Population Sampling

CHAPTER 10

Smith, T. M., & Smith, R. L. (2015). Elements of Ecology (9th ed.). Boston, MA: Pearson.

10.1 The Evolution of Life Histories Involves Trade-offs

If reproductive success (the number of offspring that survive to reproduce) is the measure of fitness, imagine designing an organism with the objective of maximizing its fitness. It would reproduce as soon as possible after birth, and it would reproduce continuously, producing large numbers of large offspring that it would nurture and protect. Yet such an organism is not possible. Each individual has a limited amount of resources that it can allocate to specific tasks. Its allocation to one task reduces its resources available for other tasks. Thus, allocation to reproduction reduces the amount of resources available for growth. Should an individual reproduce early in life or delay reproduction? For a given allocation of resources to reproduction, should an individual produce many small offspring or fewer and larger offspring? Each possible action has both benefits and costs. Thus, organisms face trade-offs in life history characteristics related to reproduction, just as they do in the adaptations related to carbon, water, and energy balance (discussed in Chapters 6 and 7). These trade-offs involve modes of reproduction; age at reproduction; allocation to reproduction; number and size of eggs, young, or seeds produced; and timing of reproduction. These trade-offs are imposed by constraints of physiology, energetics, and the prevailing physical and biotic environment—the organism’s habitat. As such, the evolution of an organism’s life history reflects the interaction between intrinsic and extrinsic factors. Extrinsic ecological factors such as the physical environment and the presence of predators or competitors directly influence age-specific rates of mortality and survivorship. Intrinsic factors relating to phylogeny (the evolutionary history of the species), patterns of development, genetics, and physiology impose constraints resulting in trade-offs among traits. In our discussion, we explore these trade-offs and the diversity of solutions that have evolved to assure success at the one essential task for continuation of life on our planet, reproduction.

10.2 Reproduction May Be Sexual or Asexual

In Chapter 5, we explored how genetic variation among individuals within a population arises from the shuffling of genes and chromosomes in sexual reproduction. In sexual reproduction between two diploid individuals, the individuals produce haploid (one-half the normal number of chromosomes) gametes—egg and sperm—that combine to form a diploid cell, or zygote, that has a full complement of chromosomes. Because the possible number of gene recombinations is enormous, recombination is an immediate and major source of genetic variability among offspring. However, not all reproduction is sexual. Many organisms reproduce asexually (see Section 8.1). Asexual reproduction produces offspring without the involvement of egg and sperm. It takes many forms, but in all cases, the new individuals are genetically the same as the parent. Strawberry plants spread by stolons, modified lateral stems from which new roots and vertical stems sprout (see Figure  8.2). The one-celled paramecium reproduces by dividing in two. Hydras, coelenterates that live in freshwater (see Figure 9.2), reproduce by budding—a process by which a bud pinches off as a new individual. In spring, wingless female aphids emerge from eggs that have survived the winter and give birth to wingless females without fertilization, a process called Parthenogenesis (Greek Parthenos, “virgin”; Latin genesis, “to be born”).

Organisms that rely heavily on asexual reproduction revert occasionally to sexual reproduction. Many of these reversions to sexual reproduction are induced by an environmental change at some time in their life cycle. During warmer parts of the year, hydras turn to sexual reproduction to produce eggs that lay dormant over the winter and from which young hydras emerge in the spring to mature and reproduce asexually. After giving birth to several generations of wingless females, aphids produce a generation of winged females that migrate to different food plants, become established, and reproduce parthenogenetically. Later in the summer, these same females move back to the original food plants and give birth to true sexual forms—winged males and females that lay eggs rather than give birth to young.

Each form of reproduction, asexual and sexual, has its trade-offs. The ability to survive, grow, and reproduce indicates that an organism is adapted to the prevailing environmental conditions. Asexual reproduction produces offspring that are genetically identical to the parent and are, therefore, adapted to the local environment. Because all individuals are capable of reproducing, asexual reproduction results in a potential for high population growth. However, the cost of asexual reproduction is the loss of genetic recombination that increases variation among offspring. Low genetic variability among individuals in the population means that the population responds more uniformly to a change in environmental conditions than does a sexually reproducing population. If a change in environmental conditions is detrimental, the effect on the population can be catastrophic.

In contrast, the mixing of genes and chromosomes that occurs in sexual reproduction produces genetic variability to the degree that each individual in the population is genetically unique. This genetic variability produces a broader range of potential responses to the environment, increasing the probability that some individuals will survive environmental changes. But this variability comes at a cost. Each individual can contribute only one-half of its genes to the next generation. It requires specialized reproductive organs that, aside from reproduction, have no direct relationship to an individual’s survival. Production of gametes (egg and sperm), courtship activities, and mating are energetically expensive. The expense of reproduction is not shared equally by both sexes. The eggs (ovum) produced by females are much larger and energetically much more expensive than sperm produced by males. As we shall examine in the following sections, this difference in energy investment in reproduction between males and females has important implications in the evolution of life history characteristics.

10.3 Sexual Reproduction Takes a Variety of Forms

Sexual reproduction takes a variety of forms. The most familiar involves separate male and female individuals. It is common to most animals. Plants with that characteristic are called dioecious (Greek di, “two,” and oikos, “home”; Figure 10.1a).

In some species, individual organisms possess both male and female organs. They are hermaphrodites (Greek hermaphroditos). In plants, individuals can be hermaphroditic by possessing bisexual flowers with both male organs, stamens, and female organs, ovaries (Figure 10.1b). Such flowers are termed perfect. Asynchronous timing of the maturation of pollen and ovules reduces the chances of self-fertilization. Other plants are monoecious (Greek mono, “one,” and oikos, “home”). They possess separate male and female flowers on the same plant (Figure  10.1c). Such flowers are called imperfect. This strategy of sexual reproduction can be an advantage in the process of colonization. A single self-fertilized hermaphroditic plant can colonize a new habitat and reproduce, establishing a new population; this is what self-fertilizing annual weeds do that colonize disturbed sites.

Among animals, hermaphroditic individuals possess the sexual organs of both males and females (both testes and ovaries), a condition common in invertebrates such as earthworms (Figure 10.2). In these species, referred to as simultaneous hermaphrodites, the male organ of one individual is mated with the female organ of the other and vice versa. The result is that a population of hermaphroditic individuals is in theory able to produce twice as many offspring as a population of unisexual individuals.

Other species are sequential hermaphrodites. Animals—such as some mollusks and echinoderms—and some plants may be males during one part of their life cycle and females in another part. Some fish may be females first, then males. Sex change usually takes place as individuals mature or grow larger. A change in the sex ratio of the population stimulates sex change among some animals. Removing individuals of the other sex initiates sex reversal among some species of marine fish (Figure 10.3). Removal of females from a social group among some coral reef fish stimulates males to change sex and become females. In other species, removal of males stimulates a one-to-one replacement of males by sex-reversing females. Among the mollusks, the Gastropoda (snails and slugs) and Bivalvia (clams and mussels) have sex-changing species. Almost all of these species change from male to female.

Plants also can undergo sex change. One such plant is jack-in-the-pulpit (Arisaema triphyllum), a clonal herbaceous plant found in the woodlands of eastern North America (Figure  10.4). Jack-in-the-pulpit may produce male flowers one year, an asexual vegetative shoot the next, and female flowers the next. Over its life span, a jack-in-the-pulpit may produce both sexes as well as an asexual vegetative shoot but in no particular sequence. Usually an asexual stage follows a sex change. Sex change in jack-in-the-pulpit appears to be triggered by the large energy cost of producing female flowers. Jack-in-the-pulpit plants generally lack sufficient resources to produce female flowers in successive years; male flowers and pollen are much cheaper to produce than female flowers and subsequent fruits.

10.4 Reproduction Involves Both Benefits and Costs to Individual Fitness

To understand how trade-offs function to influence natural selection requires an understanding of the balance between benefits and costs associated with a phenotypic trait. If the objective of reproduction is to maximize the relative fitness of the individual, then the benefit of increasing the number of offspring produced would seem obvious. Yet a central tenet of life history theory is that the behavioral, physiological, and energetic activities involved in reproduction extract some sort of cost to future reproductive success in the form of reduced survival, fecundity, or growth.

There are many examples of various activities involved in reproduction that increase an individual’s probability of mortality in addition to the direct physiological costs of reproduction. Activities associated with the acquisition of a mate (see Sections 10.11 and 10.12), defense of a breeding territory (see Chapter 11, Section 11.10), and the feeding and protection of young can reduce the probability of future survival.

The work of Tim Cutton-Block of Cambridge University provides an example of the costs of reproduction in terms of increased probability of future survival. In the development of life tables for a population of red deer in central Scotland, he examined differences in the age-specific patterns of mortality for females—referred to as milk hinds—who have reared a calf to weaning age and those who have not—referred to as yeld hinds (Figure 10.5). The higher reproductive costs to milk hinds associated with the care and feeding (lactation) of calves result in higher mortality rates than those observed for yeld hinds (Figure 10.5a).

Reproduction can also directly reduce an individual’s ability to produce future offspring. The current reproductive expenditure might leave the individual with insufficient energy resources to produce the same number of offspring during future periods of reproduction (Figure 10.5b). For example, studies by Sveinn Hanssen of the University of Tromso in Norway have shown that current reproduction results in reduced future fecundity in eider ducks. The common eider (Somateria mollissima) is a long-lived sea duck whose females do not eat during the incubation period. As a result, the reproductive effort of the female results in an increased loss of body mass and reduced immune function.

In a four-year study, Richard Primack and Pamela Hall of Boston University examined the costs of reproduction in the pink lady’s slipper orchid (Cypripedium acaule). In two eastern Massachusetts populations, the researchers randomly assigned plants to be hand pollinated (increased reproduction) or left as controls, and the treatments were repeated in four successive years. By the third and fourth years of the study, the high cost of reproduction resulted in a lower growth and flowering rate of hand-pollinated plants in comparison with the control plants. For an average-sized plant, the production of fruit in the current year results in an estimated 10–13 percent decrease in leaf area and a 5–16 percent decrease in the probability of flowering in the following year. Increased allocation of resources to reproduction relative to growth diminished future fecundity (Figure 10.6).

Interpreting Ecological Data

1. Q1. What is the approximate difference in the probability of flowering in 1987 for individuals with a leaf area of 200 cm2 that produced zero fruits and three fruits during the period from 1984 to 1986? What does this tell you about the impact of the costs of past reproduction on future prospects of reproduction?

2. Q2. According to the preceding figure, the probability of an individual with leaf area of 100 cm2 that produced zero fruits over the past three years (1984–1986) flowering in the following year (1987) is approximately 0.5 (or 50 percent). How large would an individual that bore three fruits over the past three years have to be to have the same probability of flowering?

Allocation to reproduction has been shown to reduce allocation to growth in a wide variety of plant and animal species (Figure 10.7). In many species, there is a direct relationship between body size and fecundity (Figure 10.8). As a result, an individual reproducing earlier in age will produce fewer offspring per reproductive period than an individual that postpones reproduction in favor of additional growth.

The act of reproduction at a given age, therefore, has potential implications to both age-specific patterns of mortality (survivorship) and fecundity (birthrate) moving forward. For this reason, the age at which reproduction begins—the age at maturity—is a key aspect of the organism’s life history.

10.5 Age at Maturity Is Influenced by Patterns of Age-Specific Mortality

When should an organism begin the process of reproduction? Some species begin reproduction early in their life cycle, whereas others have a period of growth and development before the onset of reproduction. If natural selection functions to maximize the relative fitness of the individual, then the age and size at maturity are optimized when the difference between the costs and benefits of maturation at different ages and sizes is maximized. That is when the “payoff” in the fitness of the individual is greatest. An important component of this evolution is the age-specific pattern of mortality because it both shapes and is shaped by the age-specific expenditures of reproductive effort.

To explore how natural selection can function to influence the age at maturity, let’s return to think about the age-specific patterns of survival and fecundity that we developed in the previous chapter, that is, the patterns of survival and fecundity that determine the trajectory of population growth (Table   10.1 ; see also Section 9.6 ). Recall that the first column labeled x shows the age or age class of individuals in the population. The column labeled sx shows the age-specific survival rates (the probability of an individual of age x surviving to age x + 1), and column bx represents the average number of female offspring produced by an individual female of age x. The three columns have been divided into three distinct age categories relating to reproduction: prereproductive, reproductive, and postreproductive. Prereproductive age categories represent juveniles, whereas the reproductive and postreproductive categories are referred to as adults. The age of maturity then represents the transition from juvenile to adult, or the age at which first reproduction occurs. In our example, we assume that the organism reproduces repeatedly following the onset of maturity until postreproductive age is achieved; however, this is not always the case, as we will discuss later. Our objective is to understand that both extrinsic and intrinsic factors influence the evolution of age at maturity.

Natural selection will favor those individuals whose age at maturity results in the greatest number of offspring produced over the lifetime of an individual. Consider a simple hypothetical example of a species that continues to grow with age only until it reaches sexual maturity and then begins to reproduce. As with the examples presented in Figure 10.8, assume that fecundity increases with body weight—the larger the individual female, the greater the number of offspring produced per time period (reproductive event). Now assume that individuals within the population vary in the age at which they achieve maturity. As a result of differences in body weight, a female that begins to reproduce at age 3 will produce 10 offspring per year over the duration of her lifetime, whereas a female that delays reproduction until age 5 will have a 50 percent greater fecundity, or 15 offspring per year (Figure  10.9). Therefore, we can calculate the cumulative number of offspring produced at any point in each female’s life by summing the number of offspring from the onset of maturity to that age (see Figure  10.9). Note in Figure 10.9 that the female that delayed maturity until year 5 has produced a greater number of offspring over her lifetime. Thus, natural selection should favor delayed maturity. However, this conclusion assumes that the females live to their maximum age (12 years). In fact, before age eight the female that matured early has a greater cumulative number of offspring, and it is only if females survive past year eight that the strategy of delayed maturity increases fitness. Recall the difference between gross and net reproductive rate presented previously (Section 9.6). The value obtained by summing the values in the bx column as was done in this example is a measure of gross reproductive rate, and the strategy of delayed maturity is clearly the winner in terms of fitness. However, the true measure of reproductive rate is net reproductive rate (R 0), as it considers both the age-specific values of fecundity (bx ) and the age-specific values of survivorship (lx ). If survival beyond age eight is an improbable event for this species, then the strategy of early maturity results in the greater fitness.

As the preceding hypothetical example demonstrates, the primary fitness advantage of delaying maturity is the larger initial body size obtained by individuals when they first reproduce. The primary cost of delaying reproduction (late maturity) is the increased risk of death before reproduction, or death before the advantage of increased fecundity as a result of delayed maturity are fully realized—in this example, death before age eight. If one assumes that natural selection acts on age-specific potential of producing future offspring, then age at maturity can be predicted from the mean juvenile and adult survival rates (sx column in Table 10.1). Decreases in the ratio of adult-to-juvenile survival (low survival for adults relative to juveniles) appear to favor reductions in age at maturity. As external factors (those unassociated with reproduction) increase adult mortality, selection would be expected to favor genotypes that mature earlier (before those ages), thus increasing their probability of contributing genes to future generations.

number of long-term experiments in which patterns of mortality have been manipulated, support the prediction that natural selection favors earlier maturation when adult survival is reduced, and conversely, that it favors delayed maturation when, relative to adult survival, juvenile survival is reduced. David Reznick and colleagues at the University of California–Riverside conducted a long-term experiment on guppies in Trinidad in which the predictions relating to age-specific patterns of mortality and age at maturity are supported. Local populations of guppies on the island differ in their life history characteristics, and differences among populations are closely associated with the identity of the predator species living in their habitat. Predator species alter age-specific survival because they are size specific in their choice of prey. Crenicichla alta (a cichlid), the main predator at one set of the localities, preys predominantly on larger guppies from sexually mature size classes. At other localities, Rivulus hartii (a killifish) is the main predator. Rivulus feeds primarily on small guppies from immature size classes. Guppies from localities with Crenicichla mature at an earlier age than do guppies from localities with Rivulus. To prove that differences in age-specific patterns of survival result from different patterns of predation causing differences in age at maturity, Reznick and colleagues transplanted guppies from a site with Crenicichla to a site that contained Rivulus, but no guppies. This manipulation released the guppies from selective predation on adults and exposed them to selective predation on juveniles.

Eleven years (30–60 generations) after the shift in predation-induced mortality from adults to juveniles, guppies responded to the increase in the ratio of adult-to-juvenile survival with significantly increased age at maturity (from 48 to 58 days). The increased age at maturity was accompanied by a larger average size at age of maturity for females and the production of fewer, but larger offspring (Figure 10.10).

10.6 Reproductive Effort Is Governed by Trade-offs between Fecundity and Survival

Fecundity is the number of offspring produced per unit of time (bx ), but the energetic costs of reproduction include a wide variety of physiological and behavioral activities in addition to the energy and nutrient demands of the reproductive event, including gonad development, movement to spawning area, competition for mates, nesting, and parental care. Together, the total energetic costs of reproduction per unit time are referred to as an individual’s reproductive effort.

The amount of energy organisms invest in reproduction varies. Herbaceous perennials invest between 15 and 20 percent of annual net production in reproduction, including vegetative propagation. Wild annuals that reproduce only once expend 15 to 30 percent, most grain crops—25 to 30 percent, and corn and barley—35 to 40 percent. The common lizard (Lacerta vivipara) invests 7 to 9 percent of its annual energy assimilation in reproduction. The female Allegheny Mountain salamander (Desmognathus ochrophaeus) expends 48 percent of its annual energy budget on reproduction.

Reproductive effort is thought to be associated with the adaptive responses to age at maturity discussed previously (Section 10.5). For example, a decline in adult (reproductive) survival rate relative to that of juveniles (prereproductive) is predicted to favor genotypes that mature earlier in life and increase reproductive effort. The probability of future survival (and therefore future reproduction) is low, so early maturity and high reproductive effort will maximize individual fitness. Conversely, an increased juvenile mortality results in delayed maturity and reduced reproductive effort. This is the pattern that was observed by Reznick and colleagues in their experiments with predation-induced mortality in populations of guppies on Trinidad (see Figure 10.10a).

Michael Fox and Allen Keast of Trent University in Canada found that pumpkinseed fish (Lepomis gibbosus) inhabiting two shallow ponds that experienced major winterkills (weather-related mortality events during winter months) matured one to two years earlier and at a smaller size (a difference >20 millimeters [m] in length) than individuals of the same species living in an adjacent lake in which winterkill did not occur. In addition, females inhabiting the high-mortality environment had a significantly higher energy allocation to reproduction than those inhabiting low-mortality environments.

In both of the aforementioned studies, the researchers found that variations in allocation to reproduction were related to patterns of mortality caused by extrinsic factors (predation or extreme temperatures). Patterns of mortality, however, are also influenced directly by reproductive effort. For example, in the study of red deer presented in Figure 10.5, allocation to reproduction resulted in an increased female mortality rate. Therefore, allocation to reproduction at any time during the life of an individual involves trade-offs between current benefits from the production of offspring and costs in terms of potential reduction in future reproduction. Natural selection functions to optimize the trade-offs between present and future reproduction.

An optimized life history is one wherein conflicts between the competing demands for survival and reproduction are resolved to the advantage of the individual in terms of fitness. To explore this relationship, we can examine how fecundity and survival vary as a function of allocation to reproduction at any given time period in an individual’s life.

Cor Dijkstra and colleagues at the University of Groningen in the Netherlands examined the trade-off between fecundity and survival in the European kestrel (Falco tinnunculus), which is a predatory bird that feeds on small mammals. Both parents provide food for the brood (offspring); therefore, reproductive allocation associated with the feeding of young can be approximated by the time (hours/day) spent in flight (hunting activity). The brood size for nesting pairs of kestrels in the study area averaged five chicks.

The researchers divided the nesting population in the study area into two groups: a nonmanipulated control group and a group in which brood size in the nests was manipulated. Starting when the nestlings were 5 to 10 days old, the researchers removed two nestlings from selected nests, thus reducing brood size by two. These chicks were then transferred to other nests, increasing the size of the brood by two. Brood enlargement forced an increase in daily hunting activities of both parents (Figure 10.11a). Despite the increase, food intake per chick declined with increased brood size. This decline resulted in reduced growth rate of the nestlings and increased nestling mortality (Figure 10.12). In addition, brood enhancement resulted in enhanced weight loss in the female parent, and survival of the parents was negatively correlated with the experimental change in brood size (Figure 10.11b). Increased allocation to reproduction (energy expenditure to the feeding and caring of offspring) resulted in a reduction in the probability of future survival of parents and, therefore, future reproduction.

Interpreting Ecological Data

1. Q1. How would a decrease in the probability of offspring survival in Figure 10.13a change the optimal value for current reproductive allocation?

2. Q2. How would a decrease in adult survival in Figure 10.11b change the optimal value for current reproductive allocation?

The responses of offspring and parental survival to brood enhancement in the study by Dijkstra reveal two patterns that are essential to understanding how natural selection functions to optimize reproductive effort. First, as reproductive effort increased, the number of offspring increased, but the probability of offspring survival decreased. Therefore, for any given value of reproductive effort, current reproductive success is the product of the two: number of offspring produced multiplied by the probability of their survival. As a result of the inverse relationship between the number of offspring and their probability of survival (Figure 10.13), the resulting pattern of current reproductive success is one of diminishing returns, with each additional unit of reproductive allocation returning a decreasing benefit in terms of current fecundity (Figure 10.14). Second, as reproductive effort increased, parental survival decreased, once again with each additional unit of reproductive allocation representing an increased cost in terms of future fecundity.Figure 10.14 illustrates these patterns in that each additional unit of reproductive allocation returns a decreasing benefit (current reproduction) and increasing cost (reduced future reproduction). The dashed line represents the sum of the values for current and future reproduction for any given allocation to reproduction (value along x-axis). The dashed line reaches its maximum value at intermediate values of reproductive allocation. Fitness of the parent is often maximized at intermediate reproductive effort (investment), particularly for organisms that reproduce repeatedly. In this analysis, optimal allocation to reproduction is not the maximum possible number of offspring that can be produced for a given reproductive event, and it is not the allocation that maximizes the benefit in terms of current fecundity (maximum offspring survival; see Figure 10.14). If natural selection functions to maximize the relative fitness of the parent, the allocation to reproduction represents a trade-off with parental, not offspring, survival. Natural selection functions to maximize fitness over the lifetime of the parent.

10.7 There Is a Trade-off between the Number and Size of Offspring

In theory, a given allocation to reproduction can potentially produce many small offspring or fewer large ones (Figure  10.15). The number of offspring affects the parental investment each receives. If the parent produces a large number of young, it can afford only minimal investment in each one. In such cases, animals provide no parental care, and plants store little food energy in seeds. Such organisms usually inhabit disturbed sites, unpredictable environments, or places such as the open ocean where opportunities for parental care are difficult at best. By dividing energy for reproduction among as many young as possible, these parents increase the chances that some young will successfully settle and reproduce in the future.

Parents that produce few young are able to expend more energy on each. The amount of energy varies with the number, size, and maturity of individuals at birth. Some organisms expend less energy during incubation. The young are born or hatched in a helpless condition and require considerable parental care. These animals, such as young mice or nestling American robins (Turdus migratorius), are altricial. Other animals have longer incubation or gestation, so the young are born in an advanced stage of development. They are able to move about and forage for themselves shortly after birth. Such young are called precocial. Examples are gallinaceous birds, such as chickens and turkeys, and ungulate mammals, such as cows and deer.

The degree of parental care varies widely. Some species of fish, such as cod (Gadus morhua), lay millions of floating eggs that drift freely in the ocean with no parental care. Other species, such as bass, lay eggs in the hundreds and provide some degree of parental care. Among amphibians, parental care is most prevalent among tropical toads and frogs and some species of salamanders. The spotted (Ambystoma maculatum) and redback (Plethodon cinereus) salamanders found in eastern North America provide such an example of contrasting life history strategies relating to the number of young produced and parental care (Figure 10.16). The spotted salamander is found under logs and piles of damp leaves in deciduous forest habitats. During the month of February, individuals migrate to ponds and other small bodies of water to reproduce. After mating, females lay up to 250 eggs in large, compact, gelatinous masses that are attached to twigs just below the water surface. After mating, adults leave the water and provide no parental care of eggs or young. In contrast, the redback salamander occupies similar habitats in mixed coniferous–deciduous forests. After mating, females lay 4 to 10 eggs, which are deposited in a cluster within the crevice of a rotting log or stump. The female then curls about the egg cluster, guarding it until the larvae hatch.

Among reptiles, which rarely exhibit parental care, crocodiles are an exception. They actively defend the nest and young for a considerable time. Invertebrates exhibit parental care to varying degrees. Octopi, crustaceans (such as lobsters, crayfish, and shrimp), and certain amphipods brood and defend eggs. Parental care is best developed among the social insects: bees, wasps, ants, and termites. Social insects perform all functions of parental care, including feeding, defending, heating and cooling, and sanitizing.

How a given investment in reproduction is allocated, the number and size of offspring produced, and the care and defense provided all interact in the context of the environment to determine the return to the individual in terms of increased fitness (see Quantifying Ecology 10.1).

10.8 Species Differ in the Timing of Reproduction

How should an organism invest its allocation to reproduction through time? Thus far we have focused on age-structured populations in which reproduction begins with the onset of maturity and continues over some period of time until either reproduction ceases (postreproductive period) or senescence occurs. Organisms that produce offspring more than once over their lifetime are called iteroparous. Iteroparous organisms include most vertebrates, perennial herbaceous plants, shrubs, and trees. As we have explored, the timing of reproduction for iteroparous species involves trade-offs. Early reproduction means earlier maturity, less growth, reduced fecundity per reproductive period, reduced survivorship, and reduced potential for future reproduction. Later reproduction means increased growth, later maturity, and increased survivorship but less time for reproduction. In effect, to maximize contributions to future generations, an organism balances the benefits of immediate reproduction and future reproductive prospects, including the cost to fecundity (total offspring produced) and its own survival (Section 10.6).

Another approach to reproduction is to initially invest all energy in growth, development, and energy storage, followed by one massive reproductive effort, and then death. In this strategy, an organism sacrifices future prospects by expending all its energy in one suicidal act of reproduction. Organisms exhibiting this mode of reproduction are called semelparous.

Semelparity is employed by most insects and other invertebrates, by some species of fish (notably, salmon), and by many plants. It is common among annuals, biennials, and some species of bamboos. Many semelparous plants, such as ragweed (Ambrosia spp.), are small, short-lived, and found in ephemeral or disturbed habitats. For them, it would not be efficient, fitness-wise, to hold out for future reproduction because their chances of success are slim. They gain maximum fitness by expending all their energy in one bout of reproduction.

Other semelparous organisms, however, are long-lived and delay reproduction. Mayflies (Ephemeroptera) may spend several years as larvae before emerging from the surface of the water for an adult life of several days devoted to reproduction. Periodical cicadas spend 13 to 17 years belowground before they emerge as adults to stage a single outstanding exhibition of reproduction. Some species of bamboo delay flowering for 100 to 120 years, produce one massive crop of seeds, and die. Hawaiian silverswords (Argyroxiphium spp.) live 7 to 30 years before flowering and dying. In general, the fitness of species that evolved semelparity must increase enough to compensate for the loss of repeated reproduction.

As we have seen, optimal reproductive effort per unit time (per reproductive event) is the balance between current and future reproduction that functions to maximize the individual’s (parental) fitness. Within this framework, semelparity implies that one single maximum reproductive effort followed by death represents the optimal strategy for the individual in the context of its environment (external constraints). It follows that iteroparity evolved through a change in conditions such that less than the maximum possible reproductive effort is optimal on the first reproductive attempt and the organism survives to reproduce during future time intervals. What type of change in conditions might bring about the shift from semelparity to iteroparity? If the external environment imposes a high adult mortality relative to juvenile mortality, and if individuals reach maturity, chances are that they will not survive much longer; therefore, future reproductive expectations are bleak. Under these conditions, semelparity would be favored. If the opposite holds true and juvenile mortality is high compared to adult mortality, an individual has a good chance of surviving into the future once it survives to maturity; hence, prospects of future reproduction are good. Under these conditions iteroparity is favored.

Quantifying Ecology 10.1 Interpreting Trade-offs

Many of the life history characteristics discussed in this chapter involve trade-offs, and understanding the nature of trade-offs involves the analysis of costs and benefits for a particular trait.

One trade-off in reproductive effort discussed in Section  10.7 involves the number and size of offspring produced. The graph in Figure 1 is similar to the one presented in Figure 10.15, showing the trade-off relationship between seed size and the number of seeds produced per plant. The example assumes a fixed allocation (100 units); therefore, the number of seeds produced per plant declines with increasing seed size.

Based on this information alone, it would appear that the best strategy for maximizing reproductive success would be to produce small seeds, thereby increasing the number of offspring produced. However, we must also consider any benefits to reproductive success that might vary as a function of seed size. The reserves of energy and nutrients associated with large seed size have been shown to increase the probability of successful establishment, particularly for seedlings in low-resource environments. For example, J. A. Ramírez-Valiente of the Center for Forestry Research (CIFOR: Madrid, Spain) found that average seed size in local populations of cork oak (Quercus suber) in Spain increases with decreasing precipitation ( Figure  2), and that increased seed size was positively related to seedling survival under dry conditions (decreasing precipitation) (also see an example of the relationship between seed size and seedling survival in shade in Chapter  6, Field Studies: Kaoru Kitajima). A generalized relationship between seed size and seedling survival for two different environments (wet and dry) is plotted in Figure 3. In both environments, survival increases with seed size; however, in dry environments, the probability of survival declines dramatically with decreasing seed size.

By multiplying the number of seeds produced by the probability of survival, we can now calculate the expected reproductive success (the number of surviving offspring produced per plant) for plants producing seeds of a given size in both the wet and dry environments (Figure 4).

In wet environments, where all seed sizes have comparable probabilities of survival, the strategy of producing many small seeds results in the highest reproductive success and fitness. In contrast, the greater probability of survival makes the strategy of producing large seeds the most successful in dry environments, even though far fewer seeds are produced.

Interpreting the trade-offs observed in life history characteristics, such as the one illustrated between seed size and the number of seeds produced, requires understanding how those trade-offs function in the context of the environment (both biotic and abiotic) in which the species lives. Costs and benefits of a trait can change as the environmental conditions change. The diversity of life history traits exhibited by species is testimony that there is no single “best” solution for all environmental conditions.

1. In the example just presented, natural selection should favor plants producing small seeds in wet environments and plants that produce larger seeds in dry environments, resulting in a difference in average seed size in these two environments. What might you expect in an environment where annual rainfall is relatively high during most years (wet) but in which periods of drought (dry) commonly persist for several years?

2. The seeds of shade-tolerant plant species are typically larger than those of shade-intolerant species. How might this difference reflect a trade-off in life history characteristics relating to successful reproduction in sun and shade environments? See the discussion of shade tolerance in Chapter 6 and the Field Studies feature in that chapter.

10.9 An Individual’s Life History Represents the Interaction between Genotype and the Environment

Natural selection acts on phenotypic variation among individuals within the population and variation in life history characteristics, such as age at maturity, allocation to reproduction, and the average number and size of offspring produced, is common among individuals within a population (see Chapter  5). The observed phenotypic variation within populations can arise from two sources: genotypic variation among individuals and interactions between the genotype and environment. Recall that most phenotypic traits are influenced by the environment; that is to say, the phenotypic expression of the genotype is influenced by the environment (see Chapter 5, Section 5.4). The ability of a genotype to give rise to different phenotypic expressions under different environmental conditions is termed phenotypic plasticity, and the set of phenotypes expressed by a single genotype across a range of environmental conditions is referred to as the norm of reaction (see Figure 5.4). Just as with the examples of phenotypic plasticity related to physiological, morphological, and behavioral characteristics involved in the thermal, energy, and water balance of plants and animals, the characteristics related to life history also exhibit reaction norms as a result of interactions between genes and environment (see Chapters 6 and 7). One life history trait that has received a great deal of focus regarding response to environmental variation is the relationship between age and size at maturity.

Let’s begin by examining the expected patterns of size and age at maturity for a given genotype. Figure 10.17 shows the graph of a growth curve for a hypothetical fish species that under the best of conditions can mature at two years of age and at a weight of 4 kilograms (kg). Now let us change the environmental conditions by reducing the availability of food. The result is a slower rate of growth (Figure  10.17). The question now becomes when would the initiation of reproduction (onset of maturity) maximize fitness for the slow-growing fish? There are three possible ways to go. First, individuals could always mature at the same size (blue line in Figure  10.17). The problem with this approach is that it now requires an additional four years to reach maturity, increasing the probability of mortality before the individual has the opportunity to breed (blue dashed line). The second approach is to always mature at the same age (green line in Figure 10.17). This approach also presents a downside; now the individual would weigh only 1.75 kg and smaller individuals produce fewer offspring (green dashed line). Somewhere between these two approaches is a compromise between the increased costs represented by the increased risk of mortality and that of reduced fecundity. The species could evolve to possess a norm of reaction for age and size at maturity (red line in Figure  10.17). The optimal solution for any growth rate would depend on the relationship between size and fecundity and the age-specific patterns of juvenile mortality.

Nicolas Tamburi and Pablo Martin of the Universidad Nacional del Sur in Argentina examined patterns of phenotypic plasticity in the age and size at maturity in the freshwater applesnail (Pomacea canaliculata) native to South America. It has a broad geographic range, and its local populations exhibit variation in life history traits. In their experiments, the researchers reared full sibling snails in isolation under a gradient of seven different levels of food availability determined by size-specific ingestion rates. The reaction norms for age and size at maturity for both male and female snails are presented in Figure  10.18. They show a marked difference between males and females. Males showed less variation in age at maturity but a wide variation in shell size. Size is largely irrelevant in gaining access to females, and male fitness can be maximized through fast maturation at the expense of size at maturity. In contrast, a minimum size is required for females to reach maturity, so there is a much greater variation in age at maturity rather than size. In both cases, the reaction norms reflect a trade-off between age and size at maturity. The differences between the reaction norms of males and females reflect basic differences in the trade-offs between the sexes as they relate to fitness.

10.10 Mating Systems Describe the Pairing of Males and Females

In all sexually reproducing species there is a social framework involving the selection of mates. The pattern of mating between males and females in a population is called the mating system (also see Chapter 5). The structure of mating systems in animal species ranges from monogamy, which involves the formation of a lasting pair bond between one male and one female, to promiscuity, in which males and females mate with one or many of the opposite sex and form no pair bond. The primary mating systems in plants are outcrossing (cross-fertilization in which pollen from one individual fertilizes the ovum of another) and autogamy (self-fertilization). However, a mixed mating system, in which plants use both outcrossing and autogamy, is common.

The mating system of a species has direct relevance to its life history because it influences allocation to reproduction, particularly in males. Competition among males for mates, courtship behavior, territorial defense, and parental care (feeding and protection of offspring) can represent a significant component of reproductive allocation. In addition, we shall see that the degree of parental care differs among mating systems and parental care has a direct effect on offspring survival. As such, a mating system is both influenced by and influences age-specific patterns of fecundity and mortality.

Monogamy is most prevalent among birds and rare among mammals, except for several carnivores, such as foxes (Vulpes spp.) and weasels (Mustela spp.), and a few herbivores, such as the beaver (Castor spp.), muskrat (Ondatra zibethica), and prairie vole (Microtus ochrogaster). Monogamy exists mostly among species in which cooperation by both parents is needed to raise the young successfully. Most species of birds are seasonally monogamous (during the breeding season) because most young birds are helpless at hatching and need food, warmth, and protection. The avian mother is no better suited than the father to provide these needs. Instead of seeking other mates, the male can increase his fitness by continuing his investment in the young. Without him, the young carrying his genes may not survive. Among mammals, the situation is different. The females lactate (produce milk), which provides food for the young. Males often contribute little or nothing to the survival of the young, so it is to their advantage in terms of fitness to mate with as many females as possible. Among the mammalian exceptions, the male provides for the female and young and defends the territory (area defended for exclusive use and access to resources; see Section 11.10 for discussion). Both males and females regurgitate food for the weaning young.

Monogamy, however, has another side. Among many species of monogamous birds, such as bluebirds (Sialia sialis), the female or male may “cheat” by engaging in extra-pair copulations while maintaining the reproductive relationship with the primary mate and caring for the young. By engaging in extra-pair relationships, the female may increase her fitness by rearing young sired by two or more males. The male increases his fitness by producing offspring with several females.

Polygamy is the acquisition of two or more mates by one individual. It can involve one male and several females or one female and several males. A pair bond exists between the individual and each mate. The individual having multiple mates—male or female—is generally not involved in caring for the young. Freed from parental duty, the individual can devote more time and energy to competition for more mates and resources. The more unevenly such crucial resources as food or quality habitat are distributed, the greater the opportunity for a successful individual to control the resource and several mates.

The number of individuals of the opposite sex an individual can monopolize depends on the degree of synchrony in sexual receptivity. For example, if females in the population are sexually active for only a brief period, as with the white-tailed deer, the number a male can monopolize is limited. However, if females are receptive over a long period of time, as with elk (Cervus elaphus), the size of a harem a male can control depends on the availability of females and the number of mates the male has the ability to defend.

Environmental and behavioral conditions result in various types of polygamy. In polygyny, an individual male pairs with two or more females. In polyandry, an individual female pairs with two or more males. Polyandry is interesting because it is the exception rather than the rule. This system is best developed in three groups of birds: the jacanas (Jacanidae; Figure  10.19), phalaropes (Phalaropus spp.), and some sandpipers (Scolopacidae). The female competes for and defends resources essential for the male and the males themselves. As in polygyny, this mating system depends on the distribution and defensibility of resources, especially quality habitat. The female produces multiple clutches of eggs, each with a different male. After the female lays a clutch, the male begins incubation and becomes sexually inactive.

The nature and evolution of male–female relationships are influenced by environmental conditions, especially the availability and distribution of resources and the ability of individuals to control access to resources. If the male has no role in feeding and protecting the young and defends no resources available to them, the female gains no advantage by remaining with him. Likewise, the male gains no increase in fitness by remaining with the female. If the habitat were sufficiently uniform, so that little difference existed in the quality of territories held by individuals, selection would favor monogamy because female fitness in all habitats would be nearly the same. However, if the habitat is diverse, with some parts more productive than others, competition may be intense, and some males will settle on poorer territories. Under such conditions, a female may find it more advantageous to join another female in the territory of the male defending a rich resource than to settle alone with a male in a poorer territory. Selection under those conditions will favor a polygamous relationship, even though the male may provide little aid in feeding the young.

10.11 Acquisition of a Mate Involves Sexual Selection

For females, the production and care of offspring represents the largest component of reproduction expenditure. For males, however, the acquisition of a mate is often the major energetic expenditure that influences fitness.

The flamboyant plumage of the peacock (Figure 10.20) presented a troubling problem for Charles Darwin. Its tail feathers are big and clumsy and require a considerable allocation of energy to grow. They are also conspicuous and present a hindrance when a peacock is trying to escape predators. In the theory of natural selection, what could account for the peacock’s tail? Of what possible benefit could it be (see Chapter  5)?

In his book The Descent of Man and Selection in Relation to Sex, published in 1871, Darwin observed that the elaborate and often outlandish plumage of birds and the horns, antlers, and large size of polygamous males seemed incompatible with natural selection. To explain why males and females of the same species often differ greatly in body size, ornamentation, and color (referred to as sexual dimorphism), Darwin developed a theory of sexual selection. He proposed two processes to account for these differences between the sexes: intrasexual selection and intersexual selection.

Intrasexual selection involves male-to-male (or in some cases, female-to-female) competition for the opportunity to mate. It leads to exaggerated secondary sexual characteristics such as large size, aggressiveness, and organs of threat, such as antlers and horns (Figure 10.21), that aid in competition for access to mates.

Intersexual selection involves the differential attractiveness of individuals of one sex to another (see this chapter, Field Studies: Alexandra L. Basolo). In the process of intersexual selection, the targets of selection are characteristics in males such as bright or elaborate plumage, vocalizations used in sexual displays, and the elaboration of some of the same characteristics related to intrasexual selection (such as horns and antlers). It is a form of assortative mating in which the female selects a mate based on specific phenotypic characteristics (see Section  5.7). There is intense rivalry among males for female attention. In the end, the female determines the winner, selecting an individual as a mate. The result is an increase in relative fitness for those males that are chosen, shifting the distribution of male phenotypes in favor of the characteristics on which female choice is based (see Chapter  5). But do characteristics such as bright coloration, elaborate plumage, vocalizations, or size really influence the selection of males by females of the species?

Marion Petrie of the University of Newcastle, England, conducted some experiments to examine intersexual selection in peacocks (Pavo cristatus). She measured characteristics of the tail feathers (referred to as the train) of male peacocks chosen by females as mates over the breeding season. Her results show that females selected males with more elaborate trains. In particular, she found a positive correlation between the number of eyespots a male had on his train (see Figure 10.20c) and the number of females he mated with. She then altered the tail feathers from a group of males with elaborate trains and found that reduction in the number of eyespots led to a reduction in mating success.

However, the train itself is not what is important; it is what the elaborate tail feathers imply about the individual. The large, colorful, and conspicuous tail makes the male more vulnerable to predation, or in many other ways, reduces the male’s probability of survival. A male that can carry these handicaps and survive shows his health, strength, and genetic superiority. Females showing preference for males with elaborately colored tail feathers produce offspring that carry genes for high viability. Thus, the selective force behind the evolution of exaggerated secondary sexual characteristics in males is preferred by females. In fact, later experiments by Petrie found that the offspring of female peacocks that mated with males having elaborate tail feathers had higher rates of survival and growth than did the offspring of those paired with males having less elaborate trains (Figures 10.20a and 10.20b). A similar mechanism may be at work in the selection of male birds with bright plumage. One hypothesis proposes that only healthy males can develop bright plumage. There is evidence from some species that males with low parasitic infection have the brightest plumage. Females selecting males based on differences in the brightness of plumage are in fact selecting males that are the most disease resistant (for example, see Section 15.7).

In some animal species, male vocalizations play an important role in courtship behavior, and numerous studies have found evidence of female mate choice based on the complexity of a male’s song. In aviary studies, Myron Baker and colleagues at the University of Trondheim (Norway) found that female great tits (Parus major) were more receptive of males with more varied or elaborate songs (Figure 10.22).

In a 20-year study of song sparrows (Melospiza melodia) inhabiting Mandarte Island, British Columbia (Canada), Jane M. Reid of Cambridge University (England) and colleagues found that males with larger song repertoires were more likely to mate and that repertoire size predicted overall measures of male and offspring fitness. Males with larger song repertoires contributed more independent offspring—those hatching and reaching independence from parental care—and recruited offspring into the breeding population on the island; furthermore, those males also contributed more independent and recruited grand-offspring to the island population (Figure 10.23). This was because these males lived longer and reared a greater proportion of hatched chicks to independence from parental care, not because females mated to males with larger repertoires laid or hatched more eggs. Furthermore, independent offspring of males with larger repertoires were more likely to recruit and then to leave more grand-offspring than were offspring of males with small repertoires.

Field Studies Alexandra L. Basolo

School of Biological Sciences, University of Nebraska–Lincoln

The elaborate and often flamboyant physical traits exhibited by males of many animal species—bright coloration, exceedingly long feathers or fins—have always presented a dilemma to the traditional theory of natural selection. Because females in the process of mate selection often favor these male traits, sexual selection (see Section 10.11) will reinforce these characteristics. However, male investment in these traits may also reduce the amount of energy available for other activities that are directly related to individual fitness, such as reproduction, foraging, defense, predator avoidance, and growth. The effect of such trade-offs in energy allocation on the evolution of animal traits is the central focus of ecologist Alexandra L. Basolo’s research, which is changing how behavioral ecologists think about the evolution of mate selection.

Basolo’s research focuses on the small freshwater fishes of the genus Xiphophorus that inhabit Central America. One group of species within this genus, the swordtail fish, exhibits a striking sexual dimorphism in the structure of the caudal fin. Males have a colorful, elongated caudal appendage, which is termed the sword ( Figure 1 ), which is absent in females. This appendage appears to play no role other than as a visual signal to females in the process of mate selection. To test the hypothesis that this trait results partly from female choice (intersexual selection), Basolo undertook a series of laboratory experiments to determine if females exhibited a preference for male sword length. Her test subject was the green swordtail, Xiphophorus helleri, shown in Figure 1. These experiments allowed females to choose between a pair of males differing in sword length. Five tests with different pairs of males were conducted in which the sword differences between paired males varied. Female preference was measured by scoring the amount of time a female spent in association with each male.

Results of the experiments revealed that females preferred males with longer swords. The greater the difference in sword length between two males, the greater was the difference in time that the female spent with them (Figure 2). The results suggest that sexual selection through female choice will influence the relative fitness of males. The benefit of having a long sword is the increased probability of mating. But what is the cost? Locomotion accounts for a large part of the energy budget of fish, and the elongated caudal fin (sword) of the male swordtails may well influence the energetic cost of swimming. The presence of the sword increases mating success (via female choice) but may well negatively affect swimming activities.

To evaluate the costs associated with sword length, Basolo undertook a series of experiments using another species of swordtail, the Montezuma swordtail (Xiphophorus montezumae) found in Mexico. Like the green swordtail, the Montezuma swordtail males have an asymmetric caudal fin as a result of an extended sword, and the presence of this sword increases mating success. The experiments were designed to quantify the metabolic costs of the sword fins during two types of swimming—routine and courtship—for males with and without sword fins. Males having average-length sword fins were chosen from the population. For some of these males, the sword was surgically removed (excised). Comparisons were then made between males with and without swords for both routine (no female present) and courtship (female present) swimming. Male courtship behavior involves a number of active maneuvers. Routine swimming by males occurs in the absence of females, whereas the presence of females elicits courtship-swimming behavior.

Basolo placed test males into a respirometric chamber—a glass chamber instrumented to measure the oxygen content of the water continuously. For a trial where a female was present, the female was suspended in the chamber in a cylindrical glass tube having a separate water system. During each trial, water was sampled from the chamber for oxygen content to determine the rate of respiration. Higher oxygen consumption indicates a higher metabolic cost (respiration rate).

Results of the experiments show a significant energy cost associated with courtship behavior (Figure 3). A 30 percent increase in net cost was observed when females were present for both groups (males with and without swords) as a result of increased courtship behavior. However, the energy cost for males with swords was significantly higher than that for males without swords for both routine and courtship swimming behavior (Figure 3). Thus, although sexual selection via female choice favors long swords, males with longer swords experience higher metabolic costs during swimming, suggesting that sexual and natural selection have opposing effects on sword evolution.

The cost of a long sword to male swordtails extends beyond the energetics of swimming. Other studies have shown that more conspicuous males are more likely to be attacked by predators than are less conspicuous individuals. In fact, Basolo and colleague William Wagner have found that in green swordtail populations that occur sympatrically (together) with predatory fish, the average sword length of males in the population is significantly shorter than in populations where predators are not present. These results suggest that although sexual selection favors longer swords, natural selection may have an opposing effect on sword length in populations with predators.

Despite the cost, both in energy and probability of survival, the sword fin of the male swordtails confers an advantage in the acquisition of mates that must offset the energy and survival costs in terms of natural selection.

10.12 Females May Choose Mates Based on Resources

A female exhibits two major approaches in choosing a mate. In the sexual selection discussed previously, the female selects a mate for characteristics such as exaggerated plumage or displays that are indirectly related to the health and quality of the male as a mate. The second approach is that the female bases her choice on the availability of resources such as habitat or food that improve fitness.

Numerous studies have shown that in some species, mate choice by females appears to be associated with the acquisition of resources, usually a defended high quality habitat or territory (see Section 11.10). Ethan Temeles of Amherst College (Amherst, Massachusetts) and J. John Kress of the National Museum of Natural History (Smithsonian Institution, Washington, D.C.) found that female purple-throated carib hummingbirds (Eulampis jugularis) on the island of Dominica in the West Indies preferred to mate with males that had high standing crops of nectar on their flower territories (Figure  10.24). A male’s ability to maintain high nectar standing crops on his territory not only depended on the number of flowers in his territory but also on his ability to enhance his territory through the prevention of nectar losses to intruders.

Andrew Balmford and colleagues at Cambridge University (England) examined the distribution of females across male territories to assess mate choice in puku (Kobus vardoni) and topi (Damaliscus lunatus), which are two species of grazing antelope in southern Africa. In both species, males defend areas (territories) in which they have exclusive use of resources. Both species are polygamous, and visitation to territories by females was found to be a good predictor of where females tended to mate. In both species, female choice (visitation rate) was correlated with the quality of forage in different territories, indicating that female choice was influenced by the quality of defended resources.

10.13 Patterns of Life History Characteristics Reflect External Selective Forces

Nature presents us with a richness of form and function in the diversity of life that inhabits our planet. Some species are large, and others are small. Some mature early, and others mature later in their lives. Some organisms produce only a few offspring over their lifetime, whereas other species produce thousands in a single reproductive event. Some organisms fit an entire lifetime into a single season, and others live for centuries. Are the characteristics exhibited by any given species a random assemblage of these traits, or is there a discernable pattern? What we have seen so far is that these characteristics, which define the life history of an individual, are not independent of one another. These characteristics are products of evolution by natural selection, the possible outcomes molded by the external environment, and constrained by trade-offs relating to fundamental physiological and developmental processes. Ecologists have long recognized that the set of characteristics that define a species’ life history covaries, forming what appear to be distinctive “suites” of characteristics that seem to be a product of broad categories of selective forces. A number of empirical models have developed to account for the observed covariation among life history traits. One such model is the fast–slow continuum hypothesis.

The fast–slow continuum hypothesis emphasizes the selective forces imposed by mortality at different stages of the life cycle. Under this scheme, species can be arranged along a continuum from those experiencing high adult mortality levels to those experiencing low adult mortality. This differential mortality is responsible for the evolution of contrasting life histories on either end of the continuum. Species undergoing high adult mortality are expected to have a shorter life cycle (longevity) with faster development rates, early maturity, and higher fecundity than those experiencing low adult mortality. This approach has proven accurate in predicting patterns of life history characteristics in many groups of species and is generally consistent with the patterns presented in the preceding sections.

Other approaches to understanding the observed correlations among life history traits have focused on constraints imposed by the abiotic environment. If the life history characteristics and mating system exhibited by a species are the products of evolution, would they not reflect adaptations to the prevailing environmental conditions under which natural selection occurred? If this is the case, do species inhabiting similar environments exhibit similar patterns of life history characteristics? Do life history characteristics exhibit patterns related to the habitats that species occupy?

One way of classifying environments (or species habitats) relates to their variability in time. We can envision two contrasting types of habitats: (1) those that are variable in time or short-lived and (2) those that are relatively stable (long-lived and constant) with few random environmental fluctuations. The ecologists Robert MacArthur of Princeton University, E. O. Wilson of Harvard University, and later E. Pianka of the University of Texas used this dichotomy to develop the concept of r- and K-selection.

The theory of r- and K-selection predicts that species adapted to these two different environments will differ in life history traits such as size, fecundity, age at first reproduction, number of reproductive events during a lifetime, and total life span. Species popularly known as r-strategists are typically short-lived. They have high reproductive rates at low population densities, rapid development, small body size, large number of offspring (with low survival), and minimal parental care. They make use of temporary habitats. Many inhabit unstable or unpredictable environments that can cause catastrophic mortality independent of population density. Environmental resources are rarely limiting. They exploit noncompetitive situations. Some r-strategists, such as weedy species, have means of wide dispersal, are good colonizers, and respond rapidly to disturbance.

K-strategists are competitive species with stable populations of long-lived individuals. They have a slower growth rate at low populations, but they maintain that growth rate at high densities. K-strategists can cope with physical and biotic pressures. They possess both delayed and repeated reproduction and have a larger body size and slower development. They produce few seeds, eggs, or young. Among animals, parents care for the young; among plants, seeds possess stored food that gives the seedlings a strong start. Mortality relates more to density than to unpredictable environmental conditions. They are specialists—efficient users of a particular environment—but their populations are at or near carrying capacity (maximum sustainable population size) and are resource-limited. These qualities, combined with their lack of means for wide dispersal, make K-strategists poor colonizers of new and empty habitats.

The terms r and K used to characterize these two contrasting strategies related to the parameters of the logistic model of population growth (presented in Chapter 11); r is the per capita rate of growth, and K is the carrying capacity (maximum sustainable population size). Using the classification of r and K, strategies for comparing species across a wide range of sizes is of limited value. For example, the correlation among body size, metabolic rate, and longevity in warm-blooded organisms results in species with small body size generally being classified as r species and those with large body size as K species (see Chapter 7). The concept of r species and K species is most useful in comparing organisms that are either taxonomic or functionally similar.

The plant ecologist J. Phillip Grime of the University of Sheffield, England, used a framework similar to that used by MacArthur and Wilson to develop a life history classification for plants. Grime’s life history classification of plants is based on the assumption that any habitat can be classified into one of two categories: stress and disturbance. Stress is defined as conditions that restrict plant growth and productivity, such as shortages of light, water, mineral nutrients, or suboptimal temperatures (see Chapter 6). Disturbance is associated with the partial or total destruction of plant biomass that arises from the activity of herbivores, pathogens, or natural disasters such as wind, fire, or flooding. When the four permutations of high and low stress couple with high and low disturbance, it is apparent that only three are suitable as habitat for plants, because in highly disturbed environments, stress does not allow for the reestablishment of plant populations. Grime suggests that the remaining three categories of habitat are associated with the evolution of distinct types of plant life history strategies—R, C, and S (Figure 10.25). Species exhibiting the R, or ruderal, strategy rapidly colonize disturbed sites. These species are typically small in stature and short-lived. Allocation of resources is primarily to reproduction, with characteristics allowing for a wide dispersal of seeds to newly disturbed sites. Predictable habitats with abundant resources favor species that allocate resources to growth, favoring resource acquisition and competitive ability (C species). Habitats in which resources are limited favor stress-tolerant species (S species) that allocate resources to maintenance. These three strategies form the end points of a triangular classification system that allows for intermediate strategies, depending on resource availability (levels of stress) and frequency of disturbance (Figure 10.26).

Ecological Issues & Applications The Life History of the Human Population Reflects Technological and Cultural Changes

The history of the human population presents what appears to be a classic example of exponential population growth, yet on closer inspection, what emerges is a story of a species that has redefined its life history through a series of technological, cultural, and economic changes over the past two centuries.

With the end of the last glacial period (~18,000 bp) and the development of agriculture some 10,000 years ago, human demographers estimate that the human population was approaching 5 million. By 1 ad the population had risen to approximately 250 million, and it would take until the beginning of the 19th century before that number would reach a billion. By the 19th century, the human population entered a period of expansive growth, rising to 2 billion by 1930. Adding the next billion would take only 30 years (1960), and on October 31, 2011, the United Nations officially declared that the human population had reached 7 billion.

So what are the prospects for the future? The United Nations’ projection of future population growth shows the global population continuing to expand over the next several decades before peaking near 10 billion later in the 21st century. Although this may appear as an astonishingly large number, it represents a significant decline in population growth rates moving forward and the possibility of population numbers stabilizing in the foreseeable future.

When combined with projections of future growth over the next century, it becomes apparent the human population is not following a continuous pattern of exponential growth. Rather, the graph of the human population presented in Figure  10.27 suggests three distinct periods, or phases, of population growth in modern time (19th century forward). In phase 1, the period before the early 20th century, population growth is slow and steady. By the early 20th century, however, Phase 2 began, which was a period of dramatic exponential growth. This period of growth continued until the latter part of the 20th century when the population growth rate began to slow. We have now entered Phase 3 as the population growth rate declines and the population potentially peaks at 10 billion.

What has caused these three phases? Why did the population growth rate explode in the early 20th century, and what caused it to decline as the 20th century came to a close? These three phases of population growth are the central components of what human demographers—ecologists who study the human population—refer to as the demographic transition. The demographic transition describes the transition from high birthrates and death rates to low birthrates and death rates as countries move from a preindustrial to an industrialized social and economic system (Figure 10.28).

Phase 1 is associated with premodern times and is characterized by a balance between high rates of birth and death. This was the situation of the human population before the late 18th century. This balance between birthrate and death rate resulted in a slow growth rate (<0.05 percent). Death rates were high because of the lack of sanitation, knowledge of disease prevention and cures, and occasional food shortages (usually climate related). The infant mortality rate in the United Kingdom and the United States during the 18th century was as high as 500 per 1000, or one in every two infants born. With high child mortality rates, there was little incentive in rural societies to control fertility.

By the early 19th century death rates began to decline, first in Europe and then in other countries, over the next 100 years. The decline in death rates would lead to Phase 2 of the transition characterized by exponential growth as the population growth rate rose (difference between birthrate and death rate increased; see Figure 10.28).

The decline was a result of improved food supply and sanitation (particularly water supplies). This decline gained momentum in the early 20th century with significant improvements in public health. Improved sanitation and the identification of causes of and cures for infectious diseases led to a dramatic decline in death rates as the 20th century progressed. The greatest reduction in death rates was realized by children; infant mortality rates declined steadily in the 20th century ( Figure  10.29). The reduced infant mortality rates had a swift and dramatic effect on population growth rates. Increases in life expectancy for older individuals (post-reproductive) has little effect on population growth rates; in contrast, increased survival rate of infants results in those individuals entering the reproductive ages and adding to overall population growth (see Section 9.7).

Phase 3 of the transition moved the population toward stability through a decline in birthrates. This phase began as early as the end of the 19th century in northern Europe and then spread to other places over the next several decades ( Figure  10.30). In the second half of the 20th century, birthrates declined, and by the early 1960s, the world population growth rate peaked at more than 2 percent and has been declining ever since. The number of new individuals added to the global population each year peaked in the 1990s.

There are a number of factors that contributed to this decline, although many of them remain speculative and are the focus of continued research by social scientists. In rural areas where children played an important role in farm life, the continued decline in infant mortality meant that at some point parents realized the need to control family size. Likewise, increased urbanization changed the traditional value of large family size that was essential to farm life. The increased role of women in the workforce and the improvements to contraception in the second half of the 20th century led to even further declines in birthrates, and by the early 1960s the world population growth rate had peaked at slightly more than 2 percent.

So begins Phase 3 of the transition. The global population growth rate has been declining since its peak in the 1960s and the number of new individuals added to the global population each year peaked in the 1990s. Demographic transition describes the patterns of human population growth for all regions of the planet, but the timing of the transition has differed for different regions. The more industrialized economies began the transition earlier, with many countries in Western Europe and Asia, such as Poland, Germany, and Japan, now exhibiting a negative growth rate. In contrast, many of the developing countries of the world are still in the mid to latter phases of Phase 2, exhibiting growth rates that still exceed 2 percent.

From an ecological perspective, the amazing point of the demographic transition is that it represents a modification of the life history of our species, not as a result of natural selection but by means of “social evolution.” Humans have dramatically altered age-specific patterns of birth and death through changes in technology and cultural changes that have occurred as the social structure has changed from rural agrarian to industrial urbanized society.

Summary

Trade-offs 10.1

Organisms face trade-offs in life history characteristics related to reproduction. Trade-offs are necessitated by the constraints of physiology, energetics, and the prevailing physical and biotic environment. Trade-offs involve conflicting demands on resources or negative correlation among traits.

Asexual and Sexual Reproduction 10.2

Fitness is an organism’s ability to leave behind reproducing offspring. Organisms that contribute the most offspring to the next generation are the fittest. Reproduction can be asexual or sexual. Asexual reproduction, or cloning, results in new individuals that are genetically the same as the parent. Sexual reproduction combines egg and sperm in a diploid cell, or zygote. Sexual reproduction produces genetic variability among offspring.

Forms of Sexual Reproduction 10.3

Sexual reproduction takes a variety of forms. Plants with separate males and females are called dioecious. An organism with both male and female sex organs is hermaphroditic. Plant hermaphrodites have bisexual flowers, or if they are monoecious, separate male and female flowers on the same individual. Some plants and animals change sex.

Benefits and Costs 10.4

The behavioral, physiological, and energetic activities involved in reproduction represent a cost to future reproductive success of the parent in the form of reduced survival, fecundity, or growth.

Age at Maturity 10.5

Natural selection favors the age at maturity that results in the greatest number of offspring produced over the lifetime of an individual. Environmental factors that result in reduced adult survival select for earlier maturation, and conversely, environmental factors that result in reduced juvenile survival relative to that of adults select for delayed maturation.

Reproductive Effort 10.6

Optimal reproductive effort represents a trade-off between current and future reproduction. Allocation to current reproduction functions to increase current fecundity but reduces parental survival, resulting in decreased future reproduction. Fitness is often maximized by an intermediate reproductive effort, particularly for organisms that reproduce repeatedly over their life spans.

Number and Size of Offspring 10.7

Organisms that produce many offspring have a minimal investment in each offspring. They can afford to send a large number into the world with a chance that a few will survive. By so doing, they increase parental fitness but decrease the fitness of the young. Organisms that produce few young invest considerably more in each one. The fitness of the young of such organisms is increased at the expense of the fitness of the parents.

Timing of Reproduction 10.8

To maximize fitness, an organism balances immediate reproductive efforts against future prospects. One alternative, semelparity, is the investment of maximum energy in a single reproductive effort. The other alternative, iteroparity, is the allocation of less energy to repeated reproductive efforts.

Reaction Norms 10.9

The characteristics related to life history, such as age at maturity, exhibit reaction norms (phenotypic plasticity) as a result of the interaction between genes and the environment.

Mating Systems 10.10

The pattern of mating between males and females in a population is the mating system. In animal species, mating systems range from monogamy to promiscuity.

Sexual Selection 10.11

In general, males compete with males for the opportunity to mate with females, but females finally choose mates. Sexual selection favors traits that enhance mating success, even if it handicaps the male by making him more vulnerable to predation. Male competition represents intrasexual selection, whereas intersexual selection involves the differential attractiveness of individuals of one sex to the other. By choosing the best males, females ensure their own fitness.

Resources and Mate Selection 10.12

Females may also choose mates based on the acquisition of resources, usually a defended territory or habitat. By choosing a male with a high-quality territory, the female may increase her fitness.

Life History Strategies 10.13

The set of characteristics that define a species’ life history covary, forming what appear to be distinctive suites of characteristics that seem to be a product of broad categories of selective forces. A number of hypotheses have been developed to explain these patterns. The fast–slow continuum hypothesis says that species can be arranged along a continuum from high to low adult mortality. High adult mortality results in selection for a shorter life cycle, faster development rates, and higher fecundity than populations experiencing low adult mortality. Another hypothesis is based on two contrasting types of habitats: those that are variable in time or short-lived and those that are relatively stable. The former habitat type creates selection pressure for short life cycle, fast development, and high reproductive rates, and high fecundity, and the latter for longevity, delayed maturity, and lower reproductive effort distributed over a longer period of time.

Human Life History Ecological Issues & Applications

The history of the human population is described by the transition from high birthrates and death rates to low birthrates and death rates as countries move from a preindustrial to an industrialized social and economic system This dynamic is known as the demographic transition and represents a modification of the life history of our species, not as a result of natural selection, but by means of “social evolution.”