Localized population divergence of vervet monkeys (Chlorocebus spp.) in South Africa: Evidence from mtDNA.

OBJECTIVE: Vervet monkeys are common in most tree-rich areas of South Africa, but their absence from grassland and semi-desert areas of the country suggest potentially restricted and mosaic local population patterns that may have relevance to local phenotype patterns and selection. A portion of the mitochondrial DNA control region was sequenced to study patterns of genetic differentiation. METHODS: DNA was extracted, and mitochondrial DNA sequences were obtained from 101 vervet monkeys at 15 localities, which represent both an extensive (widely across the distribution range) and intensive (more than one troop at most of the localities) sampling strategy. Analyses utilized Arlequin 3.1, MEGA 6, BEAST v1.5.2, and Network V3.6.1. RESULTS: The dataset contained 26 distinct haplotypes, with six populations fixed for single haplotypes. Pairwise P-distance among population pairs showed significant differentiation among most population pairs, but with nonsignificant differences among populations within some regions. Populations were grouped into three broad clusters in a maximum likelihood phylogenetic tree and a haplotype network. These clusters correspond to i) north-western, northern, and north-eastern parts of the distribution range as well as the northern coastal belt; ii) central areas of the country; and iii) southern part of the Indian Ocean coastal belt and adjacent inland areas. CONCLUSIONS: Apparent patterns of genetic structure correspond to current and past distribution of suitable habitat, geographic barriers to gene flow, geographic distance, and female philopatry. However, further work on nuclear markers and other genomic data are necessary to confirm these results.

Variation in scrotal color among widely distributed vervet monkey populations (Chlorocebus aethiops pygerythrus and Chlorocebus aethiops sabaeus).

Vervet monkeys (Chlorocebus aethiops) exhibit bright blue scrotal skin which may function to mediate social interactions by acting as a socio-sexual signal. Previous research on scrotal coloration among vervet monkeys was limited to experimental work on captive Ch. a. sabaeus, the least colorful vervet subspecies, and two field studies of the more colorful Ch. a. pygerythrus. In a study of free-ranging and captive vervet monkeys in South Africa (Ch. pygerythrus), West Africa (Ch. a. sabaeus) and the Caribbean (Ch. a. sabaeus), we examined scrotal color variation across geographically distant subspecies. We provide an exploration of how digital photographs may be used to quantify and analyze blue and green skin coloration by examining the blue-yellow opponency channel and luminance channel as color measures. We found that that at all ages the scrotal color of Ch. a. pygerythrus males was always bluer and darker than that of Ch. a. sabaeus males. Among Ch. a. pygerythrus scrotal color becomes bluer and lightens with increasing age, while the color of Ch. a. sabaeus males also lightens, but becomes less blue with increasing age. We suggest that color variation is related to maturation and may function as an age-related signal among Ch. a. pygerythrus and Ch. a. sabaeus. We also found color was related to three morphological features among adults. For Ch. a. pygerythrus, higher body weight is associated with more blue color and longer canine length is associated with lighter color. Lighter color was associated with longer body lengths among Ch. a. sabaeus. Future studies focused on color variation within age classes are needed to examine the potential signal content of color in this species.

Worldwide distribution of allelic variation at the progesterone receptor locus and the incidence of female reproductive cancers.

OBJECTIVES: Global patterns of the incidence of cancer are often attributed to environmental and lifestyle differences between regions. Less attention has been given to global patterns of allelic variation of genes that may contribute to the risk of developing cancer. METHODS: We genotyped samples from 21 populations for four variants of the progesterone receptor (PR) gene. One is an Alu insertion in intron 7 which defines the PROGINS haplotype. The others include a promoter region SNP 331+ G/A (rs10895068), a haplotype defining T/C substitution in intron 6 (rs561650), and an A/T substitution (rs608995) in the 3' untranslated region of the gene. All variants have been investigated elsewhere in association with female reproductive cancers in western populations. RESULTS: We found population differences in the frequency of each of these alleles across study populations (P < 0.01, log-likelihood G statistic, computed in FSTAT) and therefore examined the correlation between the frequency of each genetic variant and the incidence of three female reproductive cancers (breast, uterine, and ovarian) obtained from the Globocan 2008 database. Breast and ovarian cancer incidence were significantly correlated with the frequency of the Alu insertion (r = 0.86 and 0.53) and the +331 A variant (r = 0.57 and 0.73). CONCLUSIONS: Our data expand the information on genetic variation at the PR locus in non-western populations and support an argument for more work on the genetic epidemiology of cancer among nonwestern populations.

Ancient human parallel lineages within North America contributed to a coastal expansion.

Little is known regarding the first people to enter the Americas and their genetic legacy. Genomic analysis of the oldest human remains from the Americas showed a direct relationship between a Clovis-related ancestral population and all modern Central and South Americans as well as a deep split separating them from North Americans in Canada. We present 91 ancient human genomes from California and Southwestern Ontario and demonstrate the existence of two distinct ancestries in North America, which possibly split south of the ice sheets. A contribution from both of these ancestral populations is found in all modern Central and South Americans. The proportions of these two ancestries in ancient and modern populations are consistent with a coastal dispersal and multiple admixture events.

Variation in vervet (Chlorocebus aethiops) hair cortisol concentrations reflects ecological disturbance by humans.

Vervet monkeys (Chlorocebus aethiops) often live in close proximity to humans. Vervets are known to raid crops, homes and gardens in suburban areas leading to human-vervet conflict. In general, primate groups with access to human foods experience increased population densities and intra-group aggression. This suggests high stress loads for vervets living in environments with high levels of human habitat disturbance and close proximity to humans. We tested the hypothesis that populations characterized by high levels of human impact are more physiologically stressed than low human impact populations, and that this increased stress would be reflected in higher concentrations of hair cortisol. We predicted that because females would be less likely to engage in high risk foraging activities, and hence keep more distance from humans than males, their hair cortisol levels should be lower than those in males. We quantified cortisol in the hair of wild caught individuals from populations that experienced different degrees of human habitat disturbance and differences in access to human food. We found that males in high human impact groups had significantly higher hair cortisol concentrations than those in low human impact groups, although this difference was not observed in female vervets. Human impacts on vervet behavioral ecology appear to be a significant source of stress for male animals in particular.

Using the stable carbon and nitrogen isotope compositions of vervet monkeys (Chlorocebus pygerythrus) to examine questions in ethnoprimatology.

This study seeks to understand how humans impact the dietary patterns of eight free-ranging vervet monkey (Chlorocebus pygerythrus) groups in South Africa using stable isotope analysis. Vervets are omnivores that exploit a wide range of habitats including those that have been anthropogenically-disturbed. As humans encroach upon nonhuman primate landscapes, human-nonhuman primate interconnections become increasingly common, which has led to the rise of the field of ethnoprimatology. To date, many ethnoprimatological studies have examined human-nonhuman primate associations largely in qualitative terms. By using stable carbon (δ13C) and nitrogen (δ15N) isotope analysis, we use quantitative data to understand the degree to which humans impact vervet monkey dietary patterns. Based on initial behavioral observations we placed the eight groups into three categories of anthropogenic disturbance (low, mid, and high). Using δ13C and δ15N values we estimated the degree to which each group and each anthropogenically-disturbed category was consuming C4 plants (primarily sugar cane, corn, or processed foods incorporating these crops). δ13C values were significantly different between groups and categories of anthropogenic-disturbance. δ15N values were significantly different at the group level. The two vervet groups with the highest consumption of C4 plants inhabited small nature reserves, appeared to interact with humans only sporadically, and were initially placed in the mid level of anthropogenic-disturbance. However, further behavioral observations revealed that the high δ13C values exhibited by these groups were linked to previously unseen raiding of C4 crops. By revealing these cryptic feeding patterns, this study illustrates the utility of stable isotopes analysis for some ethnoprimatological questions.

Genetic diversity of North American captive-born gorillas (Gorilla gorilla gorilla).

Western lowland gorillas (Gorilla gorilla gorilla) are designated as critically endangered and wild populations are dramatically declining as a result of habitat destruction, fragmentation, diseases (e.g., Ebola) and the illegal bushmeat trade. As wild populations continue to decline, the genetic management of the North American captive western lowland gorilla population will be an important component of the long-term conservation of the species. We genotyped 26 individuals from the North American captive gorilla collection at 11 autosomal microsatellite loci in order to compare levels of genetic diversity to wild populations, investigate genetic signatures of a population bottleneck and identify the genetic structure of the captive-born population. Captive gorillas had significantly higher levels of allelic diversity (t(7) = 4.49, P = 0.002) and heterozygosity (t(7) = 4.15, P = 0.004) than comparative wild populations, yet the population has lost significant allelic diversity while in captivity when compared to founders (t(7) = 2.44, P = 0.04). Analyses suggested no genetic evidence for a population bottleneck of the captive population. Genetic structure results supported the management of North American captive gorillas as a single population. Our results highlight the utility of genetic management approaches for endangered nonhuman primate species.

Mendelian breeding units versus standard sampling strategies: Mitochondrial DNA variation in southwest Sardinia.

We report a sampling strategy based on Mendelian Breeding Units (MBUs), representing an interbreeding group of individuals sharing a common gene pool. The identification of MBUs is crucial for case-control experimental design in association studies. The aim of this work was to evaluate the possible existence of bias in terms of genetic variability and haplogroup frequencies in the MBU sample, due to severe sample selection. In order to reach this goal, the MBU sampling strategy was compared to a standard selection of individuals according to their surname and place of birth. We analysed mitochondrial DNA variation (first hypervariable segment and coding region) in unrelated healthy subjects from two different areas of Sardinia: the area around the town of Cabras and the western Campidano area. No statistically significant differences were observed when the two sampling methods were compared, indicating that the stringent sample selection needed to establish a MBU does not alter original genetic variability and haplogroup distribution. Therefore, the MBU sampling strategy can be considered a useful tool in association studies of complex traits.

Genetic analysis of early holocene skeletal remains from Alaska and its implications for the settlement of the Americas.

Mitochondrial and Y-chromosome DNA were analyzed from 10,300-year-old human remains excavated from On Your Knees Cave on Prince of Wales Island, Alaska (Site 49-PET-408). This individual's mitochondrial DNA (mtDNA) represents the founder haplotype of an additional subhaplogroup of haplogroup D that was brought to the Americas, demonstrating that widely held assumptions about the genetic composition of the earliest Americans are incorrect. The amount of diversity that has accumulated in the subhaplogroup over the past 10,300 years suggests that previous calibrations of the mtDNA clock may have underestimated the rate of molecular evolution. If substantiated, the dates of events based on these previous estimates are too old, which may explain the discordance between inferences based on genetic and archaeological evidence regarding the timing of the settlement of the Americas. In addition, this individual's Y-chromosome belongs to haplogroup Q-M3*, placing a minimum date of 10,300 years ago for the emergence of this haplogroup.

Genetic and other contributions to alcohol intake in rhesus macaques (Macaca mulatta).

BACKGROUND: The etiology of alcoholism and alcohol abuse, like many other complex diseases, is heterogeneous and multifactorial. Numerous studies demonstrate a genetic contribution to variation in the expression of alcohol-related disorders in humans. Over the past decade, nonhuman primates have emerged as a valuable model for some aspects of human alcohol abuse because of their phylogenetic proximity to humans. Long-term, longitudinal studies of rhesus macaques (Macaca mulatta) have provided much insight into environmental influences, especially early life experiences, on alcohol consumption and behavior patterns that characterize alcohol intake later in life. It is not known, however, whether there is a genetic component as well to the variation seen in alcohol consumption in rhesus macaques. A significant genetic component to variation in alcohol consumption in rhesus macaques would show for the first time that like humans, for nonhuman primates additive genetic influences are important. Moreover, their use as a model for alcohol-related disorders in humans would have even greater relevance and utility for designing experiments incorporating the expanding molecular genetics field, and allow researchers to investigate the interaction among the known environmental influences and various genotypes. METHODS: In this study, we investigate factors contributing to variation in alcohol consumption of 156 rhesus macaques collected over 10 years when subjects were adolescent in age, belonging to a single extended pedigree, with each cohort receiving identical early rearing backgrounds and subsequent treatments. To measure alcohol consumption each animal was provided unfettered simultaneous access both to an aspartame-sweetened 8.4% (v/v) alcohol-water solution, the aspartame-sweetened vehicle, and to water for 1 hour each day during the early afternoon between 13:00 and 15:00 in their home cages for a period of 5 to 7 weeks. We use multiple regression to identify factors that significantly affect alcohol consumption among these animals and a maximum likelihood program (ASReml) that, controlling for the significant factors, estimates the genetic contribution to the variance in alcohol consumption. RESULTS: Multiple regression analysis identified test cohort and rearing environment as contributing to 57 and 2%, respectively, of the total variance in alcohol consumption. Of the remaining 41% of the variance about half (19.8%) was attributable to additive genetic effects using a maximum likelihood program. CONCLUSION: This study demonstrates that, as in humans, there are additive genetic factors that contribute to variation in alcohol consumption in rhesus macaques, with other nongenetic factors accounting for substantial portions of the variance in alcohol consumption, Our findings show the presence of an additive genetic component and suggest the potential utility of the nonhuman primate as a molecular genetics tool for understanding alcohol abuse and alcoholism.

Mendelian breeding units versus standard sampling strategies: Mitochondrial DNA variation in southwest Sardinia

We report a sampling strategy based on Mendelian Breeding Units (MBUs), representing an interbreeding group of individuals sharing a common gene pool. The identification of MBUs is crucial for case-control experimental design in association studies. The aim of this work was to evaluate the possible existence of bias in terms of genetic variability and haplogroup frequencies in the MBU sample, due to severe sample selection. In order to reach this goal, the MBU sampling strategy was compared to a standard selection of individuals according to their surname and place of birth. We analysed mitochondrial DNA variation (first hypervariable segment and coding region) in unrelated healthy subjects from two different areas of Sardinia: the area around the town of Cabras and the western Campidano area. No statistically significant differences were observed when the two sampling methods were compared, indicating that the stringent sample selection needed to establish a MBU does not alter original genetic variability and haplogroup distribution. Therefore, the MBU sampling strategy can be considered a useful tool in association studies of complex traits.

The problems and promise of DNA barcodes for species diagnosis of primate biomaterials.

The Integrated Primate Biomaterials and Information Resource (www.IPBIR.org) provides essential research reagents to the scientific community by establishing, verifying, maintaining, and distributing DNA and RNA derived from primate cell cultures. The IPBIR uses mitochondrial cytochrome c oxidase subunit I sequences to verify the identity of samples for quality control purposes in the accession, cell culture, DNA extraction processes and prior to shipping to end users. As a result, IPBIR is accumulating a database of 'DNA barcodes' for many species of primates. However, this quality control process is complicated by taxon specific patterns of 'universal primer' failure, as well as the amplification or co-amplification of nuclear pseudogenes of mitochondrial origins. To overcome these difficulties, taxon specific primers have been developed, and reverse transcriptase PCR is utilized to exclude these extraneous sequences from amplification. DNA barcoding of primates has applications to conservation and law enforcement. Depositing barcode sequences in a public database, along with primer sequences, trace files and associated quality scores, makes this species identification technique widely accessible. Reference DNA barcode sequences should be derived from, and linked to, specimens of known provenance in web-accessible collections in order to validate this system of molecular diagnostics.

The structure of diversity within New World mitochondrial DNA haplogroups: implications for the prehistory of North America.

The mitochondrial DNA haplogroups and hypervariable segment I (HVSI) sequences of 1,612 and 395 Native North Americans, respectively, were analyzed to identify major prehistoric population events in North America. Gene maps and spatial autocorrelation analyses suggest that populations with high frequencies of haplogroups A, B, and X experienced prehistoric population expansions in the North, Southwest, and Great Lakes region, respectively. Haplotype networks showing high levels of reticulation and high frequencies of nodal haplotypes support these results. The haplotype networks suggest the existence of additional founding lineages within haplogroups B and C; however, because of the hypervariability exhibited by the HVSI data set, similar haplotypes exhibited in Asia and America could be due to convergence rather than common ancestry. The hypervariability and reticulation preclude the use of estimates of genetic diversity within haplogroups to argue for the number of migrations to the Americas.

Native American mtDNA prehistory in the American Southwest.

This study examines the mtDNA diversity of the proposed descendants of the multiethnic Hohokam and Anasazi cultural traditions, as well as Uto-Aztecan and Southern-Athapaskan groups, to investigate hypothesized migrations associated with the Southwest region. The mtDNA haplogroups of 117 Native Americans from southwestern North America were determined. The hypervariable segment I (HVSI) portion of the control region of 53 of these individuals was sequenced, and the within-haplogroup diversity of 18 Native American populations from North, Central, and South America was analyzed. Within North America, populations in the West contain higher amounts of diversity than in other regions, probably due to a population expansion and high levels of gene flow among subpopulations in this region throughout prehistory. The distribution of haplogroups in the Southwest is structured more by archaeological tradition than by language. Yumans and Pimans exhibit substantially greater genetic diversity than the Jemez and Zuni, probably due to admixture and genetic isolation, respectively. We find no evidence of a movement of mtDNA lineages northward into the Southwest from Central Mexico, which, in combination with evidence from nuclear markers, suggests that the spread of Uto-Aztecan was facilitated by predominantly male migration. Southern Athapaskans probably experienced a bottleneck followed by extensive admixture during the migration to their current homeland in the Southwest.