A theory of human life history evolution: Diet,intelligence, and longevity

Human life histories, as compared to those of other primates and mammals, have at least four distinctive characteristics: an exceptionally long lifespan, an extended period of juvenile dependence, support of reproduction by older post‐reproductive individuals, and male support of reproduction through the provisioning of females and their offspring. Another distinctive feature of our species is a large brain, with its associated psychological attributes: increased capacities for learning, cognition, and insight. In this paper, we propose a theory that unites and organizes these observations and generates many theoretical and empirical predictions. We present some tests of those predictions and outline new predictions that can be tested in future research by comparative biologists, archeologists, paleontologists, biological anthropologists, demographers, geneticists, and cultural anthropologists.     

Longevity and life history in hominid evolution

Under the assumption that life history in general and longevity in particular play an important part in the study of evolutionary patterns and processes, this paper focuses on predicting longevity changes across hominid evolution and attempts to throw light on the significance of such changes. We also consider some statistical arguments in the analysis of hominid life history patterns. Multiple regression techniques incorporating primate body weight and brain size data are used to predict hominied longevity and the results are compared to those in the literature. Our findings suggest that changes in hominid longevity are more likely to follow brain size than body weight, and that multiple regression techniques may be an appropriate avenue for future studies on life history variation in human evolution.     

Artificial evolution of life history and behavior

We present an individual-based model that uses artificial evolution to predict fit behavior and life-history traits on the basis of environmental data and organism physiology. Our main purpose is to investigate whether artificial evolution is a suitable tool for studying life history and behavior of real biological organisms. The evolutionary adaptation is founded on a genetic algorithm that searches for improved solutions to the traits under scrutiny. From the genetic algorithm's "genetic code," behavior is determined using an artificial neural network. The marine planktivorous fish Müller's pearlside (Maurolicus muelleri) is used as the model organism because of the broad knowledge of its behavior and life history, by which the model's performance is evaluated. The model adapts three traits: habitat choice, energy allocation, and spawning strategy. We present one simulation with, and one without, stochastic juvenile survival. Spawning pattern, longevity, and energy allocation are the life-history traits most affected by stochastic juvenile survival. Predicted behavior is in good agreement with field observations and with previous modeling results, validating the usefulness of the presented model in particular and artificial evolution in ecological modeling in general. The advantages, possibilities, and limitations of this modeling approach are further discussed.     

Parasite evolution and extinctions

We examine the evolution of diseases that show the frequency‐dependent transmission process that is commonly applied to sexually and vector‐transmitted infections. As is commonly found, the basic reproductive ratio (R₀) of the parasite is maximized by evolution. This has important implications, as it implies that for a wide range of circumstances diseases that show frequency‐dependent transmission may be selected to evolve towards driving their hosts to extinction. This contrasts with the results obtained in spatially explicit models where although parasite‐driven host extinction may occur, it is unlikely to evolve. We further show that an evolutionary constraint between transmission and virulence is required for evolution to lead to an endemic coexistence of both the host and the disease. Furthermore, this constraint needs to be saturating, such that transmission is ‘bought’ at an increasing cost in terms of virulence, to avoid evolution to extinction.     

Insect life history and the evolution of bacterial mutualism

Bacterial symbiosis has played a fundamental role in the evolution of eukaryotes. However, we still know little about how cooperative relationships with bacteria originate, and why they form in some host species but not others. Facultative symbionts that are beneficial, but not essential, provide unique insights into these processes. We use data from over a hundred aphid species to test if host life history is associated with the presence of facultative symbionts. We find that aphid species that have mutualistic associations with ants that protect them from natural enemies are less likely to carry symbionts that provide similar benefits. We also find one symbiont species occurs more frequently in unrelated aphid species that specialise on certain plant genera. In addition, aphid species that attack multiple plants often carry different symbiont complements. Our findings provide evidence of the ecological conditions that facilitate stable, mutually beneficial relationships between microbes and eukaryotic hosts.     

Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails

Using field surveys and experimental infections, we investigated the influence of a trematode parasite on life history traits of adult Lymnaea elodes snails. We found that parasitism significantly affected the growth, fecundity, and survival of host snails. Within five of the six natural L. elodes populations we sampled, shell length of echinostome-infected hosts was significantly greater than for uninfected conspecifics. Furthermore, we show that gigantism occurs among experimentally infected snails due to an accelerated growth rate and size-selective mortality following an Echinostoma revolutum infection. The fecundity of infected snails sharply decreased beginning at 3 weeks post exposure (PE) and all egg production eventually ceased for most hosts by 5–6 weeks PE. Energy constraints, imposed by parasite development, alter the host energy budget. Early in the infection, parasite depletion of host energy reserves reduces host reproduction, but sufficient resources remain to allow accelerated host growth. Mortality was increased among host snails at two distinct stages: shortly after exposure and several weeks after cercariae were first released. We did not observe tissue degradation in snails during the first 4 weeks after exposure to the parasite, but destruction of host tissues was noted among snails dying later in the infection. Received: 5 September 1997 / Accepted: 19 November 1997     

Nonconvergence in the evolution of primate life history and socio-ecology

The goal of this study was to investigate the extent of convergence in four basic life history and socio-ecological traits among the primates of Africa, Asia, South America and Madagascar. The convergence hypothesis predicts that similar abiotic conditions should result in similar adaptations in independent taxa. Because primates offer a unique opportunity among mammals to examine adaptations of independent groups to tropical environments, we collected information on body mass, activity pattern, diet and group size from all genera for quantitative tests of this hypothesis. We revealed a number of qualitative and quantitative differences among the four primate groups, indicating a lack of convergence in these basic aspects of life history and socio-ecology. Our analyses demonstrated that New World primates are on average significantly smaller than primates in other regions and characterized by a lack of species larger than about 10 kg. Madagascar harbours significantly more nocturnal species than the other regions and is home to all but one of the primates with irregular bursts of activity. Asia is the only region with strictly faunivorous primates, but lacks primarily gummivorous ones. The Neotropics are characterized by the absence of primarily folivorous primates. Solitary species are not represented in the New World, whereas solitary and pair-living species make up the majority of Malagasy primates. Lemurs live in significantly smaller groups than other primates, even after controlling for differences in body size. The lack of convergence among the major primate groups is neither primarily due to phylogenetic constraints as a result of founder effects, nor can it be sufficiently explained as a passive consequence of body size differences. However, because the role of adaptive forces, such as interspecific competition, predation or phenology in shaping the observed differences is largely unexplored, we conclude that it is premature to discard the convergence hypothesis without further tests.     

Dental development and the evolution of life history in Hominidae

Development of the dentition is critically integrated into the life cycle in living mammals. Recent work on dental development has given rise to three separate lines of evidence on the evolution of human growth and aging; these three, based on several independent studies, are reviewed and integrated here. First, comparative study of living primate species demonstrates that measures of development (e.g., age of emergence of the first permanent molar) are highly correlated with the morphological attributes brain and body weight (as highly as r = 0.98, N = 21 species). These data predict that small-bodied, small-brained Australopithecus erupted M₁ at 3–3.5 years and possessed a life span comparable to that of a chimpanzee. Second, chronological age at death for three australopithecines who died at or near emergence of M₁ is now estimated as ～3.25 years based on incremental lines in teeth; this differs substantially from expectations based on human growth schedules (5.5–6 years). Third, developmental sequences (assessed by the coefficient of variation of human dental age) observed in gracile Australopithecus and great apes diverge from those of humans to a comparable degree; sequences become more like modern humans after the appearance of the genus Homo. These three lines of evidence agree that the unique rate and pattern of human life history did not exist at the australopithecine stage of human evolution. It is proposed that the life history of early Homo matched no living model precisely and that growth and aging evolved substantially in the Hominidae during the last 2 million years.     

Adult hippocampal neurogenesis of mammals: evolution and life history

Substantial production of new neurons in the adult mammalian brain is restricted to the olfactory system and the hippocampal formation. Its physiological and behavioural role is still debated. By comparing adult hippocampal neurogenesis (AHN) across many mammalian species, one might recognize a common function. AHN is most prominent in rodents, but shows considerable variability across species, being lowest or missing in primates and bats. The latter finding argues against a critical role of AHN in spatial learning and memory. The common functional denominator across all species investigated thus far is a strong decline of AHN from infancy to midlife. As predicted by Altman and colleagues in 1973, this implies a role in transforming juvenile unpredictable to predictable behaviour, typically characterizing mammalian behaviour once reproductive competence has been attained. However, as only a fraction of mammalian species has been investigated, further comparative studies are necessary in order to recognize whether AHN has a common unique function, or whether it mediates species-specific hippocampal functions.     

A sex-specific quantitative genetic theory for life history and development

A quantitative genetic framework is developed to examine life history evolution with sex-specific differences in morphology, demographic parameters, and selection differentials occurring. Age-specific selection differentials are partitioned according to whether mediated through differential fertility, survival, or mating success, permitting the derivation of weightings according to selection mechanism as well as individual age and sex. The relationship of present to previously gained results is then examined, with applications to the evolution of bimaturism and evolutionary conservativeness of survival rate.     

Phytoplankton composition modifies predator-driven life history evolution in Daphnia

Organisms experience competing selective pressures, which can obscure the mechanisms driving evolution. Daphnia ambigua is found in lakes where a predator, the alewife (Alosa pseudoharengus) either does (anadromous) or does not (landlocked) migrate between marine and freshwater. We previously reported an association between alewife variation and life history evolution in Daphnia. However, differences in alewife migration indirectly influence phytoplankton composition for Daphnia. In ‘anadromous lakes’, Daphnia are present in the spring and experience abundant high-quality green algae. Intense predation by young-of-the-year anadromous alewife quickly eliminates these Daphnia populations by early summer. Daphnia from ‘landlocked lakes’ and lakes without alewife (‘no alewife lakes’) are present during the spring and summer and are more likely to experience high concentrations of sub-optimal cyanobacteria during the summer. To explore links between predation, resources, and prey evolution, we reared third-generation laboratory-born Daphnia from all lake types on increasing cyanobacteria concentrations. We observed several significant ‘lake type × resource’ interactions whereby the differences among lake types depended upon cyanobacteria concentrations. Daphnia from anadromous lakes developed faster, were larger at maturation, produced more offspring, and had higher intrinsic rates of increase in the absence of cyanobacteria. Such trends disappeared or reversed as cyanobacteria concentration was increased because Daphnia from anadromous lakes were more strongly influenced by the presence of cyanobacteria. Our results argue that alewife migration and phytoplankton composition both play a role in Daphnia evolution.     

动物生活史进化理论研究进展

综述了生活史性状、生活史对策、权衡、适合度及进化种群统计学等动物生活史进化领域的进展。权衡是生活史性状之间相互联系的纽带,分为生理权衡与进化权衡。适合度是相对的,与个体所处的特定环境条件有关,性状进化与适合度之间关系紧密。适合度是生活史进化理论研究的焦点。探讨动物生活史对策的理论很多,影响最大的是MacArthur和Wilson提出的r对策及K对策理论。随年龄的增长,动物存活率及繁殖率逐步下降的过程,称为衰老;解释衰老的进化理论主要有突变-选择平衡假设和多效对抗假设。进化种群统计学将种群统计学应用于生活史进化研究,为探讨表型适合度的进化提供了有效的手段。将进化种群统计学、数量遗传学及特定种系效应理论进行整合,建立完整的动物生活史进化综合理论体系,是当代此领域的最大挑战。     

Primate molar crown formation times and life history evolution revisited.

Comparative studies have convincingly demonstrated that the pattern and timing of tooth emergence are highly correlated with life-history variables and brain size. Conversely, a firm relationship between molar formation time and life-history variables has not yet been established. It seems counterintuitive that one aspect of dental development should be correlated with life-history variables, whereas the other should not. In order to shed light on this apparent discrepancy this study analyzed all data on primate molar crown formations available in the published literature in relation to life-history variables, brain size, and female body mass. Crown formation times were found to be particularly highly correlated with both female body mass and brain size. Species that depart from the overall brain/body allometry by being relatively large-bodied, e.g., Gorilla gorilla and later Theropithecus oswaldi, also have shorter molar crown formation times than expected. The reverse is not found for species that depart from the overall brain/body allometry due to their larger brains, i.e., Homo sapiens. This finding is interpreted within an evolutionary and ecological framework. Specifically, by focusing on ecological commonalities, a scenario is proposed which may allow predictions to be made about the evolutionary history of other extinct primates also. If confirmed in future studies, crown formation time may again become a powerful tool in evolutionary enquiry.     

Optimality models of phage life history and parallels in disease evolution

Optimality models constitute one of the simplest approaches to understanding phenotypic evolution. Yet they have shortcomings that are not easily evaluated in most organisms. Most importantly, the genetic basis of phenotype evolution is almost never understood, and phenotypic selection experiments are rarely possible. Both limitations can be overcome with bacteriophages. However, phages have such elementary life histories that few phenotypes seem appropriate for optimality approaches. Here we develop optimality models of two phage life history traits, lysis time and host range. The lysis time models show that the optimum is less sensitive to differences in host density than suggested by earlier analytical work. Host range evolution is approached from the perspective of whether the virus should avoid particular hosts, and the results match optimal foraging theory: there is an optimal "diet" in which host types are either strictly included or excluded, depending on their infection qualities. Experimental tests of both models are feasible, and phages provide concrete illustrations of many ways that optimality models can guide understanding and explanation. Phage genetic systems already support the perspective that lysis time and host range can evolve readily and evolve without greatly affecting other traits, one of the main tenets of optimality theory. The models can be extended to more general properties of infection, such as the evolution of virulence and tissue tropism.     

Allomaternal care, life history and brain size evolution in mammals

Humans stand out among the apes by having both an extremely large brain and a relatively high reproductive output, which has been proposed to be a consequence of cooperative breeding. Here, we test for general correlates of allomaternal care in a broad sample of 445 mammal species, by examining life history traits, brain size, and different helping behaviors, such as provisioning, carrying, huddling or protecting the offspring and the mother. As predicted from an energetic-cost perspective, a positive correlation between brain size and the amount of help by non-mothers is found among mammalian clades as a whole and within most groups, especially carnivores, with the notable exception of primates. In the latter group, the presence of energy subsidies during breeding instead resulted in increased fertility, up to the extreme of twinning in callitrichids, as well as a more altricial state at birth. In conclusion, humans exhibit a combination of the pattern found in provisioning carnivores, and the enhanced fertility shown by cooperatively breeding primates. Our comparative results provide support for the notion that cooperative breeding allowed early humans to sidestep the generally existing trade-off between brain size and reproductive output, and suggest an alternative explanation to the controversial ‘obstetrical dilemma’-argument for the relatively altricial state of human neonates at birth.     

Environmental complexity,life history,and encephalisation in human evolution

Brain size has increased threefold during the course of human evolution, whilst body weight has approximately doubled. These increases in brain and body size suggest that reproductive (and, therefore, evolutionary) rates must have slowed considerably during this period. During the same period, however, environmental heterogeneity has increased substantially. A central tenet of life-history theory states that in heterogeneous environments, organisms with fast life histories will be favoured. The human lineage, therefore, has proceeded in direct contradiction of this theory. This contribution attempts to resolve this contradiction by recourse to Godfrey-Smith’s Environmental Complexity Thesis, which states that the function of cognition is to enable the organism to deal with environmental complexity. It is suggested that among slowly reproducing organisms the behavioural flexibility provided by advanced cognitive abilities is a fundamental component of adaptation to heterogeneous environments. In the human lineage this flexibility is manifest particularly in the increasing complexity of material culture.