Concept 37.3: Reproduction Is Integrated with the Life Cycle

Reproduction is an essential part of an animal’s life cycle. Because of this, a full understanding of reproduction often involves asking questions about the life cycle. Does reproduction place limits on the rest of the life cycle? Does the life cycle compel reproduction to take place in certain ways? These are just some of the questions that arise.

Animals often gain flexibility by having mechanisms to decouple the steps in reproduction

In humans, the individual steps in the reproductive process are rigidly linked. Mating leads promptly to fertilization, fertilization leads promptly to embryonic development, and development adheres to a relatively rigid schedule, culminating in birth at a relatively fixed time after fertilization. Some other animals also show this sort of rigid sequencing. In cases like this, the individual steps in the reproductive process cannot be separately coordinated with conditions in the environment.

Many animal species, however, have evolved mechanisms of decoupling successive steps in the reproductive process, so that the time that elapses between one step and the next is flexible. Such mechanisms increase options for certain steps to be coordinated with environmental conditions independently of other steps.

Sperm storage in the female reproductive tract is a common mechanism that provides for flexible timing between copulation and fertilization. With sperm storage, fertilization can occur long after copulation.

Female blue crabs (Callinectes sapidus) illustrate the advantages of sperm storage. They typically copulate during only one short period in their lives. However, they store the sperm they acquire. Thus they can make and fertilize new masses of eggs for over a year. Queen honey bees store sperm for years. Sperm storage also occurs in certain other crustaceans and insects, and in certain bats, sharks, nonavian reptiles, and birds.

Embryonic diapause—a programmed state of arrested or profoundly slowed embryonic development—occurs in many animals. In cases of embryonic diapause, embryos start to develop but then stop for a while before continuing. This permits adjustment of the time between fertilization and completion of embryonic development.

Silkworm moths (Bombyx) use embryonic diapause to ensure that their offspring do not hatch out of their eggs in winter. The adult moths copulate, fertilization occurs, and the eggs are laid in the autumn of the year. These autumn-laid eggs are programmed to undergo a complete arrest of development (cessation of mitosis) early in embryonic development. After the eggs have entered this arrest, they must be exposed to a low temperature (5°C or lower) for about 2 months before they can emerge from the arrested state. These interacting processes—the programmed appearance of diapause and the need for extended cold exposure to terminate it—ensure that eggs laid in the autumn do not hatch into hungry caterpillars during winter. The eggs need winter cold to emerge from developmental arrest. They accordingly hatch in the spring.

Embryonic diapause in placental mammals is usually called delayed implantation. The reason for this name is that the developmental arrest involves postponing the implantation of the blastocyst into the endometrium.

One of the most astounding examples of embryonic diapause is in Antarctic fur seals (Arctocephalus gazella). This species uses delayed implantation to achieve an exact match between the length of its reproductive cycle and the length of the calendar year. The challenge these seals face is that they have only a narrow window of time, early in the Antarctic summer, to give birth. If they give birth much earlier, their offspring can be killed by late winter storms. If they give birth much later, their offspring cannot grow as much as they need to before the next winter starts.

These fur seals have evolved a reproductive cycle in which the time between copulation and birth is almost exactly 365 days. Thus they give birth and copulate in the early summer one year, and they give birth to the offspring from that copulation 365 days later in the early summer of the next year.

However, the placental development of a young Antarctic fur seal (measured from implantation to birth) lasts only 250 days. If the seals were like people—with all the steps rigidly linked—a youngster conceived in the early summer would be born around March 1 in the cold of the Antarctic winter. The seals solve this problem with delayed implantation (FIGURE 37.13). After fertilization, the blastocyst enters the uterus, but it does not implant. Instead it goes into arrest for more than 3 months and then implants. At that point, 250 days remain before the proper birthing moment.

Figure 37.13: The Role of Delayed Implantation in the Life Cycle of the Antarctic Fur Seal

Some animals can reproduce only once, but most can reproduce more than once

One of the most important reproductive characteristics of a species is the number of times that individuals are physiologically capable of reproducing during their lives. In some animals, termed semelparous, each individual is physiologically programmed to reproduce only once. Octopuses, some fish, many insects, and many marine worms are semelparous.

Octopuses and Pacific salmon provide two dramatic examples. A species of octopus that is particularly well studied is Octopus vulgaris. Many other species are believed to resemble it. Males place spermatophores (packets of sperm) in the reproductive tracts of females during mating, and the females lay fertilized eggs soon after. At that point, a female stops eating and guards her eggs for 1–2 months (FIGURE 37.14A). Guarding her eggs is her final achievement, because she dies soon after her eggs hatch. Males also die at about the same time. Both the females and males reproduce only once in their lives.

Figure 37.14: Semelparity (A) In many species of octopuses, a female produces eggs just once in her life and guards them. She does not eat while guarding her eggs, and she dies after they hatch. (B) Sockeye salmon (Oncorhynchus nerka) expend enormous resources to reach freshwater spawning areas, then die after spawning.

The same is true of Pacific salmon such as sockeye salmon (Oncorhynchus nerka). After sockeye salmon grow to adulthood over a period of 1–4 years in the Pacific Ocean (see Concept 36.3), they migrate up rivers—sometimes hundreds of miles—before spawning. As soon as they enter the rivers from the sea, both sexes stop eating. Accordingly, they power their upriver migration entirely by breaking down their own body substance. After reaching a suitable spot to spawn, they release their gametes and die (FIGURE 37.14B).

When a species is semelparous, parents often sacrifice their own well-being to an extraordinary extent to provide the resources they need to produce their offspring. This is understandable because the parents have no future reproductive potential after their single period of reproduction. By the time sockeye salmon spawn, they are often capable of little else but spawning because they have so thoroughly depleted their bodies.

Most animal species are iteroparous, meaning that individuals are physiologically capable of two or more separate periods of reproductive activity during their lives (i.e., multiple “iterations” of reproduction). In many species, for example, individuals reproduce at least once per year for as many years as they live.

The question of parental investment in offspring is far more complex in iteroparous animals than in semelparous ones. This is because when iteroparous parents produce offspring at any one time, they remain able to produce more offspring at future times. To gain the advantages of future reproduction, they must survive: as they reproduce, they must keep enough resources for themselves to preserve their own health. Their use of resources over their lives thus follows a different pattern than in semelparous species.

Seasonal reproductive cycles are common

In iteroparous animals that live in environments with regular seasonal cycles, the reproductive cycle is nearly always timed to coordinate with the environmental seasonal cycle. We humans are unusual in not showing such seasonality.

The most common pattern is for animals to reproduce in months when temperature, food supply, and other conditions are favorable—such as spring and summer—and suspend reproduction during unfavorable months such as those of winter. Some species of rabbits and mice, for example, shut down their gonads during winter. The testes of the males stop making sperm, become small, and sometimes are withdrawn from the scrotum into the abdomen. The testes then regrow, move into the scrotum, and resume sperm production in the spring. Females also suspend reproductive function and then restore it.

To describe life cycles like this, biologists often speak of animals as having a reproductive season and a nonreproductive season. In this context, “season” does not refer to the defined four seasons of the year. Instead, it refers to the months in which the animals are reproductive and those in which they are nonreproductive.

Some animals breed only once in each reproductive season. The red fox (Vulpes vulpes) of North America, for example, enters estrus for a single 1- to 6-day period—and ovulates once—each year during its reproductive season. Some other species of foxes and wolves are similar. If a female fails to mate at this time or loses her offspring, she does not enter estrus again until a full year later. Many birds also breed once per year.

Mammals more commonly superimpose an estrous cycle on their seasonal cycle. For example, during each month of her reproductive season each year, a female rat or mouse cycles in and out of estrus every 4–6 days unless she gets pregnant, as we’ve mentioned. Males produce sperm continuously during the months of the reproductive season.

Seasonal breeders require mechanisms to time their seasonal cycle. Often they employ environmental cues. Of these, the most important, in both invertebrates and vertebrates, is the amount of daylight per 24-hour day—termed the photoperiod. For example, many mice enter reproductive readiness when the photoperiod is increasing or long (i.e., during “the long days” of late spring and early summer). In this case, photoperiod is being used as a signal that the time of year is spring or summer. Because photoperiod varies in a mathematically exacting way with the time of year, it provides unambiguous information.

Circannual biological clocks are a second important mechanism for timing seasonal cycles. Sheep have internal timing mechanisms that time events for an entire year. Some other animals do as well. They use these circannual clocks to control their seasonal reproductive cycles.

ANSWER There is one important similarity. Ovulation occurs in response to a surge in the blood concentration of luteinizing hormone (LH) in both groups of mammals. Mammals that display induced and spontaneous ovulation differ, however, in how the LH surge is produced. In a species with induced ovulation, the LH surge is a direct response to copulation. The physical act of copulation stimulates sensory neurons that send signals to the brain, and the brain responds by promptly initiating the LH surge. In this way there is a deterministic connection between the presence of sperm in the female reproductive tract and the presence of ova. When sperm are provided by copulation, ova are provided by ovulation almost simultaneously.

In species with spontaneous ovulation, the timing of the LH surge depends on endogenous hormonal cycles in the female. These cycles occur on their own rhythm, more or less independently of whether copulation takes place. Accordingly, chance plays a greater role in determining whether sperm and ova will be present in the female reproductive tract at the same time. The degree of chance is reduced by estrus in many species of mammals with spontaneous ovulation. Females enter estrus approximately when they ovulate. Nonetheless, in a species with spontaneous ovulation, the timing of copulation and that of ovulation may be sufficiently different (because the two are not directly causally linked) for sperm to be present in the appropriate parts of the oviducts when ova are not, or vice versa.