Hominin life history: reconstruction and evolution

In this review we attempt to reconstruct the evolutionary history of hominin life history from extant and fossil evidence. We utilize demographic life history theory and distinguish life history variables, traits such as weaning, age at sexual maturity, and life span, from life history-related variables such as body mass, brain growth, and dental development. The latter are either linked with, or can be used to make inferences about, life history, thus providing an opportunity for estimating life history parameters in fossil taxa. We compare the life history variables of modern great apes and identify traits that are likely to be shared by the last common ancestor of Pan-Homo and those likely to be derived in hominins. All great apes exhibit slow life histories and we infer this to be true of the last common ancestor of Pan-Homo and the stem hominin. Modern human life histories are even slower, exhibiting distinctively long post-menopausal life spans and later ages at maturity, pointing to a reduction in adult mortality since the Pan-Homo split. We suggest that lower adult mortality, distinctively short interbirth intervals, and early weaning characteristic of modern humans are derived features resulting from cooperative breeding. We evaluate the fidelity of three life history-related variables, body mass, brain growth and dental development, with the life history parameters of living great apes. We found that body mass is the best predictor of great ape life history events. Brain growth trajectories and dental development and eruption are weakly related proxies and inferences from them should be made with caution. We evaluate the evidence of life history-related variables available for extinct species and find that prior to the transitional hominins there is no evidence of any hominin taxon possessing a body size, brain size or aspects of dental development much different from what we assume to be the primitive life history pattern for the Pan-Homo clade. Data for life history-related variables among the transitional hominin grade are consistent and none agrees with a modern human pattern. Aside from mean body mass, adult brain size, crown and root formation times, and the timing and sequence of dental eruption of Homo erectus are inconsistent with that of modern humans. Homo antecessor fossil material suggests a brain size similar to that of Homo erectus s. s., and crown formation times that are not yet modern, though there is some evidence of modern human-like timing of tooth formation and eruption. The body sizes, brain sizes, and dental development of Homo heidelbergensis and Homo neanderthalensis are consistent with a modern human life history but samples are too small to be certain that they have life histories within the modern human range. As more life history-related variable information for hominin species accumulates we are discovering that they can also have distinctive life histories that do not conform to any living model. At least one extinct hominin subclade, Paranthropus, has a pattern of dental life history-related variables that most likely set it apart from the life histories of both modern humans and chimpanzees.     

The evolution of menopause and human life span

Noteworthy data is emerging to support the existence of longevity-enabling genes. Our observations of the relationship between reproductive fitness and longevity among centenarians support theories that posit strong selective forces in the determination of how fast humans age and their susceptibility to diseases associated with ageing. Current data support the idea that there is no selective advantage for humans to have a lifespan of approximately 100 years. Rather, getting to such a very old age may be a by-product of longevity-enabling genes that maximize the length of time during which women can bear children, and during which they can increase the survival probabilities of their children and grandchildren. We thus review the literature pertaining to the relationship between reproductive fitness and longevity.     

Relation between replicative senescence of human fibroblasts and life history characteristics

Replicative ageing of fibroblasts in vitro has often been used as a model for organismal ageing. The general assumption that the ageing process is mirrored by cellular senescence in vitro is based on lower replicative capacity of human fibroblasts from patients with accelerated ageing syndromes, patients with age related diseases such as diabetes mellitus, and donors of higher chronological age, but these inverse relations have not been reported unequivocally. Therefore, we have performed a formal review on the replicative capacity of fibroblasts from patients suffering from accelerated ageing syndromes, age related diseases and donor age. Some 13 studies including 79 patients with accelerated ageing syndromes showed replicative capacity of fibroblasts to be consistently lower when compared to fibroblasts obtained from age-matched controls. Some 12 studies reported on a total of 160 patients with various age related diseases, but compared to age-matched controls no consistent difference in replicative capacity was reported. Finally, in the period from 1964 to 2006 a total of 23 studies, including some 1115 individuals, reported on the relation between chronological age and replicative capacity of human fibroblasts. Earlier studies preferentially described an inverse relation between replicative capacity and chronological age that was absent in studies including higher numbers of subjects and were published more recently. There was marked heterogeneity between the studies (Egger test: p = 0.018) indicating that publication bias is at play. We conclude that, except for premature ageing syndromes, replicative capacity of fibroblasts in vitro does not mirror key characteristics of human life histories.     

Polygamy and the evolution of human longevity.

An alternative to previous explanations of the rapid increase in man's longevity and intelligence during the several million years of his recent evolution from pre-hominid, clearly shorter-lived and less intelligent, primate ancestors is presented. The general thesis is that a very greatly accelerated rate of incorporation of favorable genes or gene combinations can be achieved in surprisingly few generations among social animals provided that dominant males become the patriarchs of many descendents by virtue of their partial or complete monopoly on available females. The conclusion is that man probably differs from his ancesters of 0.5 to 5 million years ago by many thousands of genes (both structural and regulatory) rather than the dozens or few hundreds that have been postulated on the basis of more classical treatments of selection pressures, gene frequency changes and mutation rates. The concepts developed here formally apply only to two alternative alleles, rather than to groups of genes which segregate independently, or to characters determined by multiple alleles. The appropriate mathematical treatment of the latter real situation is not readily visualized; nor is account taken of the likelihood that different tribes of pre-humans developed different specializations via the above mechanisms which were then (later) combined into an emerging human stock through matings between members of different tribes. The very great variability both in longevity and in intelligence between different races of animals such as dogs, which have been the objects of deliberate genetic selection by humans for particular heritable traits, may parallel our own recent history, even though the selection mechanism (deliberate human selection vs. polygamous dominance) is quite different in the two cases. The onset of civilizations consisting of amalgums between smaller, previously competing tribes, together with the humanitarian responsibilities to each other we share as a species, ironically has probably arrested further evolution of human longevity (and perhaps of intelligence) in the modern world. Possibly even retrogressive changes are occurring, except in those rare sub-populations in which special social and cultural practices tend to favor selective perpetuation of characteristics which are usually viewed as beneficial.     

Ritualized combat as an indicator of intrasexual selection effects on male life history evolution

Trade‐offs between survival, growth, current reproduction, and future reproduction influence life history evolution, leading to adaptive timing of investment in various strategies. If engagement in costly intrasexual contests to gain better access to mates is an important form of male reproductive investment, then the expression of characters that promote success in this process should be influenced by their fitness effects across the lifespan. To test this prediction, the ages at which human (Homo sapiens) males exhibit the greatest investment in morphological, behavioral, and physiological characters associated with intrasexual competition was estimated by examining the ages at which males succeed in a form of ritualized combat. The average age of international boxing champions was in the latter half of the twenties, and titles were held for about 2 years on average. Thus, peak investment in traits that enhance intrasexual competition abilities appears to coincide with ages at which males have highest reproductive success. Additionally, larger males reached peak probability of success in this ritualized combat at ages about 2.6 years greater than smaller males. Because body size is highly heritable and there is strong positive assortative mating relative to this character among humans, this may indicate a polymorphic set of reproductive strategies produced through maintenance of coadapted gene complexes. Am. J. Hum. Biol., 2010. © 2009 Wiley‐Liss, Inc.     

Reciprocal chromosome painting illuminates the history of genome evolution of the domestic cat, dog and human

Domestic cats and dogs are important companion animals and model animals in biomedical research. The cat has a highly conserved karyotype, closely resembling the ancestral karyotype of mammals, while the dog has one of the most extensively rearranged mammalian karyotypes investigated so far. We have constructed the first detailed comparative chromosome map of the domestic dog and cat by reciprocal chromosome painting. Dog paints specific for the 38 autosomes and the X chromosomes delineated 68 conserved chromosomal segments in the cat, while reverse painting of cat probes onto red fox and dog chromosomes revealed 65 conserved segments. Most conserved segments on cat chromosomes also show a high degree of conservation in G-banding patterns compared with their canine counterparts. At least 47 chromosomal fissions (breaks), 25 fusions and one inversion are needed to convert the cat karyotype to that of the dog, confirming that extensive chromosome rearrangements differentiate the karyotypes of the cat and dog. Comparative analysis of the distribution patterns of conserved segments defined by dog paints on cat and human chromosomes has refined the human/cat comparative genome map and, most importantly, has revealed 15 cryptic inversions in seven large chromosomal regions of conserved synteny between humans and cats. This revised version was published online in July 2006 with corrections to the Cover Date.     

Prebiological evolution and the metabolic origins of life

The chemoton model of cells posits three subsystems: metabolism, compartmentalization, and information. A specific model for the prebiological evolution of a reproducing system with rudimentary versions of these three interdependent subsystems is presented. This is based on the initial emergence and reproduction of autocatalytic networks in hydrothermal microcompartments containing iron sulfide. The driving force for life was catalysis of the dissipation of the intrinsic redox gradient of the planet. The codependence of life on iron and phosphate provides chemical constraints on the ordering of prebiological evolution. The initial protometabolism was based on positive feedback loops associated with in situ carbon fixation in which the initial protometabolites modified the catalytic capacity and mobility of metal-based catalysts, especially iron-sulfur centers. A number of selection mechanisms, including catalytic efficiency and specificity, hydrolytic stability, and selective solubilization, are proposed as key determinants for autocatalytic reproduction exploited in protometabolic evolution. This evolutionary process led from autocatalytic networks within preexisting compartments to discrete, reproducing, mobile vesicular protocells with the capacity to use soluble sugar phosphates and hence the opportunity to develop nucleic acids. Fidelity of information transfer in the reproduction of these increasingly complex autocatalytic networks is a key selection pressure in prebiological evolution that eventually leads to the selection of nucleic acids as a digital information subsystem and hence the emergence of fully functional chemotons capable of Darwinian evolution.     

Early life environment, life history and risk of endometrial cancer

Endometrial cancer risk is influenced by reproductive behaviours, including parity and breastfeeding, and timing of life history events such as age at menarche and menopause. One potential mechanism by which altered reproductive strategies may influence endometrial cancer risk is through exposure to reproductive hormones. Current theory suggests that high lifetime exposure to oestrogen, unopposed by progesterone, increases endometrial cancer risk; here we suggest that progesterone deficiency itself may also play a significant role. Additionally, given that reproductive profile variables are themselves influenced by early childhood conditions, we hypothesise that endometrial cancer risk may be influenced by the childhood psychosocial environment as mediated through changes to adolescent and adult reproductive behaviours and hormone exposures. Investigating reproductive cancers, including endometrial cancer, using a life history approach may help to increase understanding of why these cancers occur and potentially help implementation of early detection and screening processes in the future.     

Early life events and their consequences for later disease: a life history and evolutionary perspective.

Biomedical science has little considered the relevance of life history theory and evolutionary and ecological developmental biology to clinical medicine. However, the observations that early life influences can alter later disease risk--the "developmental origins of health and disease" (DOHaD) paradigm--have led to a recognition that these perspectives can inform our understanding of human biology. We propose that the DOHaD phenomenon can be considered as a subset of the broader processes of developmental plasticity by which organisms adapt to their environment during their life course. Such adaptive processes allow genotypic variation to be preserved through transient environmental changes. Cues for plasticity operate particularly during early development; they may affect a single organ or system, but generally they induce integrated adjustments in the mature phenotype, a process underpinned by epigenetic mechanisms and influenced by prediction of the mature environment. In mammals, an adverse intrauterine environment results in an integrated suite of responses, suggesting the involvement of a few key regulatory genes, that resets the developmental trajectory in expectation of poor postnatal conditions. Mismatch between the anticipated and the actual mature environment exposes the organism to risk of adverse consequences-the greater the mismatch, the greater the risk. For humans, prediction is inaccurate for many individuals because of changes in the postnatal environment toward energy-dense nutrition and low energy expenditure, contributing to the epidemic of chronic noncommunicable disease. This view of human disease from the perspectives of life history biology and evolutionary theory offers new approaches to prevention, diagnosis and intervention.     

A short history of human genetics in the USA.

The practicing physician discovered human genetics primarily as a result of two events. The use of the atomic bomb generated a vast amount of attention because of the fear of genetic hazards of radiation. Next, the discovery that the Down syndrome resulted from the presence of an extra chromosome finally focused the vision of the medical profession on human genetics as an area of importance in disease. It was also necessary that the erroneous fatalism about the impossibility of treating genetic diseases had to diminish before medicine would find human genetics attractive for research in therapeutic techniques. All of these things have come to pass and human genetics cannot help but enjoy a distinguished and extremely useful future.     

Genetics of factors affecting the life history ofDrosophila melanogaster. III. Egg insertion behavior

A genetic analysis of two laboratory strains ofDrosophila melanogaster that displayed opposite oviposition tendencies with respect to egg insertion behavior was performed. In general, the insertion characteristic appears to be dominant over the noninsertion characteristic and is controlled by a polygenic system associated mostly with chromosomes 2 and 3. The result of this study indicate that these genes may be concentrated at the distal end of chromosome 2L and at the distal end of chromosome 3R, and their presence on both of these chromosome regions is needed to approach the full egg insertion effect, suggesting the presence of interaction among genes in these two regions.This work was supported by Research Grant AG01934 from the National Institute of Aging to Y. Hiraizumi.     

The evolution of late life

Late life is a distinct phase of life characterized by a cessation in the deterioration of survivorship and fecundity characteristic of normal aging. Several theories have been proposed to explain non-aging at late ages, specifically with regards to late-life mortality-rate plateaus. All such theories must be compatible with formal evolutionary theory and experimental findings. Here, we develop a critique of theories of late life based on evolutionary biology.     

Developmental origins of life history: growth, productivity, and reproduction.

There is now much evidence that early life undernutrition elevates risk of diseases like cardiovascular disease. Less clear is whether the underlying developmental plasticity in metabolism and physiology evolved to serve an adaptive function, beyond these effects on pathophysiology. This review builds from principles of life history theory to propose a functional model linking early environments with adult biology. An organism has metabolic potential in excess of survival requirements, called productivity, that supports growth before being shunted into reproduction after growth ceases. This concept from inter-specific studies leads to the prediction that plasticity in growth rate will be positively correlated with components of future adult reproductive expenditure. Consistent with this idea, evidence is reviewed that early nutrition or growth rate predict offspring size in females, and increased somatic investment related to reproductive strategy in males. Thus, population birth weight and sexual size dimorphism are predicted to increase in response to improvements in early nutrition. A striking feature of the continuity of metabolic production is its perpetuation not merely during the lifecycle but across generations: in females, growth rate predicts future nutritional investment in reproduction, which in turn determines fetal growth rate in the next generation. Growth and reproduction serve as mutually-defining templates, thus creating a phenotypic bridge allowing ecologic information to be maintained during ontogeny and transmitted to offspring. Resetting of metabolic production in response to maternal nutritional cues may serve a broader goal of integrating nutritional information within the matriline, thus providing a more reliable basis for adjusting long-term strategy.     

Race and the odd history of human paleontology

Although the late 17th century witnessed the recognition of fossils as the remains of extinct organisms-because they could be incorporated into the creation story embodied in the Great Chain of Being-acceptance of human antiquity through the indisputable demonstration of the contemporaneity of human bones, stone tools, and accepted fossils was not forthcoming for nearly 2 centuries thereafter. When it did occur, however, ancient humans were not seen as presenting a pattern of diversity similar to that seen in the fossil records of nonhuman organisms. Instead, human evolution then, as now, has typically been interpreted as being unilinear. This belief can be traced to Huxley (1863), who argued that the Feldhofer Grotto Neanderthal skullcap was merely an extension into the past of morphology seen in the Australian Aborigine, whom he took to represent the primitive end of an extreme range of variation he thought characterized Homo sapiens. During the mid-20th century, Mayr and Dobzhansky (mis)used their clout as founders of the evolutionary synthesis to cement in paleoanthropology the idea that human evolutionary history was characterized by nonspeciation. As such, anything that could be interpreted as potentially representing taxic diversity was relegated to the status of individual variation. Lack of understanding of the history of human paleontology, and the biases that constrained its perspective on human evolution, continue to affect the ways in which most paleoanthropologists pigeonhole human fossils.