Estimating the population variance, standard deviation, and coefficient of variation: Sample size and accuracy.

Small sample sizes are often used in human and primate evolutionary research to estimate population parameters such as the mean, variance, and standard deviation, as well as statistical measures such as the coefficient of variation. Determining how well sample estimates represent population parameters is essential for establishing confidence in the inferences made using those samples. We present methods for determining a priori the probability, based on Cochran's theorem, that the sample variance and sample standard deviation are within a specified fraction of the population parameters. We validate these methods using random resampling with replacement of a single variable from a commonly used large craniometric data set comprising modern human population samples from around the world. Results based on Cochran's theorem, which we validate, indicate that large random samples comprising hundreds of observations, rather than tens of observations, are needed to be confident that the sample estimate is a reasonably accurate approximation of the true population variance. Smaller sample sizes on the order of tens of observations, however, are sufficient for estimating the population standard deviation. We extend our method of validation to show that the coefficient of variation mirrors closely the results for the standard deviation.

Evolutionary history of orangutan plasmodia revealed by phylogenetic analysis of complete mtDNA genomes and new biogeographical divergence dating calibration models.

During the past 15 years, researchers have shown a renewed interest in the study of the Plasmodium parasites that infect orangutans. Most recently, studies examined the phylogenetic relationships and divergence dates of these parasites in orangutans using complete mitochondrial DNA genomes. Questions regarding the dating of these parasites, however, remain. In the present study, we provide a new calibration model for dating the origins of Plasmodium parasites in orangutans using a modified date range for the origin of macaques in Asia. Our Bayesian phylogenetic analyses of complete Plasmodium sp. mitochondrial DNA genomes inferred two clades of plasmodia in orangutans (Pongo 1 and Pongo 2), and that these clades likely represent the previously identified species Plasmodium pitheci and Plasmodium silvaticum. However, we cannot identify which Pongo clade is representative of the morphologically described species. The most recent common ancestor of both Pongo sp. plasmodia, Plasmodium. hylobati, and Plasmodium. inui dates to 3-3.16 million years ago (mya) (95% highest posterior density [HPD]: 2.09-4.08 mya). The Pongo 1 parasite diversified 0.33-0.36 mya (95% HPD: 0.12-0.63), while the Pongo 2 parasite diversified 1.15-1.22 mya (95% HPD: 0.63-1.82 mya). It now seems likely that the monkey Plasmodium (P. inui) is the result of a host switch event from the Pongo 2 parasite to sympatric monkeys, or P. hylobati. Our new estimates for the divergence of orangutan malaria parasites, and subsequent diversification, are all several hundred thousand years later than previous Bayesian estimates.

Mitogenomics of macaques (Macaca) across Wallace's Line in the context of modern human dispersals.

Wallace's Line demarcates a biogeographical boundary between the Indomalaya and Australasian ecoregions. Most placental mammalian genera, for example, occur to the west of this line, whereas most marsupial genera occur to the east. However, macaque monkeys are unusual because they naturally occur on both western and eastern sides. To further explore this anomalous distribution, we analyzed 222 mitochondrial genomes from ∼20 macaque species, including new genomes from 60 specimens. These comprise a population sampling of most Sulawesi macaques, Macaca fascicularis (long-tailed macaques) specimens that were collected by Alfred R. Wallace and specimens that were recovered during archaeological excavations at Liang Bua, a cave on the Indonesian island of Flores. In M. fascicularis, three mitochondrial lineages span the southernmost portion of Wallace's Line between Bali and Lombok, and divergences within these lineages are contemporaneous with, and possibly mediated by, past dispersals of modern human populations. Near the central portion of Wallace's Line between Borneo and Sulawesi, a more ancient dispersal of macaques from mainland Asia to Sulawesi preceded modern human colonization, which was followed by rapid dispersal of matrilines and was subsequently influenced by recent interspecies hybridization. In contrast to previous studies, we find no strong signal of recombination in most macaque mitochondrial genomes. These findings further characterize macaque evolution before and after modern human dispersal throughout Southeast Asia and point to possible effects on biodiversity of ancient human cultural diasporas.

Hair cortisol and stable carbon and nitrogen isotope ratios in barbary macaques (Macaca sylvanus) from Gibraltar.

RATIONALE: Prolonged exposure to the stress hormone cortisol can precipitate a catabolic state in animals resulting in a negative nitrogen balance and increased excreted nitrogen, possibly affecting stable nitrogen and carbon isotope ratios in animal tissues. Here we test the hypothesis that stress, as measured by hair cortisol, is a significant contributor to variation in δ15 N and δ13 C values in hair. The results of the present study have important implications for the use of stable carbon and nitrogen isotope ratios measured in animal and human tissues to make inferences regarding feeding ecology and diet. METHODS: Samples containing roughly 10-20 hairs (approx. 4-6 cm long) were collected from 49 free ranging macaque monkeys (Macaca sylvanus) in Gibraltar. Hair samples were analyzed for stable carbon and nitrogen isotopes by continuous-flow isotope-ratio mass spectrometry. Cortisol extracted from matched hair samples was measured using gas chromatography/mass spectrometry. Cortisol and stable isotope ratios were compared statistically using nonparametric Kruskal-Wallis and Mann-Whitney U tests, as well as Spearman correlation. RESULTS: Correlation analysis revealed that although hair δ15 N and δ13 C values were significantly correlated with each other, neither was correlated with cortisol concentrations. Cortisol concentrations were not correlated with age-adjusted body mass index. Age category was correlated with δ13 C values but not with δ15 N values. CONCLUSIONS: The results of our study suggest that the cumulative stress experienced by these macaques under typical social and environmental conditions is not a significant contributor to variation in δ15 N and δ13 C values, nor does it have a significant effect on relative body mass.

Survey of Treponemal Infections in Free-Ranging and Captive Macaques, 1999-2012.

Survey results showed treponemal infection among pet macaques in Southeast Asia, a region with a high prevalence of human yaws. This finding, along with studies showing treponemal infection in nonhuman primates in Africa, should encourage a One Health approach to yaws eradication and surveillance activities, possibly including monitoring of nonhuman primates in yaws-endemic regions.

Global and local ancestry estimation in a captive baboon colony.

The last couple of decades have highlighted the importance of studying hybridization, particularly among primate species, as it allows us to better understand our own evolutionary trajectory. Here, we report on genetic ancestry estimates using dense, full genome data from 881 olive (Papio anubus), yellow (Papio cynocephalus), or olive-yellow crossed captive baboons from the Southwest National Primate Research Center. We calculated global and local ancestry information, imputed low coverage genomes (n = 830) to improve marker quality, and updated the genetic resources of baboons available to assist future studies. We found evidence of historical admixture in some putatively purebred animals and identified errors within the Southwest National Primate Research Center pedigree. We also compared the outputs between two different phasing and imputation pipelines along with two different global ancestry estimation software. There was good agreement between the global ancestry estimation software, with R2 > 0.88, while evidence of phase switch errors increased depending on what phasing and imputation pipeline was used. We also generated updated genetic maps and created a concise set of ancestry informative markers (n = 1,747) to accurately obtain global ancestry estimates.

Influenza virus infection in nonhuman primates.

To determine whether nonhuman primates are infected with influenza viruses in nature, we conducted serologic and swab studies among macaques from several parts of the world. Our detection of influenza virus and antibodies to influenza virus raises questions about the role of nonhuman primates in the ecology of influenza.

Technical note: comparison of the Maresh reference data with the who international standard for normal growth in healthy children.

The Maresh reference data on stature and long bone lengths in a sample of healthy middle-class children from Denver, Colorado [Maresh: Am J Dis Child 66 (1943) 227-257; Maresh: Am J Dis Child 89 (1955) 725-742; Maresh: Human growth and development (1970) p 155-200], have been used extensively by biological anthropologists to estimate juvenile age and body size using skeletal elements and to assess growth in skeletal series from different ethnic populations or archaeological cultural groups. How well these data reflect the potentially diverse growth patterns of healthy human populations from different geographic areas is unknown. Similarly, the efficacy of using the Maresh reference data to estimate stunting prevalence in prehistoric populations is unknown. This report presents the results from a comparison of the Maresh data on supine length and standing height to the World Health Organization (WHO) international child growth standard. The WHO growth standard is meant to depict typical human growth under optimal conditions and can be used to assess children worldwide, regardless of ethnicity and socioeconomic status. The results from this comparison indicate that although the Maresh reference data generally conform to the WHO standard, reflecting a normal human growth pattern, and therefore serve as a suitable reference for comparative studies of growth patterns, these reference data are not suitable for estimating stunting prevalence.

From the mouths of monkeys: detection of Mycobacterium tuberculosis complex DNA from buccal swabs of synanthropic macaques.

Although the Mycobacterium tuberculosis complex (MTBC) infects a third of all humans, little is known regarding the prevalence of mycobacterial infection in nonhuman primates (NHP). For more than a century, tuberculosis has been regarded as a serious infectious threat to NHP species. Advances in the detection of MTBC open new possibilities for investigating the effects of this poorly understood pathogen in diverse populations of NHP. Here, we report results of a cross-sectional study using well-described molecular methods to detect a nucleic acid sequence (IS6110) unique to the MTBC. Sample collection was focused on the oral cavity, the presumed route of transmission of MTBC. Buccal swabs were collected from 263 macaques representing 11 species in four Asian countries and Gibraltar. Contexts of contact with humans included free ranging, pets, performing monkeys, zoos, and monkey temples. Following DNA isolation from buccal swabs, the polymerase chain reaction (PCR) amplified IS6110 from 84 (31.9%) of the macaques. In general, prevalence of MTBC DNA was higher among NHP in countries where the World Health Organization reports higher prevalence of humans infected with MTBC. This is the first demonstration of MTBC DNA in the mouths of macaques. Further research is needed to establish the significance of this finding at both the individual and population levels. PCR of buccal samples holds promise as a method to elucidate the mycobacterial landscape among NHP, particularly macaques that thrive in areas of high human MTBC prevalence.

Infant and juvenile growth in ancestral Pueblo Indians.

The present study examines patterns of infant and juvenile growth in a diachronic sample of ancestral Pueblo Indians (AD 1300-1680) from the American Southwest. An assessment of growth patterns is accompanied by an evaluation of pathological conditions often considered to be indicators of nutritional deficiencies and/or gastrointestinal infections. Growth patterns and the distribution of pathological conditions are interpreted relative to culturally relevant age categories defined by Puebloan rites of passage described in the ethnographic literature. A visual comparison of growth distance curves revealed that relative to a modern comparative group our sample of ancestral Pueblo infant and juveniles exhibited faltering growth beginning soon after birth to about 5 years of age. A comparison of curves describing growth relative to adult femoral length, however, indicated reduced growth occurring later, by around 2 years of age. Similar to previous studies, we observed a high proportion of nonsurvivors exhibiting porotic cranial lesions during the first 2 years of life. Contrary to expectations, infants and juveniles without evidence of porotic cranial lesions exhibited a higher degree of stunting. Our study is generally consistent with previous research reporting poor health and high mortality for ancestral Pueblo Indian infants and juveniles. Through use of a culturally relevant context defining childhood, we argue that the observed poor health and high mortality in our sample occur before the important transition from young to older child and the concomitant initial incorporation into tribal ritual organization.

Brief communication: Sexual dimorphism of the juvenile basicranium.

The purpose of this article is to examine the level of sexual dimorphism exhibited in the foramen magnum and occipital condyles of juveniles, and to test the utility of this sexual dimorphism for estimating sex. Using five basicranial measurements taken from 36 juveniles of known sex and age from the Lisbon documented collection (Portugal), we evaluated sexual dimorphism in the juvenile cranial base. Our application of a method previously applied solely to adults indicated that the basicranium is sexually dimorphic in juveniles, with larger foramen magnum and occipital condyle dimensions observed in males. Significant univariate differences between males and females were found for length and breadth of the foramen magnum, and breadth of the left occipital condyle. Using these measurements, multivariate discriminant analysis indicated that sex was correctly assigned 75.8% of time. Obtained accuracy, however, was lower than reported by previous studies of adult samples. We suggest that this discrepancy is a result of population variability rather than age.

Latitudinal variation in cranial dimorphism in Macaca fascicularis.

This study examines latitudinal and insular variation in the expression of sexual dimorphism in cranial length in three geographical groupings of Macaca fascicularis. In addition, the relationship between cranial length dimorphism (CLD) and sex-specific size is examined. The results of the study identified a significant relationship between CLD and latitude for only one of the three geographic groupings. Sex-specific relationships between cranial length and CLD were detected. The pattern of these relationships varied by geographic grouping. This study is important because it demonstrates that despite very similar levels of CLD in a single primate species, there exists important geographic variability in the correlates of that dimorphism. I suggest that geographically varying ecological factors may influence sex-specific natural selection and the intensity of CLD in M. fascicularis. Gaining a better understanding of this geographical variability will require that future research examines morphological variation, including CLD, within its corresponding ecological and social contexts. Such research should be comparative, and incorporate multiple geographically separated populations with disparate environmental settings.

Further analysis of the population history of ancient Egyptians.

The origins of state formation in ancient Egypt have been the focus of recent research utilizing biological data to test hypotheses regarding in situ development of local groups, or large-scale in-migration, possibly by an invading army. The primary goal of the present research is to further test these hypotheses. Our secondary goal is to compare different distance measures and assess how they might affect interpretation of population history. We analyze craniodental nonmetric data using several different measures of biological distance, as well as a method for estimating group diversity using multidimensional scaling of distance estimates. Patterns of biological variation and population relationships were interpreted in temporal and geographic contexts. The results of our analyses suggest that the formation of the ancient Egyptian state likely included a substantial in situ process, with some level of contribution by outside migrants probable. The higher level of population structure in Lower Egypt, relative to Upper Egypt, suggests that such influence and migration by outsiders may not have been widespread geographically. These findings support, but serve to refine further those obtained by the second author in a previous study. Moreover, our comparison of distance measures indicates that the choice of measure can influence identification and interpretation of the microevolutionary processes shaping population history, despite being strongly correlated with one another.

Technical note: Applicability of tooth cementum annulation to an archaeological population.

The use of tooth cementum annulations for age determination has been deemed promising, exhibiting high correlations with chronological age. Despite its apparent potential, to date, the tooth cementum annulations method has been used rarely for estimating ages in archaeological populations. Here we examine the readability of cementum annulations and the consistency of age estimates using a sample of 116 adults from the Iron Gates Gorge Mesolithic/Neolithic series. Our examination of the method pointed to several sources of error that call into question the use of this method for estimating the chronological ages of archaeologically derived dental samples. The poor performance of the method in our analysis might be explained by taphonomic influences, including the effect of chemical and biological agents on dental microstructures.

Childhood immunization: Availability of primary care providers in Ontario.

OBJECTIVE: To examine childhood immunization levels relative to the number of family physicians, pediatricians, and public health nurses in Ontario. DESIGN: Retrospective comparative analysis of publicly available data on immunization coverage levels and the relative number of family physicians, pediatricians, and public health nurses. SETTING: Ontario. PARTICIPANTS: Seven-year-old children, family physicians, pediatricians, and public health nurses in Ontario. MAIN OUTCOME MEASURES: The association between immunization coverage levels and the relative number of family physicians, pediatricians, and public health nurses. RESULTS: We found correlations between immunization coverage levels and the relative number (ie, per 1000 Ontario residents) of family physicians (rho = 0.60) and pediatricians (rho = 0.70) and a lower correlation with the relative number of public health nurses (rho = 0.40), although none of these correlations was significant. A comparison of temporal trends illustrated that variation in the relative number of family physicians and pediatricians in Ontario was associated with similar variation in immunization coverage levels. CONCLUSION: Increasing the number of family physicians and pediatricians might help to boost access to immunizations and perhaps other components of cost-saving childhood preventive care.

Diverse contexts of zoonotic transmission of simian foamy viruses in Asia.

In Asia, contact between persons and nonhuman primates is widespread in multiple occupational and nonoccupational contexts. Simian foamy viruses (SFVs) are retroviruses that are prevalent in all species of nonhuman primates. To determine SFV prevalence in humans, we tested 305 persons who lived or worked around nonhuman primates in several South and Southeast Asian countries; 8 (2.6%) were confirmed SFV positive by Western blot and, for some, by PCR. The interspecies interactions that likely resulted in virus transmission were diverse; 5 macaque taxa were implicated as a potential source of infection. Phylogenetic analysis showed that SFV from 3 infected persons was similar to that from the nonhuman primate populations with which the infected persons reported contact. Thus, SFV infections are likely to be prevalent among persons who live or work near nonhuman primates in Asia.

Greater sciatic notch as a sex indicator in juveniles.

Using Schutkowski's method for juvenile sex determination (Schutkowski H. 1993. Am J Phys Anthropol 90:199-205), we evaluated the morphology of the greater sciatic notch of 56 ilia (23 females and 33 males) from a documented skeletal collection housed at the Bocage Museum in Lisbon (Portugal). After applying Schutkowski's original methodology and comparing the results with previous studies, we used age-adjusted metrical variables to describe greater sciatic notch depth, breadth, and angle. Although results of both morphological and metrical analyses did not reveal a statistically significant level of sexual analyses dimorphism, we found a strong correlation between pelvic morphology and age at death. On the basis of the obtained results, we argue that Schutkowski's morphological method does not predict sex accurately in all populations and that recorded correlation of iliac features with age needs to be further explored in the context of the ontogeny of sexual dimorphism.