8 Population Biology of the Elderly

James R. Carey and Catherine Gruenfelder

Introduction

An important, yet widely overlooked incongruity in ecological and evolutionary literature concerns the gap between the emphasis on understanding age-structured populations (Caswell, 1989; Charlesworth, 1994) and the elderly as a subgroup of the population. This disparity implies that age structure is important, but only within a restricted subset of younger age classes. Indeed, the elderly are often viewed as expendable and thus as possessing little real or potential ability to contribute to the fitness of the population (Williams, 1957).

There are several likely reasons for historical neglect of the elderly in behavioral ecology literature. First, it is widely known from field life tables that most individuals in the wild die young and even fewer survive to older ages (Deevey, 1947). Thus, it is argued that their role is negligible, since the elderly subgroup of animals in the wild is not only frail but also is only a small minority of the total population.

Second, the evolutionary theory of aging (Williams, 1957) suggests that older individuals contribute little to fitness of populations because, according to the Lotka model (Lotka, 1907), the force of selection decreases with age (Rose, 1991; Kirkwood, 1985). One of the problems with the use of the Lotka model to define fitness is that it does not consider some situations where the elderly may contribute substantially to the fitness of the population. For example, it does not consider circumstances in which only older adults, particularly females, overwinter and regenerate the population in the spring (Izquierdo, 1991), in which the elderly provide infant care, or in which the older matriarchs or patriarchs provide critical leadership and cohesion.

Third, senility is often used as the physical and behavioral criterion for defining and identifying the elderly in the wild—i.e., those individuals that are decrepit, moribund, and near death. Unfortunately, this anecdotal "aging" of wild individu-



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8 Population Biology of the Elderly James R. Carey and Catherine Gruenfelder Introduction An important, yet widely overlooked incongruity in ecological and evolutionary literature concerns the gap between the emphasis on understanding age-structured populations (Caswell, 1989; Charlesworth, 1994) and the elderly as a subgroup of the population. This disparity implies that age structure is important, but only within a restricted subset of younger age classes. Indeed, the elderly are often viewed as expendable and thus as possessing little real or potential ability to contribute to the fitness of the population (Williams, 1957). There are several likely reasons for historical neglect of the elderly in behavioral ecology literature. First, it is widely known from field life tables that most individuals in the wild die young and even fewer survive to older ages (Deevey, 1947). Thus, it is argued that their role is negligible, since the elderly subgroup of animals in the wild is not only frail but also is only a small minority of the total population. Second, the evolutionary theory of aging (Williams, 1957) suggests that older individuals contribute little to fitness of populations because, according to the Lotka model (Lotka, 1907), the force of selection decreases with age (Rose, 1991; Kirkwood, 1985). One of the problems with the use of the Lotka model to define fitness is that it does not consider some situations where the elderly may contribute substantially to the fitness of the population. For example, it does not consider circumstances in which only older adults, particularly females, overwinter and regenerate the population in the spring (Izquierdo, 1991), in which the elderly provide infant care, or in which the older matriarchs or patriarchs provide critical leadership and cohesion. Third, senility is often used as the physical and behavioral criterion for defining and identifying the elderly in the wild—i.e., those individuals that are decrepit, moribund, and near death. Unfortunately, this anecdotal "aging" of wild individu-

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als is subject to substantial error. Only in the last several decades have detailed longitudinal data been systematically gathered on individuals of known ages and greater emphasis been placed on understanding age structure of populations (Finch and Ricklefs, 1991). Researchers have found that the variability in the rate of aging in wild animals is as great as that in humans, and in most species, it is virtually impossible to determine the exact age of an individual by its appearance or a biomarker. This is particularly true at older ages. Indeed, "physiologic heterogeneity" is a consistent characteristic of the elderly population (Timiras, 1994). The broad objective of this paper is to extract important facts about aging and social and community structure in nonhumans and to reassemble them on a foundation of ecology and population biology. Just as certain morphological traits in animals, such as antler type, leg length, wing shape, visual acuity, gut length, and ear design, have been successfully related to the ecology and life histories of different animal species, we expect longevity and mortality patterns to be interpretable in the same context. We believe that this approach will provide insight into questions such as: What aspects of natural history favor the evolution of greater longevity? To what extent is life span a function of ecology and social structure? Is slowing of mortality at older ages a consequence of selection for certain adaptive traits at younger ages? We organized this paper into three broad sections and a discussion. In the first section we introduce foundational principles we believe are important for understanding the relationship between longevity and life history of animals. These include biodemographic concepts and behavioral characteristics, such as altruism, dominance, territoriality, learning, and culture. In the second section we present a synopsis of roles and life histories of the elderly in three selected animal groups, including elephants, cetaceans, and primates, to provide specific biological context. In the third section we explore the concept of extended longevity as a preadaptation for the evolution of eusociality in wasps. This concept is important because it broadens the evolutionary scope from microevolution, as is discussed by Rose (1991) and Kirkwood (1985), to macroevolution concerned with speciation and the evolution of broad taxonomic groups (Strickberger, 1996). In the discussion we attempt to synthesize the general findings of the natural history and roles of the elderly, discuss some common life-history patterns associated with extended life span, and suggest future directions. Foundational Concepts The Elderly: An Integration of Biodemographic Concepts Defining the Elderly Life span of animals is not an orderly unfolding of precisely timed events from fertilization to death, with the elderly as a distinct, definitive stage. There exists no objective physiological landmark for aging, such as occurs with sexual

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Figure 8-1  Physical and reproductive fitness generally peak during middle age and tend to steadily decline throughout the elderly stage (shown here to be the last third of the life course). maturation in most animals. Its onset occurs at some indeterminate point following maturity, and its progression follows timetables that differ with each individual (Timiras, 1994). Consequently, a consistent characteristic of the elderly in nature is the wide range of frailty and robustness; therefore, it is impossible to specify for any species the age at which the elderly stage begins. However, as an operational definition, we consider the elderly in nature as those individuals who survive to the later half to third of the life span (Figure 8-1). Perhaps a more realistic framework, but one that would not serve the current purposes, would be to consider functional, rather than chronological, markers to define old age (Silverstone, 1996). Life-Course Premises Many of the premises outlined by Riley (1979) for the life course and demography of older humans are general and thus relevant for understanding the life course, population dynamics, and aging of populations for any species. These premises are as follows: (1) Aging for all animals is a continual process of development, maturation, and growing old. Thus, no single stage of an individual's life can be understood apart from its antecedents and consequences. (2) Aging consists of several sets of processes, including biological, social, and

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experiential processes, all of which are systematically interactive over the life course. (3) The life-course pattern of any particular individual is affected by changes in the group and in the environment. (4) Not all individuals survive to old age. However, the importance of the elderly to the overall dynamics and welfare of the population may be disproportionately greater than their numbers. Consequences of Long Life Long life has several consequences for individuals in animal populations (Riley and Riley, 1986). First, long life prolongs opportunity to accumulate social and biological experiences. For example, long-lived individuals in social species may possess unique knowledge, such as the location of water during a drought or how to manufacture and use tools. Second, long life maximizes an individual's opportunities to complete or to change role "assignments." For example, a long-lived animal can ascend, lose, and re-attain alpha status within a troop, serve as a grandparent "caregiver"; become a forager after having been a colony "nurse"; become a breeder, by inheriting breeding territory, rather than remain a nest helper. Third, greater longevity prolongs an individual's relationships to others, including mates, parents, offspring, and associates. This feature increases the structural complexity of an individual's social networks, such as kinships, alliances, and communities. For example, when a monogamous pair of birds survives over multiple years, the relationship can become highly complex, leading to large clutch sizes and increased breeding success not seen in short-lived species (Coulson, 1966). In general, these consequences demonstrate that longer-lived individuals can significantly influence change within their group. Relevant Behavioral Principles The elderly often exhibit behaviors fundamental to behavioral ecology. This section provides background on several of these concepts that frequently appear in literature on the elderly and thus are basic to understanding the broader nature of the roles of elderly individuals. Altruism Altruism, defined by Wilson (1975) as "self-destructive behavior performed for the benefit of others," is relevant to understanding the role of the elderly in nature in several social contexts, including care-giving, allomothering, group defense, and nest care. Altruism is also apparent among the elderly in some nonsocial species. For example, altruism is demonstrated by older, foul-tasting Saturnid moths that sacrifice themselves to "teach" predators that younger counterparts are repugnant (Blest, 1963). Hamilton (1964) proposed the primary theoretical background for explaining the evolution of altruistic behavior. Hamilton's theory based altruism on the

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fundamental kinship relations of donor and recipient (Rosenberg, 1992). Altruism has since been generalized to include any form of nonselfish behavior and serves as the cornerstone for much of sociobiology (Wilson, 1975). In this sense, altruistic behavior includes care-giving to kin other than an individual's direct offspring. Feeding, protecting, warning, defending, and teaching kin, in proportion to their consanguinity, emerges as an adaptationally optimal strategy for older individuals. Many forms of altruism are evident within social species. Maxim (1979) lists four altruistic roles of aging in primates: (1) defense of territory, (2) defense against predation, (3) control of troop movement, and (4) aunt behavior. These activities are of little or no direct benefit to the elderly individuals but do serve to directly benefit the kinship community. Further, Medawar (1957) comments that altruistic behavior of grandparents should be indirectly selected for because, although grandparents are infertile and their behavior is of no benefit to themselves, "grandmotherly indulgence" does benefit the community. Hamilton (1966) also proposed that postreproductive life spans may have evolved when the older animal benefits its younger kin. For example, old postreproductive female langurs ardently defend their troops and protect troop infants to a much greater degree than younger females (Hrdy, 1981). Also, Norris and Pryor (1991) suggest that many postreproductive, yet still lactating, females in dolphin societies may be present as a source of nourishment to offspring of younger mothers while those mothers dive to great depths for prey. Diamond (1996) supports the occurrence of altruistic postreproductive females by stating that aging human females can, evidently, "do more to increase the number of people bearing her genes by devoting herself to her existing children, her potential grandchildren, and her other relatives than by producing yet another child." An example of altruism in a nonsocial species is given by Blest (1963). Blest found that cryptic New World Saturnid moths, which rely on camouflage to escape detection but are quite palatable to predators, die shortly after completing reproduction. The aposematic subgroup of New World Saturnid moths, which rely on their terrible taste to discourage predators, exhibit a long postreproductive period. Postreproductive survival of the tasty moths is detrimental to conspecifics because a predator can establish a search image of the cryptic species by feeding on palatable individuals. However, a predator's unpleasant experience with an aposematic individual would benefit its kin and other conspecifics. Thus, Blest argued that the sustained physical fitness of postreproductive aposematic moths contributes to the survival of the younger reproductives. Dominance and Leadership To dominate is to possess priority of access to the necessities of life and reproduction (Wilson, 1975). Understanding the governance of animal societies by dominance hierarchies provides the fundamental basis for studying the behav-

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ioral dynamics of social groups. Because social groups are often headed by older individuals, such as in primate societies, it follows that understanding dominance relations is basic to understanding the role of the elderly in nature. Allee (1931) addressed the issue of stable hierarchies and argued that dominance hierarchies created cooperative groups that were better able to compete with other groups. One of the classic studies on chickens, from which the concept of ''pecking order" was derived, was by Guhl and Allee (1945), who found that chickens with stable hierarchies had individuals that consumed more food and laid more eggs than chickens without hierarchies. Dugatkin (1995) provides further support to this study by demonstrating that subordinate chickens do not challenge superiors but often prefer to wait their turn. Dugatkin shows that this complacency occurs not because subordinates fear damage and retribution but that group selection has "chosen" genotypes that will not contest authority. Closely related to dominance is leadership, which is initiative and control of an activity, usually by one individual. Whereas dominance alone suggests suppression of group activity, even though it may stabilize the social interactions, an individual who is also a leader can contribute to group survival by synchronizing and stimulating group activity (Greenberg, 1947). Wilson (1975) lists several "special properties" of dominance order that have important bearing on understanding the role of the elderly in social species. First, "the peace of strong leadership" refers to how dominant animals of some primate societies, including those of gorillas, chimpanzees, macaques, spider monkeys, and squirrel monkeys, use their power to terminate fighting among subordinates. Species organized by despotisms also live in peace due to the universally acknowledged power of the tyrant (e.g., the queen bumblebee). Second, "social inertia" refers to the intrinsic stability of a dominance hierarchy. An animal that attempts to change its position in a fixed dominance hierarchy is less likely to succeed than if it made the exertion during the formative, fluid stages of the hierarchy (Guhl, 1968). Third, societies structured as "nested hierarchies" are partitioned into units and exhibit dominance both within and between components. For example, in some primate societies, hierarchies exist both within and between family lines. Territoriality A territory is an area occupied either directly by overt defense or indirectly through advertisement (Wilson, 1975). This area usually contains a scarce resource (e.g., steady food supply, shelter, space for sexual display, a site for laying eggs or bearing offspring, etc.). The adaptive advantage of territorial behavior is that successful defense of a territory increases the chances of an individual to secure its necessary share of environmental resources, to mate, and to increase survival of offspring (Kluijver and Tinbergen, 1953). Individuals resident in an area have more to gain from retaining the territory than do intruders from taking

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it. This is true because residents invest a great deal of energy and time into mastering their area and resources and may well have dependent young. A challenger is devoid of these properties and thus has nothing to lose (Gosling, 1982). Age is virtually never the sole criterion for achieving dominance or acquiring territory. However, there is likely to be a strong association with age because of two factors. First, the territory holder almost always triumphs in one-on-one encounters. Therefore, territory holders often have held their territories for a long time and thus tend to be older. Second, there is a positive relationship between age and dominance of subordinates, who are continually competing for "next-inline" status. Learning and Culture Learning, defined as any change of behavior of individuals due to experience (Cavalli-Sforza and Feldman, 1981; Alcock, 1993), is found in virtually all animal species from the simplest bacteria and protozoa to complex mammals, such as cetaceans, primates, and elephants. The mechanisms of learning can occur at different levels. Self-teaching occurs when a young individual eats a food that tastes bad and subsequently avoids it. Birds acquire songs and repertoires through imitation. Teaching occurs when inexperienced young of predator species accompany their parents on a hunt to acquire skill. The cumulative learning experiences of groups constitute unique cultures that can often be transmitted from one generation to the next (Alcock, 1993). It is widely believed that selection favors specific learning abilities as solutions to specific ecological problems (Alcock, 1993). For example, solitary animals gain useful flexibility by adjusting their diets to whatever nourishment is available. Also, many animals that hoard food must remember where their food cache is located. The ability of social animals to adjust to the behavior of others (e.g., who is dominant to whom, what one individual did to another individual, etc.) may greatly affect their reproductive success (Alcock, 1993). Information that can only be transmitted through learning includes home range, migratory pathways, location of food sources, tool construction and use, acceptability of food items, parental-care skills, and social relationships, such as pair bonding and alliances (Bonner, 1980). The Elderly In Nature: Selected Case Studies Although there are few papers published on the elderly in nature, the biological literature contains a surprising amount of information on nonhuman elderly that has never been compiled and synthesized. The life history and field biology of a large number of endangered or economically important species in all major taxonomic groups has been studied and documented in meticulous detail. This includes longitudinal studies of marked individuals or monitoring, for decades,

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individuals in laboratories and in zoos. The purpose of this section is to introduce the concept of the role of the elderly in nature, using information extracted from the biological literature on elephants, cetaceans, and primates. We begin each subsection with background information on the biology and social structure of each group to provide ecological context for the information on aging and the roles of the elderly. Elephants Ecological Background Elephants belong to the order Proboscidea, which includes the extinct mastodon and mammoth. There are only two extant species, the African elephant and the Asian elephant, although there are a number of subspecies within each group (Estes, 1991). The African forest elephant lives in the West African rain forest, whereas the savanna race inhabits lowland forests, low-lying swamps, flood plains, and woodland. Elephants also live in subdesert terrain where gallery forest or neighboring mountains provide shade, browse, and water. These animals must frequently move large distances for food and water due to seasonal variations in food distribution and abundance. Elephants are mixed feeders, concentrating on grasses in the rainy season and on woody plants in the dry season (Buss, 1961, 1990). Thus, they wander widely across the savanna during the rains, yet remain near forest and water sources at other times. Both African and Asian elephants appear to have identical social structures, of which the family is the core unit (Figure 8-2). The family consists of closely related females, including the matriarch, several younger, yet mature, females, and their calves (Eltringham, 1982). Juvenile males remain with their group until they reach sexual maturity, at which time they are driven away by the matriarch (Buss, 1990). Adult males are either solitary or remain on the distant periphery of the herd. Elephant populations are migratory within large home ranges. Activity, direction, and rate of movement are determined by the matriarch, which is typically the largest (and oldest) cow. Typically, the matriarch leads the group, while another large (and old) female brings up the rear (Douglas-Hamilton, 1987). If disturbed, the group clusters around the matriarch awaiting instruction and protection. If the matriarch is shot, the family becomes a frantic, disorganized mob and, most often, falls prey to the same fate as their leader (Eltringham, 1982). Female leadership and experience play a crucial role in elephant social organization, and thus, female life span extends well past the reproductive years (Laws. 1970). Elephants do not exhibit seasonal breeding (Poole and Moss, 1989). A female elephant is in estrus for only 3 to 6 days at a time and may conceive only once every 3 to 9 years (Poole and Moss, 1989). Thus, given the short female receptive period and the high investment in each offspring, it is crucial for a

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Figure 8-2 The social organization of elephants includes a central family core consisting of the matriarch, other adult females, sexually mature and immature female offspring, and sexually immature juvenile males. The sexually mature juvenile males roam in isolated bachelor groups. Adult males will form mating consorts with adult females. Old musth bulls remain solitary and away from the family unit. female to find a high-quality mate. Usually a female will prefer to mate with an old male that will chase away the younger males and allow the female to rest, a necessity for successful elephant reproduction (DiSilvestro, 1991). Reproduction, Life Span, and Aging Females are sexually mature at 10 years, the gestation period is 22 months, and interbirth intervals last up to 9 years (Buss and Smith, 1966). The close bond between mothers and their offspring can endure for 50 years. Males reach sexual maturity at 17 years (DiSilvestro, 1991), at which time they leave the family unit. At 30 years, a male is almost full size (3.7 meters at shoulder) and first experiences an annual condition of heightened sexual motivation, musth (Owens and Owens, 1992). There is only one musth male in an elephant population at one time because musth males are dominant and can suppress this breeding condition in other males (DiSilvestro, 1991). Although reproduction is continuous throughout an elephant's lifetime (Laws et al., 1975), the peak of female elephant fecundity occurs at 30-40 years and

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steadily declines thereafter to 37 percent of the peak at 46-50 years, 25 percent at 51-55 years, and 0 percent after 55 years (Laws, 1966). Laws et al. (1975) estimated menopause in African elephants at 55 years, although Sukumar (1989) reported a pregnant 60-year-old cow. The prime of life for an elephant is about 30-40 years (DiSilvestro, 1991). Old age begins around 50, and most elephants die by 60 (Fatti et al., 1980), although some have lived into their 70s (Freeman, 1980). Sikes (1967, 1971) believes that the upper limit of life span is 65 years and is determined by molar-teeth deterioration, so that old individuals cannot eat and survive. Elephants past 50 years usually have the temporal region of the skull depressed and sunken. This physical trait is a sign of old age but not an indication of failing health. Major Roles of the Elderly The first major role of the elderly in elephant populations is leadership. Elephant size determines dominance and is also age-dependent because elephants continue to grow throughout their lives. Therefore, older females tend to be the largest of their sex in the herd and, because elephants' social organization is matriarchal, the oldest females are usually the leaders (DiSilvestro, 1991; Redmond, 1991). Despite disease and deterioration, aging females still have an important role in elephant society, and the movements of the herd are adaptable to an aging animal (Freeman, 1980). If the matriarch is injured or killed, the family unit is lost and the animals are easily disbanded or fall prey to the same fate (e.g., poaching) in their confusion (Eltringham, 1982). When the family is approached by predators or other threatening situations, if the matriarch runs, the family runs; if she attacks, the family attacks (Hanks, 1973, 1979). The matriarch will also stand guard over any injured animal in her group, roaring loudly over the body while attempting to upright the animal. Laws et al. (1975) noted that because of the overwhelmingly matriarchal structure of elephant populations, selective culling of old or barren cows is probably disadvantageous. It removes from the population the adult females with the lowest reproductive rate, which may be helpful for population control but, more seriously, removes the leaders. The elimination of their accumulated experience must add appreciably to the disturbance factor. Moreover, the removal of matriarchs may well lead to formation of larger groups with unfavorable effects on the habitats due to more intensified localized use. The second major role of the elderly in elephant populations involves reproduction in males. Older males tend to be physically larger and possess larger, heavier tusks (Laws, 1966; Poole, 1987, 1994). Both traits have major influence on male mating success. Females prefer to mate with old bulls because consequently, offspring will inherit genes of long-lived, healthy adults, and old musth bulls will protect her from the harassment of young bulls (Lawley, 1994). After their matings, the older bull stays with the younger cow and guards or escorts her

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until the end of her estrous cycle, which provides her with some days of calm, free from male attentions, in which she hopefully will conceive (Owens and Owens, 1992; Lawley, 1994). The importance of old bulls to the success of elephant reproduction eluded many early observers of elephant behavior when considering the impact of the harvest of the "big tuskers" in ivory trade (DiSilvestro, 1991). The old bulls no longer associated with the herd were interpreted as past their prime. However, they were in their prime, although solitary as almost all adult males are, and in search of estrous females from many different herds (Poole and Moss, 1981; DiSilvestro, 1991). The third major role of elderly elephants involves essentially the collective knowledge of the matriarchs. In peaceful times, the matriarch decides where the family goes, when to move, and where and when to sleep. Seasonal movements are guided by the matriarch because she has retained knowledge of the optimal or long-forgotten food and water reserves from her long life (Shoshani, 1991). This she teaches to the younger animals (Eltringham, 1982). The solution to many problems of elephant daily life are learned rather than instinctual, making the matriarch, above all, the ultimate repository of essential survival skill that younger animals simply would not have had time to learn on their own (Lawley, 1994). As Laws et al. (1975) notes, "We feel that the dependence of a family unit upon its matriarch even in the most extreme of situations illustrates the great importance of the acquisition of experience and learning made possible by the evolution of longevity. We consider that this situation represents an evolutionary development that is now probably essential for the stability of elephant communities." The matriarch is a reservoir of "collective wisdom of the community" (Eltringham, 1982). Primates Ecological Background Nonhuman primates are composed of 185 species comprising four main branches: prosimians (including lemurs, lorises, pottos, and bush babies), New World monkeys (including capuchins, marmosets, and night squirrel monkeys), Old World monkeys (including mandrills, guenons, baboons, and colobus monkeys), and great apes (including chimpanzees, orangutans, and gorillas) (Estes, 1991). With few exceptions (e.g., macaques and langurs in temperate Japan and China) primates are confined to the tropics, and 80 percent live in rain forests (Estes, 1991). Most nonhuman primates are arboreal or cliff-dwelling; only the gorilla sleeps on the ground (Estes, 1991). Small primates, such as pottos and bush babies, feed primarily on small arthropods, but larger ones must rely on new leaves, buds, shoots, seed pods, and fruit. All monkeys and apes are sociable, and the majority live in female-bonded

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sphecids, Evans (1966) suggests that progressively provisioning Bembix live two to four times as long as mass-provisioning Gorytes. As females spend longer periods sitting in the protected nest, different selective factors become important. Mortality due to accident and predation is likely to be reduced, there is selection to reduce rates of senescence, life span increases, and mothers are more likely to be alive when some of their offspring reach adulthood (Cowan, 1991). Phase IV Generation Overlap/Primitive Eusociality The female's life is prolonged and overlaps that of the progeny that remain with her in the nest to form an extended family. Females at this phase lay eggs into an empty cell, a trait thought important in permitting evolution of the extended brood care of social wasps (Evans, 1958; Carpenter, 1991). The young females may construct more cells, lay eggs, and care for their own larvae. However, some females occasionally care for the brood of another female. These behaviors are important steps because the evolution of sociality is not possible without overlap of generations and, at least, rudimentary division of labor. Jayakar and Spurway (1966) believe that the ability to care for more than one cell and larva simultaneously is an important evolutionary step toward eusociality. Phase V Caste Differentiation Extensive overlap of generations occurs because of extended life spans and because a clear division of labor and caste systems begins to emerge. Wasps have opportunities for fitness gain by associating with relatives of different generations (Cowan, 1991). Differential feeding of larvae occurs. Early progeny are workers, but some intermediate forms are present between these and true females. A single queen, usually the original foundress, is much more long lived than the workers and monopolizes oviposition, referred to as queen control. As long as the colony remains small and the life spans of reproductive individuals and helpers do not differ significantly, helpers may be expected to resist evolutionary specialization as workers because this would reduce or eliminate their chances to replace their mother as the sole reproductive female (Alexander et al., 1991). As eusocial colonies become large and long-lasting, mothers become increasingly specialized as reproductives, and offspring specialize as workers and soldiers. As this happens, daughters have fewer opportunities to become replacement reproductives, both because the mother lives longer and because so many other individuals are available to replace the mother as well. Thus the identity of a queen's replacement becomes a sweepstakes, with each individual having a chance of, perhaps, one in 50,000 or one in a million (Alexander et al., 1991). One consequence of increased longevity as a preadaptation to sociality is that the stage is set for the evolution of large colonies that have certain advantages over smaller ones, including the ability to organize labor more efficiently, integrate colony activities, defend the nest more aggressively, and exert homeostatic control over physical conditions within the nest (Jeanne, 1991).

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Evolution of Life Span in Eusocial Workers Few uses of the disposable-soma theory of senescence (Kirkwood, 1985) are more apt than when this concept is applied to worker castes in social insects. The fact that honeybee workers are expendable is apparent from their sting and aggressive defensive behavior. Because honeybees' stings are barbed, their stings and adjacent tissues remain anchored in the skin of intruders, thereby creating a chemical alarm that guides other guards to the enemy (Seeley, 1985). Thus the gerontological question is not whether workers are "disposable," but rather how long they should live relative to the "needs" of the colony. Insights into this question can be gained by considering the relationship of the number of births in a monogynous (single queen) colony (bq) , daily death rate of workers (dw), and maximal colony size (N*) as given in the equation (Carey, 1993): It is evident from this simple equation that colony size can increase by either increasing daily birth rate or decreasing daily death rate of workers. For example, if bq = 100 eggs/day and dw = 0.10, then N* = 1,000. However, if either dw decreased to 0.01 or bq increased to 1,000, then the maximal colony size, N*, would increase to 10,000 individuals. A more complete range of tradeoffs between birth and death rates for a fixed maximal colony size is given in Table 8-4. Primitive social-insect colonies probably maintain a modest colony size by evolving an increased life span of the as-yet-undifferentiated "worker" caste. This is because high egg production in queens requires a highly evolved system of food provisioning and propholaxis (liquid food exchange). At the early stages of the evolution of eusociality, it is probably easier to extend life span in all colony members. However, in more advanced groups, when queen longevity is several fold greater than workers, the worker life span is probably determined by needs of colony defense, predictability of food resources, and colony-maintenance requirements. TABLE 8-4 Maximum Size of Social Insect Colonies Given Different Worker Life Expectancies and Queen Daily Egg Production   Queen Daily Egg Production Life Expectation 100 1000 10,000 100,000 20 days 2,000 20,000 200.000 2,000,000 50 days 5,000 50,000 500.000 5,000,000 100 days 10,000 100,000 1,000,000 10,000,000 200 days 20,000 200,000 2,000.000 20,000,000   SOURCE: Carey (1993; tables 5-12).

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Discussion General Themes The overall theme of this paper is that, as a subgroup, the elderly play important roles in the cohesion and dynamics of groups, populations, and communities. They serve as care-givers, as guardians, as leaders, as stabilizing centers, as teachers, as sexual consorts, and as midwives. The elderly are at an evolutionary forefront when their brood-care behavior contributes to population fitness, which, in turn, may lead to evolution of sociality in insects and perhaps to other evolutionary pathways in other species. Virtually all behaviors exhibited by the elderly have an evolutionary basis, yet evolutionary aspects of behavior are seldom considered in the context of aging biology. Perhaps the time has come to expand the scope of gerontology and demography of aging to include behavioral to better incorporate the contributions of the elderly to the fitness of populations. Another theme of this paper, particularly concerned with longevity as a preadaptation for the evolution of eusociality, is that it is important to distinguish between micro- and macroevolutionary aspects of aging and longevity change. Clearly, the evolutionary scale of change for fruit fly selection experiments (Rose, 1991) involving the cost of reproduction is different from changes involving the emergence of major taxonomic groups, new structures, physiological processes, or major adaptive shifts (i.e., eusociality). It is important to recognize differences in evolutionary scales because the macroevolutionary scale provides context for broad differences in life spans, which may shed light on more subtle, microevolutionary differences. Cost of reproduction tradeoffs or metabolic-rate differences may help explain longevity constraints in microevolutionary settings but provide little insight into why, for example, bats and birds live longer than similarly sized mammals. Explanations for these life span differences may have more to do with macroevolutionary causes, such as the evolution of sociality or changes in ecological factors, than with proximate factors, such as reproductive costs. Biodemographic Perspectives on Life Span In many species a substantial amount of energy is devoted to offspring care. Demographically, this results in reduction of birth rate. For example, Van Lawick-Goodall's (1976:86) description of the chimpanzee's early life is informative: The infant does not start to walk until he is six months old, and he seldom ventures more than a few yards from his mother until he is over nine months old. He may ingest a few scraps of solid food when he is six months, but solids do not become a significant part of his diet until he is about two years of age and he

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TABLE 8-5 Partial List of Life-History Traits Associated with Extended Longevity in Animals Long gestation or developmental period Small number of offspring per pregnancy, brood, or litter Long interbirth intervals Long period of offspring dependency Intense parenting or brood care Strong social bonds Protracted learning period and increased learning potential Home base, nest, or territory as locus Monogamy/pair bonding Enhanced sibling relationships continues to nurse until he is between four-and-a-half and six years old. Moreover, while he may travel short distances...when he is about four years old, he continues to make long journeys riding on his mother's back until he is five or six. As Lovejoy (1981) notes, the extreme degree of parental investment has profound demographic consequences. When the basic life-history patterns of humans are considered, noting that chimpanzees often live 30-35 years in the wild and that species with intensive parental care usually live substantially longer than species with little or no parental care, all the evidence suggests that the evolved life span of primitive humans was several fold greater than the life expectancy of 15-25 years (Hayflick, 1994). For example, if the maturation period of early hominids was 15 years, the birth interval was 5 years, and survival to adulthood was 30 percent to 50 percent (even with intensive parental care), then a female must live 35 years just to replace herself and her mate and 50 years to adequately care for her last-born child (i.e., the mother's death would substantially reduce the survival chances of several dependent offspring, and even the survival chances of other members of the group if she is involved in cooperative care of the young). If probability of survival to adulthood was less than 30 percent and/or a percentage of the females were sterile, then the last age of reproduction would increase to 40 years and life span would increase to 55 years. This value is consistent with predictions of life spans based on correlations between longevity, brain weight, and adult size (Hayflick, 1994). Our approach combines biological and demographic logic with perspectives on the life histories of other species. Table 8-5 contains a list of life-history traits that appear to associate with increased longevity in many of these species. Gerontological and Demographic Implications The perspectives provided by exploring the natural history and the roles of the elderly in nonhuman populations have the potential to greatly expand the

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scope of gerontology and the demography of aging by providing important ecological and biological context for these disciplines. Specifically, we have identified four different demographic and gerontological concepts that will benefit from further inquiry into the role of the elderly in nature. First, perspectives on the natural history of the elderly will provide a broader and deeper biological foundation for life-course analysis in demography, including the integration of concepts in demographic sociology (Riley and Riley, 1986), those in sociobiology (Wilson, 1975), and those in life-history theory (Roff, 1992). Second, emphasis on research on the elderly in nonhuman species may encourage evolutionary biologists to reevaluate the evolutionary theories of aging and senescence. Theories may need to be reformulated to account for situations where the elderly contribute a disproportionate share of genes to the next generation. Emphasis on the importance of the elderly at the population level will also provide important context for studies concerning adaptive demography or the optimal age/stage/size composition of various social groups (Oster and Wilson, 1978), as well as for the rate of genetic change in age-structured populations (Rose, 1991; Charlesworth, 1994). Third, the concept ''roles" of the elderly provide an organizational theme for interdisciplinary aspects of aging. For example, retirement has been referred to by social demographers as a "roleless role," lacking content and sure rewards (Riley and Riley, 1986). But social scientists have no biological foundation upon which to construct theories of social roles, just as many biologists have long thought that very few animals in natural habitats could evade predators and disease long enough to grow old. Fourth, in humans, the role of the elderly at the oldest ages is becoming almost synonymous with the role of elderly women. The aging society is increasingly becoming a society of older women, often widows. Our future studies will examine whether this feminization of the elderly is general, whether there are gender-specific roles of the elderly, and, if so, how and why these exist. Indeed, infant and juvenile care given by older "aunts" appears to be fairly common across many species. Thus, the literature on inclusive fitness theory (Hamilton. 1964) can be brought to bear on the development of aging theory and the behavioral traits of the elderly. These concepts have not yet been introduced to the gerontological literature; they are clearly fundamental to a deeper understanding of how older caregivers help perpetuate their own genes. Acknowledgments We thank Lynn Kimsey and Robert Jeanne for their insights and help with wasp evolution, and Claudia Graham and Shin-min Tsai for graphics. We are particularly indebted to the undergraduates who enrolled in our University of California at Davis research course on the role of the elderly in nature: Karen Abalos, Harold Amogan, Sophie Betts, Alicia Cook, Kimberly Day, Hoa Giang,

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