Honors & Awards

  • Ruth L. Kirschstein Postdoctoral National Research Service Award, National Institutes of Health (NIAID) (2010-2013)

Professional Education

  • Doctor of Philosophy, University of Minnesota Twin Cities (2010)
  • B.S., DePaul University (2000)

Stanford Advisors

Research & Scholarship

Current Research and Scholarly Interests

Population and evolutionary genetics, with a focus on immunogenetics (Major histocompatibility complex (MHC), and KIR genes)

Primate behavioral ecology, with a focus on mate choice and reproductive success, direct (genetic) fitness consequences to behavior kin selection and kin recognition, and parental investment


All Publications

  • Signature Patterns of MHC Diversity in Three Gombe Communities of Wild Chimpanzees Reflect Fitness in Reproduction and Immune Defense against SIVcpz. PLoS biology Wroblewski, E. E., Norman, P. J., Guethlein, L. A., Rudicell, R. S., Ramirez, M. A., Li, Y., Hahn, B. H., Pusey, A. E., Parham, P. 2015; 13 (5)


    Major histocompatibility complex (MHC) class I molecules determine immune responses to viral infections. These polymorphic cell-surface glycoproteins bind peptide antigens, forming ligands for cytotoxic T and natural killer cell receptors. Under pressure from rapidly evolving viruses, hominoid MHC class I molecules also evolve rapidly, becoming diverse and species-specific. Little is known of the impact of infectious disease epidemics on MHC class I variant distributions in human populations, a context in which the chimpanzee is the superior animal model. Population dynamics of the chimpanzees inhabiting Gombe National Park, Tanzania have been studied for over 50 years. This population is infected with SIVcpz, the precursor of human HIV-1. Because HLA-B is the most polymorphic human MHC class I molecule and correlates strongly with HIV-1 progression, we determined sequences for its ortholog, Patr-B, in 125 Gombe chimpanzees. Eleven Patr-B variants were defined, as were their frequencies in Gombe's three communities, changes in frequency with time, and effect of SIVcpz infection. The growing populations of the northern and central communities, where SIVcpz is less prevalent, have stable distributions comprising a majority of low-frequency Patr-B variants and a few high-frequency variants. Driving the latter to high frequency has been the fecundity of immigrants to the northern community, whereas in the central community, it has been the fecundity of socially dominant individuals. In the declining population of the southern community, where greater SIVcpz prevalence is associated with mortality and emigration, Patr-B variant distributions have been changing. Enriched in this community are Patr-B variants that engage with natural killer cell receptors. Elevated among SIVcpz-infected chimpanzees, the Patr-B*06:03 variant has striking structural and functional similarities to HLA-B*57, the human allotype most strongly associated with delayed HIV-1 progression. Like HLA-B*57, Patr-B*06:03 correlates with reduced viral load, as assessed by detection of SIVcpz RNA in feces.

    View details for DOI 10.1371/journal.pbio.1002144

    View details for PubMedID 26020813

  • Sexually Coercive Male Chimpanzees Sire More Offspring CURRENT BIOLOGY Feldblum, J. T., Wroblewski, E. E., Rudicell, R. S., Hahn, B. H., Paiva, T., Cetinkaya-Rundel, M., Pusey, A. E., Gilby, I. C. 2014; 24 (23): 2855-2860


    In sexually reproducing animals, male and female reproductive strategies often conflict. In some species, males use aggression to overcome female choice, but debate persists over the extent to which this strategy is successful. Previous studies of male aggression toward females among wild chimpanzees have yielded contradictory results about the relationship between aggression and mating behavior. Critically, however, copulation frequency in primates is not always predictive of reproductive success. We analyzed a 17-year sample of behavioral and genetic data from the Kasekela chimpanzee (Pan troglodytes schweinfurthii) community in Gombe National Park, Tanzania, to test the hypothesis that male aggression toward females increases male reproductive success. We examined the effect of male aggression toward females during ovarian cycling, including periods when the females were sexually receptive (swollen) and periods when they were not. We found that, after controlling for confounding factors, male aggression during a female's swollen periods was positively correlated with copulation frequency. However, aggression toward swollen females was not predictive of paternity. Instead, aggression by high-ranking males toward females during their nonswollen periods was positively associated with likelihood of paternity. This indicates that long-term patterns of intimidation allow high-ranking males to increase their reproductive success, supporting the sexual coercion hypothesis. To our knowledge, this is the first study to present genetic evidence of sexual coercion as an adaptive strategy in a social mammal.

    View details for DOI 10.1016/j.cub.2014.10.039

    View details for Web of Science ID 000345808700031

    View details for PubMedID 25454788

  • Fitness benefits of coalitionary aggression in male chimpanzees BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY Gilby, I. C., Brent, L. J., Wroblewski, E. E., Rudicell, R. S., Hahn, B. H., Goodall, J., Pusey, A. E. 2013; 67 (3): 373-381
  • Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA Degnan, P. H., Pusey, A. E., Lonsdorf, E. V., Goodall, J., Wroblewski, E. E., Wilson, M. L., Rudicell, R. S., Hahn, B. H., Ochman, H. 2012; 109 (32): 13034-13039


    The gastrointestinal tract harbors large and diverse populations of bacteria that vary among individuals and within individuals over time. Numerous internal and external factors can influence the contents of these microbial communities, including diet, geography, physiology, and the extent of contact among hosts. To investigate the contributions of such factors to the variation and changes in gut microbial communities, we analyzed the distal gut microbiota of individual chimpanzees from two communities in Gombe National Park, Tanzania. These samples, which were derived from 35 chimpanzees, many of whom have been monitored for multiple years, provide an unusually comprehensive longitudinal depth for individuals of known genetic relationships. Although the composition of the great-ape microbiota has been shown to codiversify with host species, indicating that host genetics and phylogeny have played a major role in its differentiation over evolutionary timescales, the geneaological relationships of individual chimpanzees did not coincide with the similarity in their gut microbial communities. However, the inhabitants from adjacent chimpanzee communities could be distinguished based on the contents of their gut microbiota. Despite the broad similarity of community members, as would be expected from shared diet or interactions, long-term immigrants to a community often harbored the most distinctive gut microbiota, suggesting that individuals retain hallmarks of their previous gut microbial communities for extended periods. This pattern was reinforced in several chimpanzees sampled over long temporal scales, in which the major constituents of the gut microbiota were maintained for nearly a decade.

    View details for DOI 10.1073/pnas.1110994109

    View details for Web of Science ID 000307551700044

    View details for PubMedID 22826227

  • Genetic and 'cultural' similarity in wild chimpanzees PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Langergraber, K. E., Boesch, C., Inoue, E., Inoue-Murayama, M., Mitani, J. C., Nishida, T., Pusey, A., Reynolds, V., Schubert, G., Wrangham, R. W., Wroblewski, E., Vigilant, L. 2011; 278 (1704): 408-416


    The question of whether animals possess 'cultures' or 'traditions' continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the 'method of exclusion,' begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.

    View details for DOI 10.1098/rspb.2010.1112

    View details for Web of Science ID 000285541800013

    View details for PubMedID 20719777

  • Visual Kin Recognition in Nonhuman Primates (Pan troglodytes and Macaca mulatta) Inbreeding Avoidance or Male Distinctiveness? JOURNAL OF COMPARATIVE PSYCHOLOGY Parr, L. A., Heintz, M., Lonsdorf, E., Wroblewski, E. 2010; 124 (4): 343-350


    Faces provide important information about identity, age, and even kinship. A previous study in chimpanzees reported greater similarity between the faces of mothers and sons compared with mothers and daughters, or unrelated individuals. This was interpreted as an inbreeding avoidance mechanism where females, the dispersing gender, should avoid mating with any male that resembles their mother. Alternatively, male faces may be more distinctive than female faces, biasing attention toward males. To test these hypotheses, chimpanzees and rhesus monkeys matched conspecifics' faces of unfamiliar mothers and fathers with their sons and daughters. Results showed no evidence of male distinctiveness, rather a cross-gender effect was found: chimpanzees were better matching moms with sons and fathers with daughters. Rhesus monkeys, however, showed an overwhelming bias toward male-distinctiveness. They were faster to learn male faces, performed better on father-offspring and parent-son trials, and were best matching fathers with sons. This suggests that for the rhesus monkey, inbreeding avoidance involves something other than facial phenotypic matching but that among chimpanzees, the visual recognition of facial similarities may play an important role.

    View details for DOI 10.1037/a0020545

    View details for Web of Science ID 000284672600001

    View details for PubMedID 21090888

  • Impact of Simian Immunodeficiency Virus Infection on Chimpanzee Population Dynamics PLOS PATHOGENS Rudicell, R. S., Jones, J. H., Wroblewski, E. E., Learn, G. H., Li, Y., Robertson, J. D., Greengrass, E., Grossmann, F., Kamenya, S., Pintea, L., Mjungu, D. C., Lonsdorf, E. V., Mosser, A., Lehman, C., Collins, D. A., Keele, B. F., Goodall, J., Hahn, B. H., Pusey, A. E., Wilson, M. L. 2010; 6 (9)


    Like human immunodeficiency virus type 1 (HIV-1), simian immunodeficiency virus of chimpanzees (SIVcpz) can cause CD4+ T cell loss and premature death. Here, we used molecular surveillance tools and mathematical modeling to estimate the impact of SIVcpz infection on chimpanzee population dynamics. Habituated (Mitumba and Kasekela) and non-habituated (Kalande) chimpanzees were studied in Gombe National Park, Tanzania. Ape population sizes were determined from demographic records (Mitumba and Kasekela) or individual sightings and genotyping (Kalande), while SIVcpz prevalence rates were monitored using non-invasive methods. Between 2002-2009, the Mitumba and Kasekela communities experienced mean annual growth rates of 1.9% and 2.4%, respectively, while Kalande chimpanzees suffered a significant decline, with a mean growth rate of -6.5% to -7.4%, depending on population estimates. A rapid decline in Kalande was first noted in the 1990s and originally attributed to poaching and reduced food sources. However, between 2002-2009, we found a mean SIVcpz prevalence in Kalande of 46.1%, which was almost four times higher than the prevalence in Mitumba (12.7%) and Kasekela (12.1%). To explore whether SIVcpz contributed to the Kalande decline, we used empirically determined SIVcpz transmission probabilities as well as chimpanzee mortality, mating and migration data to model the effect of viral pathogenicity on chimpanzee population growth. Deterministic calculations indicated that a prevalence of greater than 3.4% would result in negative growth and eventual population extinction, even using conservative mortality estimates. However, stochastic models revealed that in representative populations, SIVcpz, and not its host species, frequently went extinct. High SIVcpz transmission probability and excess mortality reduced population persistence, while intercommunity migration often rescued infected communities, even when immigrating females had a chance of being SIVcpz infected. Together, these results suggest that the decline of the Kalande community was caused, at least in part, by high levels of SIVcpz infection. However, population extinction is not an inevitable consequence of SIVcpz infection, but depends on additional variables, such as migration, that promote survival. These findings are consistent with the uneven distribution of SIVcpz throughout central Africa and explain how chimpanzees in Gombe and elsewhere can be at equipoise with this pathogen.

    View details for DOI 10.1371/journal.ppat.1001116

    View details for Web of Science ID 000282373000015

    View details for PubMedID 20886099

  • Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz NATURE Keele, B. F., Jones, J. H., Terio, K. A., Estes, J. D., Rudicell, R. S., Wilson, M. L., Li, Y., Learn, G. H., Beasley, T. M., Schumacher-Stankey, J., Wroblewski, E., Mosser, A., Raphael, J., Kamenya, S., Lonsdorf, E. V., Travis, D. A., Mlengeya, T., Kinsel, M. J., Else, J. G., Silvestri, G., Goodall, J., Sharp, P. M., Shaw, G. M., Pusey, A. E., Hahn, B. H. 2009; 460 (7254): 515-519


    African primates are naturally infected with over 40 different simian immunodeficiency viruses (SIVs), two of which have crossed the species barrier and generated human immunodeficiency virus types 1 and 2 (HIV-1 and HIV-2). Unlike the human viruses, however, SIVs do not generally cause acquired immunodeficiency syndrome (AIDS) in their natural hosts. Here we show that SIVcpz, the immediate precursor of HIV-1, is pathogenic in free-ranging chimpanzees. By following 94 members of two habituated chimpanzee communities in Gombe National Park, Tanzania, for over 9 years, we found a 10- to 16-fold higher age-corrected death hazard for SIVcpz-infected (n = 17) compared to uninfected (n = 77) chimpanzees. We also found that SIVcpz-infected females were less likely to give birth and had a higher infant mortality rate than uninfected females. Immunohistochemistry and in situ hybridization of post-mortem spleen and lymph node samples from three infected and two uninfected chimpanzees revealed significant CD4(+) T-cell depletion in all infected individuals, with evidence of high viral replication and extensive follicular dendritic cell virus trapping in one of them. One female, who died within 3 years of acquiring SIVcpz, had histopathological findings consistent with end-stage AIDS. These results indicate that SIVcpz, like HIV-1, is associated with progressive CD4(+) T-cell loss, lymphatic tissue destruction and premature death. These findings challenge the prevailing view that all natural SIV infections are non-pathogenic and suggest that SIVcpz has a substantial negative impact on the health, reproduction and lifespan of chimpanzees in the wild.

    View details for DOI 10.1038/nature08200

    View details for Web of Science ID 000268257000039

    View details for PubMedID 19626114

  • Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii ANIMAL BEHAVIOUR Wroblewski, E. E., Murray, C. M., Keele, B. F., Schumacher-Stankey, J. C., Hahn, B. H., Pusey, A. E. 2009; 77 (4): 873-885
  • Alpha Male Chimpanzee Grooming Patterns: Implications for Dominance "Style" AMERICAN JOURNAL OF PRIMATOLOGY Foster, M. W., Gilby, I. C., Murray, C. M., Johnson, A., Wroblewski, E. E., Pusey, A. E. 2009; 71 (2): 136-144


    In social primates, individuals use various tactics to compete for dominance rank. Grooming, displays and contact aggression are common components of a male chimpanzee's dominance repertoire. The optimal combination of these behaviors is likely to differ among males with individuals exhibiting a dominance "style" that reflects their tendency to use cooperative and/or agonistic dominance tactics. Here, we examine the grooming behavior of three alpha male chimpanzees at Gombe National Park, Tanzania. We found that (1) these males differed significantly in their tendency to groom with other males; (2) each male's grooming patterns remained consistent before, during and after his tenure as alpha, and (3) the three males tended to groom with high- middle- and low-ranking partners equally. We suggest that body mass may be one possible determinant of differences in grooming behavior. The largest male exhibited the lowest overall grooming rates, whereas the smallest male spent the most time grooming others. This is probably because large males are more effective at physically intimidating subordinates. To achieve alpha status, a small male may need to compensate for reduced size by investing more time and energy in grooming, thereby ensuring coalitionary support from others. Rates of contact aggression and charging displays conformed to this prediction, suggesting that each male exhibited a different dominance "style."

    View details for DOI 10.1002/ajp.20632

    View details for Web of Science ID 000262392200006

    View details for PubMedID 19025996

  • An unusual incident of adoption in a wild chimpanzee (Pan troglodytes) population at Gombe National Park American Journal of Primatology Wroblewski, E. E. 2008; 70

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