Publications by authors named "Alexander V Georgiev"

22 Publications

  • Page 1 of 1

CD4 receptor diversity represents an ancient protection mechanism against primate lentiviruses.

Proc Natl Acad Sci U S A 2021 Mar;118(13)

Lukuru Wildlife Research Foundation, Tshuapa-Lomami-Lualaba Project, BP 2012, Kinshasa, Democratic Republic of the Congo.

Infection with human and simian immunodeficiency viruses (HIV/SIV) requires binding of the viral envelope glycoprotein (Env) to the host protein CD4 on the surface of immune cells. Although invariant in humans, the Env binding domain of the chimpanzee CD4 is highly polymorphic, with nine coding variants circulating in wild populations. Here, we show that within-species CD4 diversity is not unique to chimpanzees but found in many African primate species. Characterizing the outermost (D1) domain of the CD4 protein in over 500 monkeys and apes, we found polymorphic residues in 24 of 29 primate species, with as many as 11 different coding variants identified within a single species. D1 domain amino acid replacements affected SIV Env-mediated cell entry in a single-round infection assay, restricting infection in a strain- and allele-specific fashion. Several identical CD4 polymorphisms, including the addition of -linked glycosylation sites, were found in primate species from different genera, providing striking examples of parallel evolution. Moreover, seven different guenons ( spp.) shared multiple distinct D1 domain variants, pointing to long-term trans-specific polymorphism. These data indicate that the HIV/SIV Env binding region of the primate CD4 protein is highly variable, both within and between species, and suggest that this diversity has been maintained by balancing selection for millions of years, at least in part to confer protection against primate lentiviruses. Although long-term SIV-infected species have evolved specific mechanisms to avoid disease progression, primate lentiviruses are intrinsically pathogenic and have left their mark on the host genome.
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http://dx.doi.org/10.1073/pnas.2025914118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8020793PMC
March 2021

Hysterangium bonobo: A newly described truffle species that is eaten by bonobos in the Democratic Republic of Congo.

Mycologia 2020 Nov-Dec;112(6):1203-1211. Epub 2020 Sep 4.

Department of Plant Pathology, University of Florida , Gainesville, Florida 32611.

Many animals have been shown to eat fungi and most truffle-like fungi depend on animals for spore dispersal via mycophagy. Although these interactions are widespread, they are understudied in many habitats. In this study, we show that bonobos () forage and feed on an undescribed truffle species in the rainforests of the Democratic Republic of Congo. Based on morphological and molecular assessment of collections, we show that the species eaten by bonobos is a previously undescribed taxon described here as . This species is known in the local Bantu language (Bongando) as simbokilo and is used for baiting traps to catch several species of small mammals. Our findings highlight the need for further research into mycophagy and systematics of sequestrate fungi in Africa.
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http://dx.doi.org/10.1080/00275514.2020.1790234DOI Listing
September 2020

Evolutionary life history theory as an organising framework for cohort studies: insights from the Cebu Longitudinal Health and Nutrition Survey.

Ann Hum Biol 2020 Mar;47(2):94-105

Department of Anthropology, Northwestern University, Evanston, IL, USA.

By tracking a group of individuals through time, cohort studies provide fundamental insights into the developmental time course and causes of health and disease. Evolutionary life history theory seeks to explain patterns of growth, development, reproduction and senescence, and inspires a range of hypotheses that are testable using the longitudinal data from cohort studies. Here we review two decades of life history theory-motivated work conducted in collaboration with the Cebu Longitudinal Health and Nutrition Survey (CLHNS), a birth cohort study that enrolled more than 3000 pregnant women in the Philippines in 1983 and has since followed these women, their offspring and grandoffspring. This work has provided evidence that reproduction carries "costs" to cellular maintenance functions, potentially speeding senescence, and revealed an unusual form of genetic plasticity in which the length of telomeres inherited across generations is influenced by reproductive timing in paternal ancestors. Men in Cebu experience hormonal and behavioural changes in conjunction with changes in relationship and fatherhood status that are consistent with predictions based upon other species that practice bi-parental care. The theoretical expectation that early life cues of mortality or environmental unpredictability will motivate a "fast" life history strategy are confirmed for behavioural components of reproductive decision making, but not for maturational tempo, while our work points to a broader capacity for early life developmental calibration of systems like immunity, reproductive biology and metabolism. Our CLHNS findings illustrate the power of life history theory as an integrative, lifecourse framework to guide longitudinal studies of human populations.
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http://dx.doi.org/10.1080/03014460.2020.1742787DOI Listing
March 2020

Experimental evidence that female rhesus macaques () perceive variation in male facial masculinity.

R Soc Open Sci 2019 Jan 30;6(1):181415. Epub 2019 Jan 30.

Department of Anthropology, New York University, 25 Waverly Place, New York, NY 10003, USA.

Among many primate species, face shape is sexually dimorphic, and male facial masculinity has been proposed to influence female mate choice and male-male competition by signalling competitive ability. However, whether conspecifics pay attention to facial masculinity has only been assessed in humans. In a study of free-ranging rhesus macaques, , we used a two-alternative look-time experiment to test whether females perceive male facial masculinity. We presented 107 females with pairs of images of male faces-one with a more masculine shape and one more feminine-and recorded their looking behaviour. Females looked at the masculine face longer than at the feminine face in more trials than predicted by chance. Although there was no overall difference in average look-time between masculine and feminine faces across all trials, females looked significantly longer at masculine faces in a subset of trials for which the within-pair difference in masculinity was most pronounced. Additionally, the proportion of time subjects looked toward the masculine face increased as the within-pair difference in masculinity increased. This study provides evidence that female macaques perceive variation in male facial shape, a necessary condition for intersexual selection to operate on such a trait. It also highlights the potential impact of perceptual thresholds on look-time experiments.
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http://dx.doi.org/10.1098/rsos.181415DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6366174PMC
January 2019

Is male rhesus macaque facial coloration under intrasexual selection?

Behav Ecol 2017 Nov-Dec;28(6):1472-1481. Epub 2017 Sep 11.

Department of Anthropology, New York University, 25 Waverly Pl, New York, NY 10003, USA.

Exaggerated male traits can evolve under intra- or intersexual selection, but it remains less clear how often both mechanisms act together on trait evolution. While the males of many anthropoid primate species exhibit colorful signals that appear to be badges of status under intrasexual selection, the red facial coloration of male rhesus macaques () appears to have evolved primarily under intersexual selection and female mate choice. Nonetheless, experiments show that red color is salient to males, raising the question of whether the signal may also be under intrasexual selection. Here, we examine whether males express this signal more strongly in competitive contexts. Facial images were collected on all 15 adult males of a free-ranging social group during the peak of the mating season, and coloration was quantified using visual models. Results show that males more similar in facial redness were more likely to interact aggressively than more dissimilar ones, suggesting that color may be involved in the assessment of rivals. Furthermore, males exhibited darker coloration on days they were observed copulating, and dominance rank predicted facial redness only on copulating days, suggesting that coloration may also advertise motivation to defend a mate. Male rhesus macaque facial coloration may thus mediate agonistic interactions with rivals during competition over reproductive opportunities, such that it is under both inter- and intrasexual selection. However, color differences were small, raising perceptibility questions. It remains possible that color variation reflects differences in male condition, which in turn alter investment towards male-male competition and mating effort.
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http://dx.doi.org/10.1093/beheco/arx110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5872909PMC
September 2017

Allometry and Ecology of the Bilaterian Gut Microbiome.

mBio 2018 03 27;9(2). Epub 2018 Mar 27.

Division of Gastroenterology, Hepatology, and Nutrition, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.

Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. Here, we investigated the influence of several well-known ecological principles on animal-associated microbiota by characterizing gut microbial specimens from bilaterally symmetrical animals () ranging from flies to whales. A rigorously vetted sample set containing 265 specimens from 64 species was assembled. Bacterial lineages were characterized by 16S rRNA gene sequencing. Previously published samples were also compared, allowing analysis of over 1,098 samples in total. A restricted number of bacterial phyla was found to account for the great majority of gut colonists. Gut microbial composition was associated with host phylogeny and diet. We identified numerous gut bacterial 16S rRNA gene sequences that diverged deeply from previously studied taxa, identifying opportunities to discover new bacterial types. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. Samples from larger animals harbored greater numbers of anaerobic communities, specifying a mechanism for generating more-complex microbial environments. Predictions for species/abundance relationships from models of neutral colonization did not match the data set, pointing to alternative mechanisms such as selection of specific colonists by environmental niche. Taken together, the data suggest that niche complexity increases with gut size and that niche selection forces dominate gut community construction. The intestinal microbiome of animals is essential for health, contributing to digestion of foods, proper immune development, inhibition of pathogen colonization, and catabolism of xenobiotic compounds. How these communities assemble and persist is just beginning to be investigated. Here we interrogated a set of gut samples from a wide range of animals to investigate the roles of selection and random processes in microbial community construction. We show that the numbers of bacterial species increased with the weight of host organisms, paralleling findings from studies of island biogeography. Communities in larger organisms tended to be more anaerobic, suggesting one mechanism for niche diversification. Nonselective processes enable specific predictions for community structure, but our samples did not match the predictions of the neutral model. Thus, these findings highlight the importance of niche selection in community construction and suggest mechanisms of niche diversification.
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http://dx.doi.org/10.1128/mBio.00319-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5874926PMC
March 2018

Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species.

Nat Commun 2017 11 21;8(1):1635. Epub 2017 Nov 21.

Department of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.

Malaria parasites, though widespread among wild chimpanzees and gorillas, have not been detected in bonobos. Here, we show that wild-living bonobos are endemically Plasmodium infected in the eastern-most part of their range. Testing 1556 faecal samples from 11 field sites, we identify high prevalence Laverania infections in the Tshuapa-Lomami-Lualaba (TL2) area, but not at other locations across the Congo. TL2 bonobos harbour P. gaboni, formerly only found in chimpanzees, as well as a potential new species, Plasmodium lomamiensis sp. nov. Rare co-infections with non-Laverania parasites were also observed. Phylogenetic relationships among Laverania species are consistent with co-divergence with their gorilla, chimpanzee and bonobo hosts, suggesting a timescale for their evolution. The absence of Plasmodium from most field sites could not be explained by parasite seasonality, nor by bonobo population structure, diet or gut microbiota. Thus, the geographic restriction of bonobo Plasmodium reflects still unidentified factors that likely influence parasite transmission.
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http://dx.doi.org/10.1038/s41467-017-01798-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5696340PMC
November 2017

Alpha male status and availability of conceptive females are associated with high glucocorticoid concentrations in high-ranking male rhesus macaques (Macaca mulatta) during the mating season.

Horm Behav 2018 01 14;97:5-13. Epub 2017 Oct 14.

Institute for Mind and Biology, The University of Chicago, USA.

The relationship between male mating opportunities, stress, and glucocorticoid concentrations is complicated by the fact that physiological stress and glucocorticoid concentrations can be influenced by dominance rank, group size, and the stability of the male dominance hierarchy, along with ecological factors. We studied the three highest-ranking males in nine different social groups within the same free-ranging population of rhesus macaques on Cayo Santiago, Puerto Rico, during the mating season, to examine variation in glucocorticoid concentrations in relation to number of females that conceived each month, alpha status, number of adult males in a group, and male rank hierarchy stability. We found that glucocorticoid concentrations were highest in the early mating season period when more females conceived in each group and declined linearly as the mating season progressed and the number of conceptive females decreased. Alpha males had significantly higher mean monthly glucocorticoid concentrations than other high-ranking males throughout the study period. Male age, number of adult males in a group, and hierarchy stability were not significantly associated with glucocorticoid concentrations. Our findings suggest that alpha males may experience significantly higher levels of physiological stress than their immediate subordinates and that this stress coincides with the period of the mating season when most conceptions occur.
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http://dx.doi.org/10.1016/j.yhbeh.2017.09.014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6180231PMC
January 2018

Is early postnatal growth velocity, a proxy of minipubertal androgen action, related to adult second-to-fourth digit (2D:4D) ratios in men? A test in Cebu, Philippines.

Am J Hum Biol 2017 Nov 31;29(6). Epub 2017 Jul 31.

Department of Anthropology, Northwestern University, 1810 Hinman Avenue, Evanston, Illinois, 60208.

Objectives: The ratio of the length of the second to the fourth digit (2D:4D) of the hand is often used as an index of prenatal androgen exposure but it might also be affected by androgens during "minipuberty," a period of temporarily high testosterone (T) production in the first few months of life. To examine this, we tested the prediction that men with lower 2D:4D ratios had greater weight growth velocities during the first months of life-a metric recently shown to correlate with concurrent T levels.

Methods: We related early growth data to 2D:4D ratios of both hands measured in 756 men (25-26 years) from Cebu, The Philippines.

Results: Birth-to-fourth-month (B4M) weight gain velocity (a proxy of early postnatal androgen action) was not associated with adult 2D:4D ratios of either hand, when the latter was measured continuously. When comparing men with more male-typical digit ratios (<1.0) to those with more female-typical ratios (≥ 1.0), the group of men with more male-typical ratios had greater B4M weight velocity, but this was only the case for the left hand.

Conclusions: We found modest evidence that adult digit ratios relate to an anthropometric correlate of androgen exposure during minipuberty. Definitive assessment of the role of postnatal T in shaping digit ratios will require direct measures of perinatal T related to longitudinally assessed digit ratios.
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http://dx.doi.org/10.1002/ajhb.23047DOI Listing
November 2017

Bonobos Maintain Immune System Diversity with Three Functional Types of MHC-B.

J Immunol 2017 May 27;198(9):3480-3493. Epub 2017 Mar 27.

Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305;

Fast-evolving MHC class I polymorphism serves to diversify NK cell and CD8 T cell responses in individuals, families, and populations. Because only chimpanzee and bonobo have strict orthologs of all , their study gives unique perspectives on the human condition. We defined polymorphism of , the bonobo ortholog of , for six wild bonobo populations. Sequences for exon 2 and 3 were determined from the genomic DNA in 255 fecal samples, minimally representing 110 individuals. Twenty-two alleles were defined, each encoding a different Papa-B protein. No Papa-B is identical to any chimpanzee Patr-B, human HLA-B, or gorilla Gogo-B. Phylogenetic analysis identified a clade of MHC-B, defined by residues 45-74 of the α domain, which is broadly conserved among bonobo, chimpanzee, and gorilla. Bonobo populations have 3-14 Papa-B allotypes. Three Papa-B are in all populations, and they are each of a different functional type: allotypes having the Bw4 epitope recognized by killer cell Ig-like receptors of NK cells, allotypes having the C1 epitope also recognized by killer cell Ig-like receptors, and allotypes having neither epitope. For population Malebo, these three Papa-B are the only Papa-B allotypes. Although small in number, their sequence divergence is such that the nucleotide diversity (mean proportional distance) of in Malebo is greater than in the other populations and is also greater than expected for random combinations of three Overall, has substantially less diversity than in chimpanzee subspecies and in indigenous human populations, consistent with bonobo having experienced narrower population bottlenecks.
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http://dx.doi.org/10.4049/jimmunol.1601955DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5469624PMC
May 2017

Second-to-fourth digit ratio (2D:4D) is unrelated to measures of somatic reproductive effort among young men from Cebu, the Philippines.

Am J Phys Anthropol 2017 07 27;163(3):437-445. Epub 2017 Mar 27.

Department of Anthropology, Northwestern University, Evanston, Illinois.

Objectives: A low second-to-fourth (2D:4D) digit ratio, a retrospective marker of high prenatal androgens, predicts increased investment in costly sexually dimorphic traits in men in some studies, although results are mixed. Here we test the hypothesis that the association of low 2D:4D ratios with increased muscularity and decreased adiposity depends on current testosterone (T) levels, such that digit ratio will be a particularly strong predictor of outcomes among men exhibiting a mating-effort-oriented endocrinological profile (high T). We also test the association between 2D:4D and somatic traits independently of T.

Materials And Methods: We related 2D:4D digit ratios, and their interaction with T, to handgrip strength, lean mass, arm muscle area, and skinfold thickness in a sample of young, childess men (20-22 y) from Cebu, Philippines (N = 623).

Results: Digit ratio did not significantly predict men's T-dependent somatic traits. Interactions between 2D:4D and morning T, similarly, did not predict male muscularity or adiposity. Although two of the interactions were significant or marginally significant (p < .1), after adjusting for multiple testing the evidence in support of our hypothesis was weak.

Discussion: We found no evidence that 2D:4D predicted measures of somatic reproductive effort in this sample of young men from Cebu, who as a group could be considered mostly mating-oriented. These relationships were also not contingent upon, or stronger, when considering the moderating effect of concurrent T levels. In this sample, 2D:4D was therefore either a poor proxy of prenatal androgen exposure or prenatal androgens had limited influence on adult somatic outcomes.
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http://dx.doi.org/10.1002/ajpa.23215DOI Listing
July 2017

Androgen receptor polyglutamine repeat length (AR-CAGn) modulates the effect of testosterone on androgen-associated somatic traits in Filipino young adult men.

Am J Phys Anthropol 2017 06 14;163(2):317-327. Epub 2017 Mar 14.

Department of Anthropology, Northwestern University, Evanston, Illinois.

Objectives: The androgen receptor (AR) mediates expression of androgen-associated somatic traits such as muscle mass and strength. Within the human AR is a highly variable glutamine short-tandem repeat (AR-CAGn), and CAG repeat number has been inversely correlated to AR transcriptional activity in vitro. However, evidence for an attenuating effect of long AR-CAGn on androgen-associated somatic traits has been inconsistent in human populations. One possible explanation for this lack of consistency is that the effect of AR-CAGn on AR bioactivity in target tissues likely varies in relation to circulating androgen levels.

Materials And Methods: We tested whether relationships between AR-CAGn and several androgen-associated somatic traits (waist circumference, lean mass, arm muscle area, and grip strength) were modified by salivary (waking and pre-bed) and circulating (total) testosterone (T) levels in young adult males living in metropolitan Cebu, Philippines (n = 675).

Results: When men's waking T was low, they had a reduction in three out of four androgen-associated somatic traits with lengthening AR-CAGn (p < .1), consistent with in vitro research. However, when waking T was high, we observed the opposite effect-lengthening AR-CAGn was associated with an increase in these same somatic traits.

Discussion: Our finding that longer AR-CAGn predicts greater androgen-associated trait expression among high-T men runs counter to in vitro work, but is generally consistent with the few prior studies to evaluate similar interactions in human populations. Collectively, these results raise questions about the applicability of findings derived from in vitro AR-CAGn studies to the receptor's role in maintaining androgen-associated somatic traits in human populations.
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http://dx.doi.org/10.1002/ajpa.23208DOI Listing
June 2017

Genetic diversity of STLV-2 and interspecies transmission of STLV-3 in wild-living bonobos.

Virus Evol 2016 Jan 25;2(1):vew011. Epub 2016 May 25.

Unité Mixte Internationale 233, Institut de Recherche pour le Développement, INSERM U1175, and University of Montpellier, Montpellier, 34394, France.

There are currently four known primate T-cell lymphotropic virus groups (PTLV1-4), each of which comprises closely related simian (STLV) and human (HTLV) viruses. For PTLV-1 and PTLV-3, simian and human viruses are interspersed, suggesting multiple cross-species transmission events; however, for PTLV-2 this is not so clear because HTLV-2 and STLV-2 strains from captive bonobos () form two distinct clades. To determine to what extent bonobos are naturally infected with STLV, we screened fecal samples (n = 633) from wild-living bonobos (n = 312) at six different sites in the Democratic Republic of Congo (DRC) for the presence of STLV nucleic acids. STLV infection was detected in 8 of 312 bonobos at four of six field sites, suggesting an overall prevalence of 2.6% (ranging from 0 to 8%). Six samples contained STLV-2, while the two others contained STLV-3, as determined by phylogenetic analysis of partial and Long Terminal Repeats (LTR) sequences. The new STLV-2 sequences were highly diverse, but grouped with previously identified STLV-2 strains as a sister clade to HTLV-2. In contrast, the new STLV-3 sequences did not cluster together, but were more closely related to STLVs from sympatric monkey species. These results show for the first time that fecal samples can be used to detect STLV infection in apes. These results also show that wild-living bonobos are endemically infected with STLV-2, but have acquired STLV-3 on at least two occasions most likely by cross-species transmission from monkey species on which they prey. Future studies of bonobos and other non-human primate species in Central Africa are needed to identify the simian precursor of HTLV-2 in humans.
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http://dx.doi.org/10.1093/ve/vew011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4900509PMC
January 2016

Early developmental exposures shape trade-offs between acquired and innate immunity in humans.

Evol Med Public Health 2016 24;2016(1):256-69. Epub 2016 Aug 24.

Department of Anthropology, Northwestern University, Evanston, IL 60208, USA.

Background And Objectives: Life history theory predicts resource allocation trade-offs between competing functions and processes. We test the hypothesis that relative investment towards innate versus acquired immunity in humans is subject to such trade-offs and that three types of early developmental exposures are particularly salient in shaping adult immunophenotype: (i) pathogen exposure, (ii) nutritional resources; and (iii) extrinsic mortality cues.

Methodology: We quantified one aspect each of innate and acquired immune function, via C-reactive protein and Epstein-Barr virus antibodies, respectively, in a sample of 1248 men and women from the Philippines (ca. 21.5 years old). Early developmental exposures were assessed via long-term data collected prospectively since participants' birth (1983-4). We calculated a standardized ratio to assess relative bias towards acquired versus innate immune function and examined its relationship to a suite of predictors via multiple regression.

Results: In partial support of our predictions, some of the measures of higher pathogen exposure, greater availability of nutritional resources, and lower extrinsic mortality cues in early life were associated with a bias toward acquired immunity in both men and women. The immune profile of women, in particular, appeared to be more sensitive to early life pathogen exposures than those of men. Finally, contrary to prediction, women exhibited a greater relative investment toward innate, not acquired, immunity.

Conclusions And Implications: Early environments can exert considerable influence on the development of immunity. They affect trade-offs between innate and acquired immunity, which show adaptive plasticity and may differ in their influence in men and women.
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http://dx.doi.org/10.1093/emph/eow022DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4996124PMC
August 2016

Cospeciation of gut microbiota with hominids.

Science 2016 Jul;353(6297):380-2

Department of Integrative Biology, 2506 Speedway A5000, University of Texas at Austin, Austin, TX 78712, USA.

The evolutionary origins of the bacterial lineages that populate the human gut are unknown. Here we show that multiple lineages of the predominant bacterial taxa in the gut arose via cospeciation with humans, chimpanzees, bonobos, and gorillas over the past 15 million years. Analyses of strain-level bacterial diversity within hominid gut microbiomes revealed that clades of Bacteroidaceae and Bifidobacteriaceae have been maintained exclusively within host lineages across hundreds of thousands of host generations. Divergence times of these cospeciating gut bacteria are congruent with those of hominids, indicating that nuclear, mitochondrial, and gut bacterial genomes diversified in concert during hominid evolution. This study identifies human gut bacteria descended from ancient symbionts that speciated simultaneously with humans and the African apes.
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http://dx.doi.org/10.1126/science.aaf3951DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4995445PMC
July 2016

Trade-offs between acquired and innate immune defenses in humans.

Evol Med Public Health 2016 6;2016(1):1-16. Epub 2016 Jan 6.

Department of Anthropology, Institute for Policy Research, Northwestern University, Evanston, IL 60208.

Immune defenses provide resistance against infectious disease that is critical to survival. But immune defenses are costly, and limited resources allocated to immunity are not available for other physiological or developmental processes. We propose a framework for explaining variation in patterns of investment in two important subsystems of anti-pathogen defense: innate (non-specific) and acquired (specific) immunity. The developmental costs of acquired immunity are high, but the costs of maintenance and activation are relatively low. Innate immunity imposes lower upfront developmental costs, but higher operating costs. Innate defenses are mobilized quickly and are effective against novel pathogens. Acquired responses are less effective against novel exposures, but more effective against secondary exposures due to immunological memory. Based on their distinct profiles of costs and effectiveness, we propose that the balance of investment in innate versus acquired immunity is variable, and that this balance is optimized in response to local ecological conditions early in development. Nutritional abundance, high pathogen exposure and low signals of extrinsic mortality risk during sensitive periods of immune development should all favor relatively higher levels of investment in acquired immunity. Undernutrition, low pathogen exposure, and high mortality risk should favor innate immune defenses. The hypothesis provides a framework for organizing prior empirical research on the impact of developmental environments on innate and acquired immunity, and suggests promising directions for future research in human ecological immunology.
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http://dx.doi.org/10.1093/emph/eov033DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4703052PMC
January 2016

Oxidative stress as an indicator of the costs of reproduction among free-ranging rhesus macaques.

J Exp Biol 2015 Jul 23;218(Pt 13):1981-5. Epub 2015 Apr 23.

Institute for Mind and Biology, The University of Chicago, 940 E 57th St, Chicago, IL 60637, USA.

Sex differences in longevity may reflect sex-specific costs of intra-sexual competition and reproductive effort. As male rhesus macaques experience greater intrasexual competition and die younger, we predicted that males would experience greater oxidative stress than females and that oxidative stress would reflect sex-specific measures of reproductive effort. Males, relative to females, had higher concentrations of 8-OHdG and malondialdehyde, which are markers of DNA oxidative damage and lipid peroxidation, respectively. Older macaques had lower 8-OHdG levels than younger ones, suggesting that oxidative stress decreases in parallel with known age-related declines in reproductive investment. Among males, a recent period of social instability affected oxidative status: males who attacked others at higher rates had higher 8-OHdG levels. Multiparous lactating females with daughters had higher 8-OHdG levels than those with sons. No differences in antioxidant capacity were found. These results lend initial support for the use of oxidative stress markers to assess trade-offs between reproductive effort and somatic maintenance in primates.
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http://dx.doi.org/10.1242/jeb.121947DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4510843PMC
July 2015

What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago.

Am J Primatol 2016 Jan 16;78(1):92-105. Epub 2015 Jan 16.

University of Chicago, Chicago, Illinois.

Research with the rhesus macaque population on Cayo Santiago can provide a unique perspective on the costs of sociality and reproduction in primates. Because the Cayo macaques live in unusually large groups and in a predator-free environment, in which their artificial food source lacks seasonal variation in abundance or quality, these monkeys constitute a semi-experimental study of the costs and benefits of group living. Here we review several long- and short-term studies that have focused on female life history and stress physiology. Long-term demographic data have shown that rhesus macaque females of middle- and low-ranking matrilines have lower adult survival probabilities than females of high-ranking matrilines. Costs of reproductive effort are also evident: adult females were more likely to die during the birth than during the mating season and they experienced higher cortisol levels when lactating. Lower-ranking females, in particular, experienced greater relative increase in cortisol production during lactation, in comparison to middle- and high-ranking females. Older high-ranking females had lower plasma cortisol levels than younger ones but cortisol levels were similarly high among young and old middle- and low-ranking females. Higher plasma cortisol levels and/or fecal glucocorticoid concentrations are associated with higher plasma concentrations of some proinflammatory cytokines. High cortisol, in turn, may be associated with chronic inflammation, and perhaps also with immunosuppression. In sum, the studies reviewed here provide multiple lines of evidence that sociality and reproductive effort impose measurable costs on female rhesus macaques. In line with socio-ecological theory, female dominance rank consistently emerges as an important modulator of variation in female life histories and physiology. The Cayo Santiago macaques are therefore a valuable model for elucidating the mechanisms by which within-group competition and reproduction impact health and survival in nonhuman primates and in humans.
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http://dx.doi.org/10.1002/ajp.22368DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4627861PMC
January 2016

African origin of the malaria parasite Plasmodium vivax.

Nat Commun 2014 ;5:3346

Division of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK.

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.
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http://dx.doi.org/10.1038/ncomms4346DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4089193PMC
November 2015

When violence pays: a cost-benefit analysis of aggressive behavior in animals and humans.

Evol Psychol 2013 Jul 18;11(3):678-99. Epub 2013 Jul 18.

Institute for Mind and Biology, The University of Chicago, Illinois, USA..

An optimization analysis of human behavior from a comparative perspective can improve our understanding of the adaptiveness of human nature. Intra-specific competition for resources provides the main selective pressure for the evolution of violent aggression toward conspecifics, and variation in the fitness benefits and costs of aggression can account for inter-specific and inter-individual differences in aggressiveness. When aggression reflects competition for resources, its benefits vary in relation to the characteristics of the resources (their intrinsic value, abundance, spatial distribution, and controllability) while its costs vary in relation to the characteristics of organisms and how they fight (which, in turn, affects the extent to which aggression entails risk of physical injury or death, energetic depletion, exposure to predation, psychological and physiological stress, or damage to social relationships). Humans are a highly aggressive species in comparison to other animals, probably as a result of an unusually high benefit-to-cost ratio for intra-specific aggression. This conclusion is supported by frequent and widespread occurrence of male-male coalitionary killing and by male-female sexual coercion. Sex differences in violent aggression in humans and other species probably evolved by sexual selection and reflect different optimal competitive strategies for males and females.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3859192PMC
July 2013

Seed predation by bonobos (Pan paniscus) at Kokolopori, Democratic Republic of the Congo.

Primates 2011 Oct 10;52(4):309-14. Epub 2011 Aug 10.

Department of Human Evolutionary Biology, Harvard University, Peabody Museum, 11 Divinity Ave, Cambridge, MA 02138, USA.

We compared the feeding ecology of the Hali-Hali community of bonobos (Pan paniscus) at Kokolopori, a new field site in the Democratic Republic of the Congo, between two periods 5 months apart. During the first study period (SP1), bonobos relied heavily on the dry seeds of Guibourtia (Caesalpiniaceae), mostly eaten from the ground. The second period (SP2) was characterized by high consumption of ripe tree fruit. Terrestrial herbaceous vegetation (THV) contributed little to the diet in either study period. The low amount of ripe fruit and the high reliance on seeds in the diet during SP1 were associated with high cortisol production and low levels of urinary C-peptide in females, suggesting nutritional stress. However, female gregariousness was not constrained during the fruit-poor period, probably because high seed abundance on the ground ameliorated scramble feeding competition. This is the first description of extensive seed predation by bonobos. It suggests that bonobo feeding ecology may be more similar to that of chimpanzees than previously recognized.
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http://dx.doi.org/10.1007/s10329-011-0256-4DOI Listing
October 2011

Origin of the human malaria parasite Plasmodium falciparum in gorillas.

Nature 2010 Sep;467(7314):420-5

Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama 35294, USA.

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.
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http://dx.doi.org/10.1038/nature09442DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2997044PMC
September 2010