Chapter 2: Life, reproduction, and sex.
* Define sex.
* Describe asexual and sexual reproduction.
* Review mitosis and meiosis.
* Discuss why sexual reproduction occurs.
* Characterize the major reproductive strategies of mammals.
Amoebas at the start Were not complex; They tore themselves apart And started Sex.
WHAT IS SEX?
This first stanza from the poem "Sex," by Arthur Guiterman (1871-1943) raises some important fundamental questions about reproduction. Guiterman is describing a common type of reproduction--cell division. But is this sex? There can be much confusion regarding the meaning of sex and how it is related to reproduction. This is because we use the word in several different ways. Sex and reproduction seem to be linked, but when people speak of having sex, they are not necessarily referring to engaging in a reproductive activity. We also identify individual humans according to their sex (male or female), but are we always making reference to their roles in the reproductive process? This seems unlikely. For example, when we identify a human as male or female, we frequently rely on characteristics (hair style, type of clothing, and so on) that reflect social norms, not biological traits such as type of genitalia. What exactly do we mean when we speak of sex? Before we can engage in a study of reproductive physiology, it is important to clear up any confusion regarding sex and reproduction.
As noted in the first chapter, reproduction can be defined as a means by which an organism replicates itself. There are two major modes of reproducing; sexual and asexual (meaning without sex). One way to develop a deeper understanding of these terms is to explore how sex is related to reproduction. Specifically, we will consider whether sex is a necessary and/or sufficient condition for reproduction. A necessary condition means that something (e.g., sex) is a prerequisite for something else (e.g., reproduction). A sufficient condition means that something is all that is required for something else. We will establish such relationships between sex and reproduction as we examine various definitions of sex.
There are several ways of conceptualizing sex. In the broadest, biological sense of the term, sex is the process whereby a new individual arises from the recombination of genes from separate sources. Using this definition, it is possible to identify three different types of sex (Figure 2-1). The first is transgenic sex (also known as conjugation) practiced by bacteria. Bacteria frequently receive genes from other bacteria or viruses. For example, the multicellular bacterium, Streptomyces griseus, can receive genes from Escherichia coli, a vastly different single-celled bacterium.
[FIGURE 2-1 OMITTED]
The second type of sex is hypersex, characteristic of the protoctists; microorganisms that comprise one of the five kingdoms of living organisms (i.e., protoctista; plantae, animalia, fungi, and bacteria). The amebas, to which Guiterman refers, are members of this kingdom. Hypersex occurs when different organisms merge and develop a permanent symbiotic relationship. You are undoubtedly acquainted with at least one example of this phenomenon. The familiar mitochondria, oxygen metabolizing organelles found in almost all eukaryotic cells, were once bacteria that merged with anaerobic bacteria (those that can not metabolize oxygen) to create aerobic organisms that can metabolize oxygen.
The third type of sex is perhaps the one with which you are most familiar; meiotic sex. This is the type of sex practiced by animals, fungi, and plants, and involves specialized sex cells (gametes) that possess only half the number of chromosomes as other body cells (somatic cells). Gametes are produced via meiosis, a type of cell division that reduces the number of chromosomes in a cell (also known as reduction division). During meiotic sex, two different types of gametes, each with a haploid (half the full complement) number of chromosomes, undergo syngamy (fusion to form one cell) to form a zygote, with the diploid (full complement) number of chromosomes.
The important lesson from this brief survey of sex is that in the community of living organisms, sex is not necessary for reproduction. Only in the case of meiotic sex is sex a necessary condition for reproduction. Although bacteria can exchange genetic material and unicellular protoctists can merge to form larger cells, in neither of these cases is the exchange of genes necessary for reproduction to occur. Bacteria reproduce via a process known as binary fission; that is, simple cell division. Unicellular protoctists will fuse with each other, but they can also reproduce by dividing. This discussion illustrates a second way of defining sex; that is, as a mode of reproduction. In sexual reproduction, production of new individuals requires the recombination genes from two parents. The other major approach to reproducing is asexual reproduction. Organisms that reproduce asexually do so by mitosis or cell division; that is, one individual cell divides into two identical copies.
The close association between sex and reproduction has significant implications for organisms that rely solely on this mode of reproduction. One of the most important is that in order to engage in sexual reproduction, individuals must have the ability to recognize members of their own species as well as members of the so-called opposite sex. This requirement permeates almost every aspect of animal life. The anatomic, behavioral, and physiologic differences between males and females of a particular species serve the purpose of ensuring that the two types of gametes (spermatozoa and oocyte) encounter each other and merge. Thus, in the case of sexual reproduction, sex can also refer to the reproductive role (i.e., providing male or female gametes) of an individual. In this sense of the term, to say that someone is male or female is analogous to saying that the individual is a scientist, or actor; that is, to make reference to something that individual does in a particular context.
There is a tendency for humans to over-extrapolate the aforementioned implications of sexual reproduction. Although it is true that humans reproduce sexually (recombination of genes via fusion of gametes), it is also well-known that humans frequently practice sex (assume reproductive roles) but without reproducing. Unless the individuals practicing sex are fertile (i.e., have the ability to conceive), reproduction will not occur. Infertility (temporary inability to reproduce) can occur spontaneously (e.g., due to disease) or can be induced intentionally (e.g., use of birth control). For centuries, humans have practiced various means of birth control in order to sever the link between having sex and reproducing. The implication of this discussion is that sex can be thought of in yet another way; that is, as one's sexuality. Sexuality refers to practices in which a person engages to achieve sexual gratification, not necessarily for the purpose of reproducing. There are a variety of practices that we label as sex that have little, if anything, to do with reproduction; for example, oral sex, anal sex, cyber sex, phone sex, and so on. In these cases, the sexual practices of individuals do not coincide with their reproductive roles in meiotic sex. Whether or not they should coincide is an ethical matter that has been the subject to considerable debate for centuries.
In light of the previous discussion, we can conclude that among all species sex is not a necessary condition for reproduction. Many organisms reproduce without sex (asexual reproduction), and some of them engage in sex without reproducing. In sexually reproducing species, sex is usually a prerequisite for reproduction. However, recent success with cloning in some animals raises the possibility that sex is not a necessary condition for reproduction even in sexually reproducing species. Is sex a sufficient condition for reproduction? Clearly not in species that reproduce asexually. In sexually reproducing species, sex is a sufficient condition for producing a zygote. However, reproduction also depends on that zygote developing into an individual that can reproduce. In mammals, a male and female might produce gametes, mate, and produce a zygote, but reproduction can still fail due to a variety of reasons, including embryonic and neonatal death (either spontaneous or induced).
In summary, sex has several different meanings. With respect to mammalian reproduction, the subject of this book, we will use the term to make reference to a mode of reproduction that requires the recombination of genes via fusion of gametes. With respect to individuals engaging in sexual reproduction we will use the terms male and female to refer to their roles in this reproductive process.
MITOSIS AND MEIOSIS
The hallmark of sexual reproduction is the production of gametes (game-to-genesis) via meiosis. However, the production of sperm cells and oocytes also involves mitosis. Early in development, a series of mitotic divisions produces an abundance of diploid cells that are the precursors of cells that eventually undergo meiosis to form gametes. In somatic tissues, mitosis contributes to growth by increasing cell numbers. You should become familiar with the details of mitosis and meiosis because these cellular mechanisms are of fundamental importance in reproductive physiology. Discussions of spermatogenesis (production of spermatozoa) and oogenesis (production of oocytes) in later chapters are based on the assumption that you understand these processes.
Figure 2-2 illustrates the process of mitosis in a cell from an organism for which the diploid number of chromosomes is four. As you may recall from elementary biology, chromosomes exist in homologous pairs. Thus in this case, the organism has two homologous pairs of chromosomes. In mitosis, one parent cell will divide and give rise to two identical offspring cells (also known as daughter cells). Our example begins with the interphase portion of a cell cycle; that is, the phase when the cell is not dividing. Interphase chromosomes are decondensed; that is, long and thin. By the end of this phase, chromosomes begin to contract and condense; that is, shorten and thicken. In addition, the chromosomes replicate such that each chromosome consists of two identical chromatids joined at the centromere. During early mitotic prophase, the centrioles begin to migrate laterally and the nuclear membrane begins to break down. By late prophase, the spindle forms; that is, a network of microtubules along which chromosomes migrate. At this time, the chromosomes migrate towards the equatorial region of the cell. Metaphase is the time when the centrioles are located at opposite ends of the cell, joined by the spindle. The distinguishing feature of metaphase is the alignment of chromosomes along the equator of the cell. During anaphase, the centromere of each chromosome splits and each chromatid migrates to opposite poles of the spindle. Finally, during telophase, the spindle degrades, chromosomes decondense, two nuclear membranes form around each set of chromosomes, and cytokinesis (division of the cytoplasm) occurs, resulting in two identical offspring cells.
[FIGURE 2-2 OMITTED]
Meiosis (Figure 2-3) differs from mitosis in three important ways. First, one parent cell gives rise to four offspring cells (gametes). Second, each of the offspring cells has only half the number of chromosomes as the parent cell; that is, a haploid number of chromosomes. Third, there are two cell divisions involved in meiosis.
As with mitosis, meiotic interphase is the stage preceding division. By the end of this phase chromosomes have condensed and have replicated to form chromatids and centromeres. Meiotic prophase is much longer than mitotic prophase, and can be divided into four steps. During the leptotene stage, chromosomes begin to thicken. By the time of the zygotene stage the chromosomes are fully condensed and the homologous pairs begin to line up parallel to each other. Throughout early prophase, the centrioles migrate laterally and eventually occupy opposite sides of the cell. During the third, or pachytene, stage of meiotic prophase, chromosomes are shortened and thickened and lie in pairs. By the time the cell enters the diplotene/diakinesis stage the chromosomes shorten further and microtubules begin to radiate from the centrioles. During this later part of prophase, homologous pairs of chromosomes are tightly linked and their chromatids overlap. The point at which this crossing over occurs is known as the chiasmata. This permits the exchange of pieces of chromatids between homologous pairs of chromosomes. Meiotic metaphase 1 is characterized by the disappearance of the nuclear membrane, a well-defined spindle, and homologous pairs of chromosomes aligned at the equatorial region of the cell. During anaphase 1, homologous chromosomes move in opposite directions along the spindle. By late telophase 1, nuclear membranes have formed and cytokinesis is complete, yielding two offspring cells, each containing one member of each homologous pair of chromosomes. During the remaining stages of meiosis, the offspring cells undergo another division similar to mitosis. Each chromosome, with its chromatids, moves to the cell equator along the spindle during metaphase 2. During anaphase 2, the chromosomes separate and each half migrates to opposite ends of the cell. In telophase 2, a second division is completed giving rise to two gametes; that is, cells with half as many chromosomes as the original parent cell.
[FIGURE 2-3 OMITTED]
One of the most important features of meiosis is the fact that each of the four gametes arising from the parent cell is genetically unique. This is due to the random segregation of homologous chromosomes and chromatid exchange among homologues during the first meiotic prophase. This feature of meiosis enhances genetic variation among offspring. As discussed in the next section, genetic variation is important in evolution. A species with greater genetic variation is more likely to adapt to environmental changes, and therefore is more likely to survive than a species with less variation.
WHY SEXUAL REPRODUCTION?
One can't help but marvel at the intricate mechanisms governing sexual reproduction. Research aimed at understanding how these mechanisms work has been compared to peeling an onion. Once one level of understanding is achieved there is a deeper layer waiting to be peeled back. Whether you are a student beginning your study of this subject, or an experienced scientist seeking to understand molecular mechanisms regulating fertility, a daunting question will linger in the back of your mind. Why is there sexual reproduction in the first place? As noted in the first chapter, this is an ultimate question requiring an answer based largely on theory. You might think it's a waste of time to theorize about such things, but before you reject this type of inquiry, consider what cartoonist and author James Thurber once wrote; "Sometimes it is better to know some of the questions than all of the answers." Science is all about knowing which questions to ask. In fact, scientists are reluctant to say that they actually know the answer to a scientific question. The best they can do is to provide a hypothesis, which can be thought of as a tentative answer to a question. Much can be learned from questioning and developing theoretical answers. Asking why there is sexual reproduction provides the opportunity for us to put our best scientific theories to use. If such theories provide a satisfactory explanation, then we enhance our understanding of the world we live in. Such understanding can help us live more skillfully--at least until a better explanation comes along!
We will address why sexual reproduction exists in two steps. First, we will consider why reproduction can exist in the world. Second, we will consider why sexual reproduction exists, and why it is maintained.
Reproduction, Life, and Thermodynamics
What is the most fundamental trait of all living beings? Any organism that we consider to be alive has the ability to maintain itself in the presence of a continually changing environment. Biologist Lynn Margulis calls this property is autopoiesis, meaning self-maintenance. An autopoietic entity is self-bounded (has a membrane or skin), self-generating (the boundary is produced by the entity), and self-perpetuating (they use energy continuously to maintain themselves, even when they are not growing or reproducing). A more familiar way of understanding autopoeisis is to say that each living being is determined by its own metabolism; that is, its own internal set of biochemical processes that provide energy for vital processes and activities. Reproduction is one vital process supported by metabolism. When an organism fails to shunt energy to the biochemical reactions supporting reproductive activity, it fails to reproduce.
Autopoietic entities are open, thermodynamic systems. In other words, they are systems through which energy flows. Some of the energy is captured to run life-sustaining processes, and the rest is lost as heat and wastes (urinary, fecal, and gaseous). Living beings capture energy in different ways. Plants and other photosynthetic organisms capture solar energy in the form of various hydrocarbons (carbohydrates, lipids, and proteins), which they store and use to fuel their metabolic processes. Animals capture energy from plants, either directly by consuming the plants (herbivorous animals), or indirectly by consuming other animals that consume plants (carnivorous animals), or both (omnivorous animals). Figure 2-4 shows the energy flow through a cow, which is an herbivore. Energy from plants is consumed, digested, absorbed, and transported to various tissues where it is metabolized or stored for later use. In mammals, much of this dietary energy is used for basal metabolism, voluntary movements, thermoregulation, lactation, growth, and, of course, reproduction. This scheme illuminates the important relationship between reproduction and energy metabolism. When there isn't enough dietary energy to fuel all of these vital processes some processes, cease. As it turns out, reproduction is among the lowest priorities; that is, it is usually the first process to be eliminated during times of restricted energy intake.
The aforementioned scheme outlining the partitioning of energy in living beings illustrates one of the most important fundamental laws of physics; the so-called second law of thermodynamics. In any system, whether it is an inanimate object such as a television or an autopoietic entity such as a cow, a portion of the energy consumed by the system will be lost as entropy. Entropy is the energy that is not available to the system to power its work. Not all the electrical energy flowing into your television is used to provide pictures and sound. A good portion of that energy can't be used and is given off as heat. The same is true for living beings. Using our cow as an example, the energy dissipated in the form of heat and various wastes is not available to the animal. Another way of looking at this phenomenon is to consider how the different forms of energy behave. The energy of the plants that serve as the cow's feed, is potential energy; energy based on a particular chemical structure of hydrocarbon nutrients. When the cow metabolizes these chemicals, energy is liberated (kinetic energy). Some of it is used to power various biochemical pathways, whereas the rest is distributed among molecules that make up waste products. Wastes represent kinetic energy that is too randomly distributed to be of use to the animal. From a purely energetic perspective, the cow (or any living being) is a system that facilitates the movement of energy from a highly ordered state to a more random state. This insight provides the basis for an explanation of why reproduction can exist in the first place.
[FIGURE 2-4 OMITTED]
As noted earlier, living beings are open systems; they are open to incoming energy. However, they are all part of a very large closed system known as the universe. According to thermodynamic theory, the total amount of energy in a closed system remains constant, but energy can exist in different forms (potential and kinetic). When an energy gradient exists within a closed system (i.e., when energy is distributed between potential and kinetic forms) the system moves toward a state of equilibrium, which is the most disordered or most homogeneous state. This explains why heat flows from a warm body to a cool one, or why molecules diffuse from a high concentration to a lower one. At equilibrium both bodies become the same intermediate temperature or the two solutions end up with the same intermediate concentration. Astronomers believe that our universe is moving towards a state of equilibrium; that is, the highly ordered potential energy of the stars, including our sun, is slowly being converted to disordered (kinetic) energy. Life on earth contributes to this process; that is, living beings capture the potential energy of the sun and dissipate it to various forms of kinetic energy. Reproduction is one of the life sustaining processes that plays a role in this process. Therefore, one can say that life (and reproduction) exists because of energy gradients in the universe. Life is only one of countless mechanisms that help move the universe to a state of equilibrium.
BOX 2-1 Focus on Fertility: Entropy and Human Lifestyles The entropy law of thermodynamics is fundamentally important, yet most of us are either unaware of it, or ignore it in our day-to-day activities. Nevertheless, the implications of this law are of practical significance and influence all aspects of our lives. Living beings metabolize dietary energy to support various vital processes. Because this process isn't 100 percent efficient, metabolism produces various wastes which are forms of entropy. With the exception of humans, all living beings rely solely on solar energy, either directly (photosynthetic organisms) or indirectly (organisms that consume photosynthetic organisms or organisms that consume organisms that consume photosynthetic organisms). Humans, on the other hand, employ other fuels to produce, process, and distribute their foods. This means that humans generate considerably more entropy than other life forms, especially humans who live in industrialized societies. Jeremy Rifkin illustrates this by analyzing the entropy associated with procuring the loaf of bread you routinely purchase from your nearest grocery store. The following energy-requiring steps are required to make this bread available to the consumer: 1) wheat is planted, cultivated, and harvested; 2) wheat is transported by trucks to a bakery plant; 3) wheat is processed (refined and bleached) into flour; 4) flour is enriched with vitamins and minerals; 5) preservatives and dough conditioners are added to the flour; 6) dough is formed into loaves and baked; 7) bread loaves are packaged in plastic wrappers and boxed; 8) loaves are trucked to grocery stores; 9) bread is housed in climate-controlled grocery stores until purchased; 10) consumer transports bread (via automobile) to her home; and 11) bread is consumed. Each of these steps requires energy and generates entropy; that is, waste. The energy costs of human reproduction in an industrialized world can also be quite high. Finding a mate and establishing a family typically requires energy expenditures for transportation, clothing, entertainment, and so on. Couples with fertility problems may expend even more energy by using assisted reproductive technologies (artificial insemination, in vitro fertilization, embryo transfer, and so on). Other aspects of human life are no less complicated. Consider the energy-dependent steps involved with going to work, taking a vacation, watching a movie or downloading music to your MP3 player. When we examine our lives from a thermodynamic perspective, it becomes clear that we humans consume an astounding amount of energy and generate staggering amounts of entropy in the form of solid wastes, greenhouse gases, and chemical pollutants.
Why Sexual Reproduction?
This question can be broken down to two parts. First, why did sexual reproduction occur in the first place? Second, why is sexual reproduction maintained? These questions arise from the so-called paradox of sex; that is, sex is widespread, but seems too costly to be beneficial to an organism. The costs associated with this type of reproduction seem to be considerably higher than those for asexual reproduction and include: 1) costs associated with mating or conjugation, 2) costs associated with producing offspring, and 3) costs associated with the risk of producing offspring via randomly mixing genes from two individuals. If this is indeed true, then why do so many species practice sexual reproduction? Why didn't asexual organisms out-compete the sexual organisms?
With respect to the cost of mating, considerable time and energy are required to find and secure mates. In some sexually reproducing species, mate selection involves investment of energy in particular body shapes, coloration schemes, behavioral displays, and so on. Moreover, searching for and mating with a partner makes sexual reproduction much slower than asexual reproduction. The costs associated with producing offspring stem from the fact that the reproductive unit in sexual reproduction is the mating couple. In asexual reproduction, one individual can give rise to two individuals, whereas in sexual reproduction two individuals are required to produce one individual. Thus the net reproductive rates for the two types of reproduction are 1 and 0.5, respectively. In order for a sexually reproducing pair to achieve the same reproductive rate as an asexually reproducing individual, they have to invest in producing twice as many offspring. Finally, there are risks associated with mixing genes from different individuals. In general, recombination of genes destroys advantageous gene combinations faster than it creates new ones.
With these costs in mind, it is difficult to understand how sexual reproduction can exist in so many species. It may be easier to explain why sex arose in the first place than to explain why it persisted, so let's take on the simpler question first. One sound explanation is that sex originated as a nonlethal infection in bacteria. The genes that allow a bacterium to be copied and transferred to other individuals might have spread throughout a population because the rate of infection by these genes was much faster than the onset of any lethal or fitness-reducing consequences. Although this may explain how sex got its start, it doesn't explain why sex persisted as a mode of reproduction.
Many biologists argue that sexual reproduction should have disappeared soon after its appearance. They assert that asexually reproducing species would have out-competed sexually reproducing species, due to the high costs of sexual reproduction, unless sexual reproduction offered some other advantages the outweighed these costs. The conventional explanation for why sexual reproduction is maintained is that it increases variation in offspring, and that this variation allows sexual organisms to adapt to lethal environmental changes faster than asexual organisms. Although this is a standard textbook explanation, there are serious problems with this idea. First, sex doesn't necessarily increase genetic variation in a species. Second, natural selection need not promote genetic variation. Third, evolution need not favor increased genetic exchange. It is beyond the scope of this book to explore these criticisms in any detail. However, the basis of these criticisms can be summarized in the following manner. Sexual reproduction is only one of many mechanisms whereby genetic variations can arise. Mutations, symbiogenesis, and various forms of stress also generate variations, both in sexual and asexual organisms. Any attempt to make generalizations regarding the relative benefits of sexual reproduction is complicated by the fact that the type of reproduction expressed by a particular species is determined by the specific context in which it evolved; that is, its natural history. As noted in a previous section, organisms have engaged in different types of sex for billions of years, irrespective of how they reproduce. Sexual reproduction may not be as much a trait that has been directly selected for as much as it is an evolutionary path by which sexually-reproducing organisms came to be. This mode of reproduction may very well have been an improvisational aspect of evolution as suggested by reproductive physiologist Irving Rothchild. In other words, sex may not have provided any advantage to early organisms who practiced it (e.g., bacteria), but descendents made use of it in different types of environments. In other words, sex may not have been advantageous until environmental conditions made it so. What this means is that an understanding of why a certain species reproduces the way it does requires a detailed understanding of not only the genetic changes that occurred in its evolution, but also the environmental changes that may have accompanied such changes.
SEXUAL REPRODUCTION IN MAMMALS
The evolutionary path from bacterial transgenic sex to the meiotic sex of animals is complex and has been the subject of considerable research and speculation in biology. For our own purposes, we will have to ignore the past 3.5 billion years of evolution and focus our attention on animals that have been around for only the last 200 million years; that is, mammals.
As we study mammalian reproduction, it will become clear that the cost of reproduction in these species is very large. A significant amount of energy is required for mammals to find and select mating partners, not to mention the costs of pregnancy, lactation, and rearing offspring. This is true whether we are speaking of wild mammals or domestic mammals. The high cost of reproduction in mammals is readily apparent in the livestock industry. Producers of cattle, sheep, pigs, and horses spend a tremendous amount of time and money on reproductive management. If the cost of reproduction in mammals is so high, then why have mammals endured over the past 200 million years? We can address this question in the same way we addressed the question about sexual reproduction. Mammals have been successful because their traits allow them to thrive in the environments they inhabit. There really is no good way to understand why an animal reproduces the way it does without understanding its environment and how it interacts with it.
SUMMARY OF MAJOR CONCEPTS
* In biology, sex can refer to the creation of a new individual via recombination of genes from separate sources, or a mode of reproduction (fusion of gametes which are produced via meiosis).
* Sex is neither a necessary nor sufficient condition for reproduction.
* Reproduction is one of several life-sustaining processes that are dependent on the ability of living beings to capture and metabolize energy.
* The biochemical reactions that sustain life obey the laws of thermodynamics; that is, they capture part of the potential energy of the sun to support metabolism and dissipate the remaining energy as waste or entropy.
* Although sexual reproduction requires more energy than asexual reproduction, it has proven to be a highly successful strategy for numerous species living under a wide variety of circumstances.
1. How many times during the past 24 hours has the word sex entered your thoughts and/or conversations? How was this word used? In other words, what definitions did you employ? Give some examples of how you might use the term differently.
2. In basic arithmetic, you learned that 1 + 1 = 2. However, with respect to sexual organisms 1 + 1 = 1. Explain this discrepancy.
3. Women and men who engage in heavy athletic training (e.g., long-distance running, swimming, bicycling, and so on) experience infertility; that is, they fail to produce sufficient gametes to reproduce.
Explain this in terms energy metabolism and thermodynamics.
4. Is sex a necessary and/or a sufficient condition for reproduction in humans? Explain.
Margulis, L. and D. Sagan. 1997. What is Sex? New York: Simon and Schuster.
Otto, S.P. and T. Lenormand. 2002. Resolving the paradox of sex and recombination. Nature Reviews Genetics 3:252-261.
Rothchild, I. 2003. The yolkless egg and the evolution of eutherian viviparity. Biology of Reproduction 68:337-357.
Rifkin, J. 1980. Entropy: A New World View. New York: The Viking Press.
Keith K. Schillo, PhD
Department of Animal and Food Sciences
University of Kentucky
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|Author:||Schillo, Keith K.|
|Publication:||Reproductive Physiology of Mammals, From Farm to Field and Beyond|
|Date:||Jan 1, 2009|
|Previous Article:||Chapter 1: Introduction.|
|Next Article:||Chapter 3: Organization and structure of mammalian reproductive systems.|