayed fertilization and delayed implantation

The opportunity to find a suitable mate is essential for reproduction, but because gestation is fixed in duration, timing of mating has direct implications on the timing of parturition. However, mammals have evolved two strategies to separate

in time mating and parturition: delayed fertilization and delayed implantation.

Delayed fertilization

Sperm storage occurs in bats inhabiting northern temperate regions such as the little brown bat (Myotis lucifugus), and also in many bats such as noctule (Nyctalus noctula). In the little brown bat, the testes become scrotal in the spring, and most sperm production is completed by September. The sperm are then stored until copulation commences months later. Females are inseminated in the fall and winter, while they are in hibernation. Sperm are then stored again, this time in the female reproductive tract, the uterus, where they remain motile for almost 200 days in the noctule. Females ovulate much later, and active development of the embryos starts in the spring. For bats, delayed fertilization allows males to copulate when they are in best condition in the fall, and parturition to occur just prior to emergence of insects. Because of the energy required for copulation, mating in the spring would be at the time of worst male condition. Delayed fertilization also allows females to give birth immediately after spring arrives, thus allowing more time for offspring growth before the next hibernation period. Thus, delayed fertilization is especially advantageous for species with long periods of dormancy, and allows females to compare breeding males via sperm competition.

Delayed implantation

Delayed implantation is a peculiar reproductive process in which fertilized eggs come to a halt in their development, usually at the blastocyst stage. After a period of time that varies among species and that is somewhat flexible, the blastocysts implant on the uterine wall and start developing for a duration called "true gestation." Delayed implantation occurs in marsupials, rodents, roe deer, and bats, but probably is best known in carnivores. In the Carnivora, not all species exhibit delayed implantation, but the best examples probably are in the Mustelidae, Ursidae, and pinnipeds (Odobenidae, Phocidae, Otariidae). Examples of species that have delayed implantation include American marten (Martes americana), wolverine (Gulo gulo), black bear (Ursus americanus), giant panda (Ailuropoda melanoleuca), and northern fur seal (Callorhinus ursinus). In bears, mating occurs after den emergence in the spring, but birth of offspring does not occur until late winter of next year, a full 9-10 months later. Delayed implantation likely evolved to uncouple the tight relationship between mating and birth, and because it is most prevalent in northern species, would provide an advantage to allow parturition at the time of greatest food availability and possibly mating to occur at the time of greatest mate availability. Possibly, mating systems may influence delayed implantation and at least two species in North America show variable delay, the American mink (Mustela vison) and the striped skunk (Mephitis mephitis), where the delay varies from 0–14 days. In the pinnipeds, delayed implantation would allow females to mate when conditions are favorable to maximize male competition and availability, thus allowing females to breed at a time when seals are aggregated, thus facilitating mate choice.

Peculiar mechanisms: Inbreeding avoidance

Inbreeding is a word that describes breeding of one individual to another that is related, and in most animals, mammals included, is relatively rare. This is likely so because breeding with relatives has deleterious effects on the survival of the offspring, and often leads to reduced fertility. In evolution, inbreeding is rapidly selected against. Not surprisingly then, animals go to great lengths to avoid breeding with animals to whom they are related. To accomplish this, animals must be able to either recognize relatives (kin recognition) or, as an alternate strategy, recognize situations that could lead to breeding with relatives.

Kin recognition has been demonstrated in numerous mammals, and is probably most developed in humans. The alternate scenario of recognizing situations that lead to breeding with relatives is thought to explain sex differences in dispersal. In mammals, dispersal from natal areas is most common in males whereas females tend to stay closer to the home range or territory of their mother. Although several explanations for dispersal have been proposed, at the top of the list is that dispersal may reduce possibility of inbreeding. This would be most common in polygamous species where males copulate with numerous females. In this scenario, many of the resident females present during the next breeding season would be related to the males, and hence, males often disperse after a successful breeding season.

Peculiar mechanism: Reproduction in armadillos

Armadillos are placental mammals (Order Xenarthra) that occupy the southern United States, Central America, and the northeastern half of South America. They differ from other placental mammals in numerous ways. The uterus is simplex, just like that of humans, but there is no vagina and instead, a urogenital sinus serves as vagina and urethra. Males have internal testes and no scrotum, and have among the longer penes of mammals, reaching one third the length of the body in nine-banded armadillos (Dasypus novemcinctus). The oddities are not limited to morphology, but include the physiology as well.

Nine-banded armadillos have unusual delayed implantation. Armadillos breed in June, July or August, and the only fertilized egg becomes a blastocyst after 5-7 days at which point it enters the uterus. Development then ceases and the blastocyst remains free-floating in the uterus until November or December when it implants, and then the zygote divides twice to form four identical embryos. After 5 months of gestation, four identical quadruplets are born usually in May. Although identical twins are known to occur in humans, nine-banded armadillos regularly have identical offspring, most often four of them. But the mystery does not end there: a captive female held in solitary confinement gave birth to a litter of four females 24 months after her capture, or 32 months after she could have mated in the wild! Although the mechanism is not clearly understood, either her implantation delay lasted 23-24 months, or this particular female had produced two eggs, one of which would have remained dormant for at least 15 months.

Peculiar morphology: The mammalian penis bone

A peculiar bony structure exists in the penis of many mammalian species, and this bone, often referred to as baculum or os penis, is probably one of the most puzzling and least understood bones of the mammalian skeleton. Present in a variety of orders including Insectivora, Chiroptera, Primates, Rodentia, and Carnivora, this bone does not occur in all Orders in the Mammalia, but also does not occur in all species within each Order. Within a species the bone also varies in size, with older individuals typically possessing longer penis bones. In the mammals, the largest penis bone in absolute and relative size occurs in the walrus (Odobenus rosmarus), where the baculum may reach up to 22 in (54 cm) in length. In contrast, the bone is mostly vestigial in rodents such as North American beavers (Castor canadensis), and very small in all felids (cats), which have spines on the penis.

There are obvious costs to possessing a penis bone as evidenced from accounts of penis bone fractures. Historical hypotheses suggested that the bone may provide additional support to the penis for copulation, may protect the urethra from collapsing and blocking sperm passage in species that copulate for long periods, or else may help stimulate females into ovulation. However, all hypotheses have weaknesses and the most current hypothesis explaining the evolution of the mammalian penis bone in carnivores suggest that the largest penis bone evolved in species with promiscuous mating systems as a way for females to assess male quality during copulation. However, explanations may not be exclusive and possibly other functions may exist in other taxa. Undoubtedly, the full significance of this bone into the evolution of mammals has not yet been fully understood and remains an enigmatic puzzle to solve for mammalian scientists.


Resources

Books

Adams, C. E., ed. Mammalian Egg Transfer. Boca Raton: CRC Press, 1982.

Asdell, S. A. Patterns of Mammalian Reproduction. 2nd ed. Ithaca, NY: Cornell University Press, 1964.

Eberhard, W. G. Sexual Selection and Animal Genitalia. Cambridge, MA: Harvard University Press, 1985.

Kosco, M. Mammalian Reproduction. Eglin, PA: Allegheny Press, 2000.

Tomasi, T. E. Mammalian Energetics: Interdisciplinary Views of Metabolism and Reproduction. Ithaca, NY: Comstock Publishing Association, 1996.

Zaneveld, L. J. D., and R. T. Chatterton. Biochemistry of Mammalian Reproduction. New York: John Wiley & Sons, 1982.

Periodicals

Ferguson, S. H., J. A. Virgl, and S. Lariviére. "Evolution of delayed implantation and associated grade shifts in life history traits of North American carnivores." Écoscience 3 (1996): 7–17.

Jaffe, K. "The dynamics of the evolution of sex: Why the sexes are, in fact, always two?" Intersciencia 21 (1996): 259–267.

Jia, Z., E. Duan, Z. Jiang, and Z. Wang. "Copulatory plugs in masked palm civets: Prevention of semen leakage, sperm storage, or chastity enhancement?" Journal of Mammalogy 83 (2002): 1035–1038.

Kenagy, G. J., and S. C. Trombulak. "Size and function of mammalian testes in relation to body size." Journal of Mammalogy 67 (1986): 1–22.

Larivière, S., and S. H. Ferguson. "On the evolution of the mammalian baculum: Vaginal friction, prolonged intromission or induced ovulation?" Mammal Review 32 (2002): 283–294.

Larivière, S., and S. H. Ferguson. "The evolution of induced ovulation in North American carnivores." Journal of Mammalogy 84 (2003): in press.

Laursen, L., and M. Bekoff. "Loxodonta africana." Mammalian Species 92 (1978): 1–8.

McBee, K., and R. J. Baker. "Dasypus novemcinctus." Mammalian Species 162 (1982): 1–9.

Miller, E. H., and L. E. Burton. "It's all relative: Allometry and variation in the baculum (os penis) of the harp seal, Pagophilus groenlandicus (Carnivora: Phocidae)." Biological Journal of the Linnean Society 72 (2001): 345–355.

Miller, E. H., A. Ponce de León, and R. L. DeLong. "Violent interspecific sexual behavior by male sea lions (Otariidae): Evolutionary and phylogenetic implications." Marine Mammal Science 12 (1996): 468–476.

Moller, A. P. "Ejaculate quality, testes size and sperm production in mammals." Functional Ecology 3 (1989): 91–96.

Pasitschniak-Arts, M., and L. Marinelli. "Ornithorhynchus anatinus." Mammalian Species 585 (1998): 1–9.

Patterson, B. D., and C. S. Thaeler Jr. "The mammalian baculum: Hypotheses on the nature of bacular variability." Journal of Mammalogy 63 (1982): 1–15.

Poole, W. E. "Macropus giganteus." Mammalian Species 187 (1982): 1–8.

Rissman, E. F. "Mating induces puberty in the female musk shrew." Biology of Reproduction 47 (1992): 473–477.

Sharman, G. B. "Reproductive physiology of marsupials." Science 167 (1970): 1221–1228.

Sharman, G. B., and P. E. Pilton. "The life history and reproduction of the red kangaroo (Megaleia rufa)." Proceedings of the Zoological Society of London 142 (1964): 29–48.

Stockley, P. "Sperm competition risk and male genital anatomy: Comparative evidence for reduced duration of female sexual receptivity in primates with penile spines." Evolutionary Ecology 16 (2002): 123–137.

Storrs, E. E., H. P. Burchfield, and R. J. W. Rees. "Superdelayed parturition in armadillos: A new mammalian survival strategy." Leprosy Review 59 (1988): 11–15.

Serge Larivière, PhD

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