31.2. Evolution of Vertebrate Sexual Reproduction

Vertebrate sexual reproduction evolved in the ocean before vertebrates colonized the land. The females of most species of marine bony fish produce eggs, or ova, in batches and release them into the water. The males generally release their sperm into the water containing the eggs where the union of the free gametes occurs. This process is known as external fertilization.

Although seawater is not a hostile environment for gametes, it does cause the gametes to disperse rapidly, so their release by females and males must be almost simultaneous. Thus, most marine fish restrict the release of their eggs and sperm to a few brief and well-defined periods. Some reproduce just once a year, while others do so more frequently. There are few seasonal cues in the ocean that organisms can use as signals for synchronizing reproduction, but one allpervasive signal is the cycle of the moon. Once each month, the moon approaches closer to the earth than usual, and when it does, its increased gravitational attraction causes somewhat higher tides. Many marine organisms sense the tidal changes and entrain the production and release of their gametes to the lunar cycle.

Fertilization is external in most fish but internal in most other vertebrates. The invasion of land posed the new danger of desiccation (drying out), a problem that was especially severe for the small and vulnerable gametes. On land, the gametes could not simply be released near each other, because they would soon dry up and perish. Consequently, there was intense selective pressure for terrestrial vertebrates (as well as some groups of fish) to evolve internal fertilization—that is, the introduction of male gametes into the female reproductive tract. By this means, fertilization still occurs in a nondesiccating environment, even when the adult animals are fully terrestrial. The vertebrates that practice internal fertilization have three strategies for embryonic and fetal development. Depending upon the relationship of the developing embryo to the mother and egg, those vertebrates with internal fertilization may be classified as oviparous, ovoviviparous, or viviparous.

Oviparity. In oviparity, the eggs, after being fertilized internally, are deposited outside the mother’s body to complete their development. This is found in some bony fish, most reptiles, some cartilaginous fish, some amphibians, a few mammals, and all birds.

Ovoviviparity. In ovoviviparity, the fertilized eggs are retained within the mother to complete their development, but the embryos still obtain all of their nourishment from the egg yolk. The young are fully developed when they are hatched and released from the mother. This is found in some bony fish (including mollies, guppies, and mosquito fish), some cartilaginous fish, and many reptiles.

Viviparity. In viviparity, the young develop within the mother and obtain nourishment directly from their mother’s blood, rather than from the egg yolk. This is found in most cartilaginous fish (figure 31.4), some amphibians, a few reptiles, and almost all mammals.

Figure 31.4. Viviparous vertebrates carry live, mobile young within their bodies.

The young complete their development within the body of the mother and are then released as small but competent adults. Here a lemon shark has just given birth to a young shark, which is still attached by the umbilical cord.

Fish and Amphibians

Most fish and amphibians, unlike other vertebrates, reproduce by means of external fertilization.

Fish. Fertilization in most species of bony fish (teleosts) is external, and the eggs contain only enough yolk to sustain the developing embryo for a short time. After the initial supply of yolk has been exhausted, the young fish must seek its food from the waters around it. Development is speedy, and the young that survive mature rapidly. Although thousands of eggs are fertilized in a single mating, many of the resulting individuals succumb to microbial infection or predation, and few grow to maturity.

In marked contrast to the bony fish, fertilization in most cartilaginous fish is internal. The male introduces sperm into the female through a modified pelvic fin. Development of the young in these vertebrates is generally viviparous.

Amphibians. The amphibians invaded the land without fully adapting to the terrestrial environment, and their life cycle is still tied to the water. Amphibians, like the red-spotted newt in figure 31.5, reproduce in the water and have aquatic larval stages before moving to the land. Fertilization is external in many amphibians, just as it is in most species of bony fish. Gametes from both males and females are released through the cloaca, a common opening used by the digestive, reproductive, and urinary systems. Among the frogs and toads, the male grasps the female and discharges fluid containing the sperm onto the eggs as they are released into the water (figure 31.6). Although the eggs of most amphibians develop in the water, there are some interesting exceptions shown in figure 31.7. In two species of frogs (one being the Darwin’s frog in figure 31.7d), the eggs develop in the vocal sacs and the stomach, and the young frogs leave through their parent’s mouth!

Figure 31.5. Life cycle of the red-spotted newt.

Many salamanders have both aquatic and terrestrial stages in their life cycle. In the red-spotted newt (Notophthalmus viridescens), eggs are laid in water and hatch into aquatic larvae with external gills and a finlike tail. After a period of growth, the larvae can metamorphose into a terrestrial "red eft" stage that later metamorphoses again to produce aquatic, breeding adults.

Figure 31.6. The eggs of frogs are fertilized externally.

When frogs mate, as these two are doing, the clasp of the male induces the female to release a large mass of mature eggs, over which the male discharges his sperm.

Figure 31.7. Different ways young develop in frogs.

(a) In the poison arrow frog, the male carries the tadpoles on his back. (b) In the female Surinam frog, froglets develop from eggs in special brooding pouches on the back. (c) In the South American pygmy marsupial frog, the female carries the developing larvae in a pouch on her back. (d ) Tadpoles of the Darwin's frog develop into froglets in the vocal pouch of the male and emerge from the mouth.

The time required for development of most amphibians is much longer than that for fish, but amphibian eggs do not include a significantly greater amount of yolk. Instead, the process of development in most amphibians is divided into embryonic, larval, and adult stages, in a way reminiscent of the life cycles found in some insects. The embryo develops within the egg, obtaining nutrients from the yolk. After hatching from the egg, the aquatic larva then functions as a free-swimming, food-gathering machine, often for a considerable period of time. The larvae may increase in size rapidly; some tadpoles, which are the larvae of frogs and toads, grow in a matter of weeks from creatures no bigger than the tip of a pencil into individuals as big as a goldfish. When the larva has grown large enough, it undergoes a developmental transition, or metamorphosis, into the terrestrial adult form.

Reptiles and Birds

Most reptiles and all birds are oviparous, laying amniotic eggs that are protected by watertight membranes from desiccation. After the eggs are fertilized internally, they are deposited outside of the mother’s body to complete their development. Like most vertebrates that fertilize internally, most male reptiles use a cylindrical organ, the penis, to inject sperm into the female, a process called copulation (figure 31.8). The penis, containing erectile tissue, can become quite rigid and penetrate far into the female reproductive tract. Reptiles exhibit all three types of internal fertilization. Most are oviparous, laying eggs and then abandoning them. These eggs are surrounded by a leathery shell that is deposited as the egg passes through the oviduct, the part of the female reproductive tract leading from the ovary. Other species of reptiles are ovoviviparous (forming eggs that develop into embryos and hatch within the body of the mother) or viviparous (developing inside the mother while being nourished by her rather than by the yolk of an egg).

Figure 31.8. The introduction of sperm by the male into the female's body is called copulation.

All birds practice internal fertilization, though most male birds lack a penis. In some of the larger birds (including swans, geese, and ostriches), however, the male cloaca extends to form a false penis. Figure 31.9a shows the formation of a bird’s egg. As the fertilized egg (ovum) passes along the oviduct (from top to bottom here), glands secrete albumin proteins (the egg white) and the hard, calcareous shell that distinguishes bird eggs from reptilian eggs. While modern reptiles are poikilotherms (animals whose body temperature varies with the temperature of their environment), birds are homeotherms (animals that maintain a relatively constant body temperature independent of environmental temperatures). Hence, most birds incubate their eggs after laying them to keep them warm (figure 31.9b).

Figure 31.9. Egg formation and incubation in birds.

(a) In birds, fertilization of the egg (ovum) takes place within the female, in the upper portion of the oviduct. As the fertilized egg passes down the oviduct, albumin (egg white), shell membranes, and the shell is secreted around the egg. (b) Bird eggs must be kept warm after they are laid. This blue-footed booby is incubating its two eggs.

The shelled eggs of reptiles and birds constitute one of the most important adaptations of these vertebrates to life on land, because shelled eggs can be laid in dry places. Such eggs are known as amniotic eggs because the embryo develops within a fluid-filled cavity surrounded by a membrane called the amnion. The amnion is an extraembryonic membrane—that is, a membrane formed from embryonic cells but located outside the body of the embryo. Amniotic eggs contain three other extraembryonic membranes, one of which is a yolk sac. In contrast, the eggs of fish and amphibians contain only one extraembryonic membrane, the yolk sac.

Mammals

Some mammals are seasonal breeders, reproducing only once a year, such as dogs, foxes, and bears, whereas others, such as horses and sheep, have multiple, short reproductive cycles throughout a given time of the year. Among the latter, the females generally undergo the reproductive cycles, whereas the males are more constant in their reproductive activity. Cycling in females involves the periodic release of a mature ovum from the ovary in a process known as ovulation.

Most female mammals are “in heat,” or sexually receptive to males, only around the time of ovulation. This period of sexual receptivity is called estrus, and the reproductive cycle is therefore called an estrous cycle. Females continue to cycle until they become pregnant.

In the estrous cycle of most mammals, changes in the secretion of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) by the anterior pituitary gland cause changes in egg cell development and hormone secretion in the ovaries. Humans and apes have menstrual cycles that are similar to the estrous cycles of other mammals in their cyclic pattern of hormone secretion and ovulation. Unlike mammals with estrous cycles, however, human and some ape females bleed when they shed the inner lining of their uterus, a process called menstruation, and may engage in copulation at any time during the cycle.

Rabbits and cats differ from most other mammals in that they are induced ovulators. Instead of ovulating in a cyclic fashion regardless of sexual activity, the females ovulate only after copulation as a result of a reflex stimulation of LH secretion (described later). This makes them extremely fertile.

Monotremes (the most primitive mammals, consisting solely of the duck-billed platypus and the echidna), are oviparous, like the reptiles from which they evolved. They incubate their eggs in a nest (figure 31.10a) or specialized pouch, and the young hatchlings obtain milk from their mother’s mammary glands by licking her skin, because monotremes lack nipples. All other mammals are viviparous, divided into two subcategories based on how they nourish their young.

Marsupials, a group that includes opossums and kangaroos, give birth to fetuses that are incompletely developed. They complete their development in a pouch of their mother’s skin, where they obtain nourishment from nipples of her mammary glands (figure 31.10b).

Placental mammals (figure 31.10c) retain their young for a much longer period of development within the mother’s uterus. The fetuses are nourished by a structure known as the placenta, which is derived from both an extraembryonic membrane and from the mother’s uterine lining. Because the fetal and maternal blood vessels are in very close proximity in the placenta, the fetus can obtain nutrients by diffusion from the mother’s blood. The placenta is discussed in more detail later in this chapter.

Figure 31.10. Reproduction in mammals.

(a) Monotremes, like the duck-billed platypus shown here, lay eggs in a nest. (b) Marsupials, such as this kangaroo, give birth to small fetuses that complete their development in a pouch. (c) In placental mammals, such as this doe nursing her fawn, the young remain inside the mother's uterus for a longer period of time and are born relatively more developed. (c) Placentals

Key Learning Outcome 31.2. Fertilization is external in frogs and most bony fish and internal in other vertebrates. Birds and most reptiles lay watertight eggs, as do monotreme mammals. All other mammals are viviparous.