A milk-sharing economy allows placental mammals to overcome their metabolic limits.

SignificanceHere, we demonstrate that a naturally evolving behavior (allonursing) has greater effect on reproductive power (mass per unit of time) and output (litter mass at birth) than does artificial selection (domestication). Additionally, we demonstrate the importance of resource optimization afforded by sociality (rather than resource abundance per se) in shaping a species' life history profile and its ability to overcome its own physiological constraints.

Lack of evidence for coevolution between oxytocin receptor N-terminal variants and monogamy in placental mammals.

Oxytocin (OXT) is a neurohypophyseal hormone that influences a wide range of affiliative behaviors, such as pair-bonding and infant care, across mammals. The effects of OXT depend significantly on an adequate interaction with its receptor, OXTR. OXTR belongs to the G-protein coupled receptor family. The extracellular N-terminal domain of OXTR interacts with the linear C-terminal tail of OXT and is required for OXT binding. Across mammalian species there is a genetic diversity in OXTR terminal sequence. Previous work on primates has shown an association between OXTR phylogeny and monogamy. However, it is not clear whether this variation coevolved with either mating system (monogamy) or infant care behaviors (such as allomaternal care). Here, we take a phylogenetic comparative and evolutionary modeling approach across a wide range of placental mammals (n = 60) to test whether OXTR N-terminal variants co-evolved with either monogamy or allomaternal care behaviors. Our results indicate that the diversity in OXTR N-terminal region is unlikely to provide the underlying genetic bases for variation in mating system and/or allomaternal behavior as we find no evidence for co-evolution between protein sequence and affiliative behaviors. Hence, the role played by OXT in influencing affiliative behaviors is unlikely to be mediated by the genetic diversity of its receptor.

Life history in primate teeth is revealed by changes in major and minor element concentrations measured via field-emission SEM-EDS analysis.

Overcoming the non-specificity of histological accentuated growth lines in hard tissues is an ongoing challenge. Identifying season at death and reproductive events has profound implications for evolutionary, ecological and conservation studies. Dental cementum is a mineralized tissue with yearly periodicity that continues deposition from tooth formation until death, maintaining a record spanning almost the entire life of an individual. Recent work has successfully employed elemental analysis of calcified incremental tissues to detect changes in extrinsic conditions such as diet and climate and to identify two important life-history milestones: weaning and sexual maturity. Here, we employ field-emission scanning electron microscopy and energy-dispersive X-ray analysis to measure the relative concentrations of calcium, phosphorous, oxygen, magnesium and sodium in the cementum of 34 teeth from seven male and female rhesus macaques with known medical and life-history information. We find that changes in relative magnesium concentrations correspond with reproductive events in females and breastfeeding in infants. Additionally, we observe seasonal calcium patterns in 77.3% of the samples.

Growth of Neanderthal infants from Krapina (120-130 ka), Croatia.

Modern humans have a slow and extended period of childhood growth, but to what extent this ontogenetic pathway was present in Neanderthals is debated. Dental development, linked to the duration of somatic growth across modern primates, is the main source for information about growth and development in a variety of fossil primates, including humans. Studies of Neanderthal permanent teeth report a pace of development either similar to recent humans or relatively accelerated. Neanderthal milk teeth, which form and emerge before permanent teeth, provide an opportunity to determine which pattern was present at birth. Here we present a comparative study of the prenatal and early postnatal growth of five milk teeth from three Neanderthals (120 000-130 000 years ago) using virtual histology. Results reveal regions of their milk teeth formed quickly before birth and over a relatively short period of time after birth. Tooth emergence commenced towards the earliest end of the eruption schedules displayed by extant human children. Advanced dental development is consistent with expectations for Neanderthal infant feeding.

Weaning, parturitions and illnesses are recorded in rhesus macaque (Macaca mulatta) dental cementum microstructure.

Many open questions in evolutionary studies relate to species' physiological adaptations, including the evolution of their life history and reproductive strategies. There are few empirical methods capable of detecting and timing physiologically impactful events such as weaning, parturition and illnesses from hard tissue remains of either extant or extinct species. Cementum is an incremental tissue with post eruption annual periodicity, which covers the tooth root and functions as a recording structure of an animal's physiology. Here we test the hypothesis that it is possible to detect and time physiologically impactful events through the analysis of dental cementum microstructure. Our sample comprises 41 permanent and deciduous teeth from male and female rhesus macaques (Macaca mulatta) with known medical, lifestyle and life history information. We develop a semi-automated method of cementum histological analysis for the purpose of event detection and timing, aimed at significantly reducing the amount of intra- and interobserver errors typically associated with histological analyses. The results of our work show that we were able to detect known events including weaning, parturition, illness and physical trauma with high accuracy (false negative rate = 3.2%; n = 1), and to time them within an average absolute difference of 0.43 years (R2 = .98; p < .05). Nonetheless, we could not distinguish between the several types of stressful events underlying the changes in cementum microstructure. While this study is the first to identify a variety of life history events in macaque dental cementum, laying foundations for future work in conservation and evolutionary studies of both primates and toothed mammals at large, there are some limitations. Other types of analyses (possibly chemical ones) are necessary to tease apart the causes of the stressors.

Population differences in dental cementum growth rates: Implications for using cementum thickness as a method for age estimation.

OBJECTIVES: Age at death estimation is a key element to many research questions in biological anthropology, archeology, and forensic science. Dental cementum is a tissue of choice for the estimation of age at death in adult individuals as it continues deposition for the entirety of an individual's life. Previous works have devised regression formulas correlating cementum thickness to age at death. However, interpopulation variances are unknown, and it is therefore not clear whether regressions based on a single population are applicable to individuals with different ancestries. MATERIALS AND METHODS: Here, we use a sample (n = 52) of teeth from individuals with known age at tooth extraction/death of European, African, and East Asian ancestry to assess whether there are interpopulations differences in cementum growth rate. We measured growth rate in four different areas (2nd and 5th decile of both the lingual and buccal aspect of the root) of each tooth and used nonparametric tests to evaluate population differences in growth rate between homologous regions of the teeth. RESULTS: The results of the analyses show that, even after controlling for tooth size, individuals of European ancestry have significantly lower growth rates than those of both African and East Asian ancestry across all four tooth areas. DISCUSSION: These results call into question the applicability of the regression formulas derived from European ancestry individuals to individuals of other ancestries.

Reading children's teeth to reconstruct life history and the evolution of human cooperation and cognition: The role of dental enamel microstructure and chemistry.

Studying infants in the past is crucial for understanding the evolution of human life history and the evolution of cooperation, cognition, and communication. An infant's growth, health, and mortality can provide information about the dynamics and structure of a population, their cultural practices, and the adaptive capacity of a community. Skeletal remains provide one way of accessing this information for humans recovered prior to the historical periods. Teeth in particular, are retrospective archives of information that can be accessed through morphological, micromorphological, and biogeochemical methods. This review discusses how the microanatomy and formation of teeth, and particularly enamel, serve as archives of somatic growth, stress, and the environment. Examining their role in the broader context of human evolution, we discuss dental biogeochemistry and emphasize how the incremental growth of tooth microstructure facilitates the reconstruction of temporal data related to health, diet, mobility, and stress in past societies. The review concludes by considering tooth microstructure as a biomarker and the potential clinical applications.

Neurodevelopmental timing and socio-cognitive development in a prosocial cooperatively breeding primate (Callithrix jacchus).

Primate brain development is shaped by inputs received during critical periods. These inputs differ between independent and cooperative breeders: In cooperative breeders, infants interact with multiple caregivers. We study how the neurodevelopmental timing of the cooperatively breeding common marmoset maps onto behavioral milestones. To obtain structure-function co-constructions, we combine behavioral, neuroimaging (anatomical and functional), and neural tracing experiments. We find that brain areas critically involved in observing conspecifics interacting (i) develop in clusters, (ii) have prolonged developmental trajectories, (iii) differentiate during the period of negotiations between immatures and multiple caregivers, and (iv) do not share stronger connectivity than with other regions. Overall, developmental timing of social brain areas correlates with social and behavioral milestones in marmosets and, as in humans, extends into adulthood. This rich social input is likely critical for the emergence of their strong socio-cognitive skills. Because humans are cooperative breeders too, these findings have strong implications for the evolution of human social cognition.

Human Amygdala Volumetric Patterns Convergently Evolved in Cooperatively Breeding and Domesticated Species.

The amygdala is a hub in brain networks that supports social life and fear processing. Compared with other apes, humans have a relatively larger lateral nucleus of the amygdala, which is consistent with both the self-domestication and the cooperative breeding hypotheses of human evolution. Here, we take a comparative approach to the evolutionary origin of the relatively larger lateral amygdala nucleus in humans. We carry out phylogenetic analysis on a sample of 17 mammalian species for which we acquired single amygdala nuclei volumetric data. Our results indicate that there has been convergent evolution toward larger lateral amygdala nuclei in both domesticated and cooperatively breeding mammals. These results suggest that changes in processing fearful stimuli to reduce fear-induced aggression, which are necessary for domesticated and cooperatively breeding species alike, tap into the same neurobiological proximate mechanism. However, humans show changes not only in processing fearful stimuli but also in proactive prosociality. Since cooperative breeding, but not domestication, is also associated with increased proactive prosociality, a prominent role of the former during human evolution is more parsimonious, whereas self-domestication may have been involved as an additional stepping stone.

Elemental composition of primary lamellar bone differs between parous and nulliparous rhesus macaque females.

Extracting life history information from mineralized hard tissues of extant and extinct species is an ongoing challenge in evolutionary and conservation studies. Primary lamellar bone is a mineralized tissue with multidien periodicity that begins deposition prenatally and continues until adulthood albeit with concurrent resorption, thus maintaining a record spanning several years of an individual's life. Here, we use field-emission scanning electron microscopy and energy-dispersive X-ray analysis to measure the relative concentrations of calcium, phosphorous, oxygen, magnesium and sodium in the femora of seven rhesus macaque with known medical and life-history information. We find that the concentration of these elements distinguishes parous from nulliparous females; that in females calcium and phosphorus are lower in bone formed during reproductive events; and that significant differences in relative magnesium concentration correlate with breastfeeding in infants.

Dental cementum virtual histology of Neanderthal teeth from Krapina (Croatia, 130-120 kyr): an informed estimate of age, sex and adult stressors.

The evolution of modern human reproductive scheduling is an aspect of our life history that remains vastly uncomprehended. The present work aims to address this gap by validating a non-destructive cutting-edge methodology to infer adult life-history events on modern teeth with known life history and then applying it to fossil specimens. We use phase-contrast synchrotron X-ray microtomography to visualize the dental cementum of 21 specimens: nine contemporary humans; 10 Neanderthals from Krapina (Croatia, 130-120 kyr); one Neolithic Homo sapiens from Ajmana (Serbia); and one Mesolithic H. sapiens from Vlasac (Serbia). We were able to correctly detect and time (root mean square error = 2.1 years; R2 = 0.98) all reproductive (menarche, parturition, menopause) and other physiologically impactful events in the modern sample. Nonetheless, we could not distinguish between the causes of the events detected. For the fossil specimens, we estimated age at death and age at occurrence of biologically significant events. Finally, we performed an exploratory analysis regarding possible sexual dimorphism in dental cementum microstructure, which allowed us to correctly infer the sex of the Neolithic specimen, for which the true value was known via DNA analysis.

The expression of care: Alloparental care frequency predicts neural control of facial muscles in primates.

The adaptive value of facial expressions has been debated in evolutionary biology ever since Darwin's seminal work. Among mammals, primates, including humans, exhibit the most intricate facial displays. Although previous work has focused on the role of sociality in the evolution of primate facial expressions, this relationship has not been verified in a wide sample of species. Here, we examine the relationship between allomaternal care (paternal or alloparental) and the morphology of three orofacial brainstem nuclei (facial; trigeminal motor; hypoglossal) across primates to test the hypothesis that allomaternal care explains variation in the complexity of facial expressions, proxied by relative facial nucleus size and neuropil fraction. The latter represents the proportion of synaptically dense tissue and may, therefore, correlate with dexterity. We find that alloparental care frequency predicts relative neuropil fraction of the facial nucleus, even after controlling for social system organization, whereas allomaternal care is not associated with the trigeminal motor or hypoglossal nuclei. Overall, this work suggests that alloparenting requires increased facial dexterity to facilitate nonverbal communication between infants and their nonparent caregivers and/or between caregivers. Accordingly, alloparenting and complex facial expressions are likely to have coevolved in primates.

Adaptive Immune Response Associated with a Zirconium-Containing, Cemented, Total Knee Arthroplasty: A Case Report.

CASE: A 69-year-old woman underwent revision total knee arthroplasty for patellar component aseptic loosening. The periprosthetic tissue demonstrated histologic features of an adaptive immune response (aseptic lymphocyte-dominant vasculitis-associated lesion [ALVAL]). No particles of corrosion debris were identified. The inflammation seemed to be associated with zirconium oxide (ZrO2) particles added as a bone cement radio-opacifier. CONCLUSION: The factors responsible for the adaptive immune response cannot be determined with certainty; however, this is the first reported case of ALVAL associated with ZrO2-containing bone cement. Previous reports describing ALVAL around failed total knee prostheses have not included observations about the type of contrast material added to cement.

Parturitions, menopause and other physiological stressors are recorded in dental cementum microstructure.

The life history pattern of recent humans is uniquely derived in many of its aspects including an extended post-reproductive lifespan combined with short interbirth intervals. A number of theories have been proposed to explain the evolution of this unusual pattern. However most have been difficult to test due to the fragmentary nature of the hominin fossil record and the lack of methods capable of inferring such later life history events. In search of a method we tested the hypothesis that the physiologically impactful events of parturition and menopause are recorded in dental cementum microstructure. We performed histomorphological analyses of 47 teeth from 15 individuals with known life history events and were able to detect reproductive events and menopause in all females. Furthermore, we found that other stressful events such as systemic illnesses and incarceration are also detectable. Finally, through the development of a novel analytical method we were able to time all such events with high accuracy (R-squared = 0.92).