Research in the Snyder-Mackler (SMack) lab in the School of Life Sciences and Center for Evolution and Medicine at Arizona State University sits at the nexus of the social environment and the genome. We use molecular genetic techniques to probe the dynamic interaction between the social environment and the genome with the aim of understanding the fitness consequences of behavioral variation.


Join us: We’re always looking for talented researchers – from PhDs to high school students – to join our lab. If you think what we do is interesting and want to be part of our team, please fill out this google form and I’ll be in touch.

Read on to learn more about our team and what we do!

Team

Our team is a community, and we expect community members to contribute to a friendly, safe, equitable, and welcoming environment. Everyone agrees to (1) maintain a collaborative atmosphere and learn from one another, (2) treat one another with respect, combat discrimination, and ensure that people of (including but not limited to) all races, gender-identities, national origins, ethnicities, religions, citizen statuses, ages, sexual orientations, ability statuses, physical appearances, and socioeconomic statuses are and feel equally welcome and valued, and (3) stand up for one another in the face of bias, harassment, discrimination. We agree to communicate about failures in these commitments, either directly and/or through ASU’s reporting mechanism.

Lab Alumni

Research

Broadly, our lab investigates the causes and consequences of variation in the social environment from the molecular to the organismal levels. Our work involves a few complementary study systems, which allow us to probe questions central to human health, aging, and evolutionary biology.

Rhesus macaques

Studies of social environmental effects can be difficult to interpret due to the complexity of the human social environment and the inability, due to ethical concerns, to perform experimental manipulations. This has led many researchers to turn to our close genetic relatives, nonhuman primates. Rhesus macaques (Macaca mulatta) are a particularly important model for human social behavior, health, and aging because they exhibit strikingly similar age-related changes in physiological, cognitive, and immune function, but compacted into a lifespan that is 3-4 times shorter. As in humans, the social environment has also been linked to mortality in some nonhuman primates, including close relatives of macaques.

Social environmental modifiers of aging.

More socially integrated individuals are healthier and live longer, and this association is the strongest in the oldest individuals in a population.  To identify the molecular underpinnings of this link, we draw behavioral and genomic data from both captive and free-ranging macaques. We merge cutting-edge functional genomic analyses with behavioral observation methods to study how behavioral variation might insulate individuals from the detrimental effects of social stress on health. This research has implications for understanding how social stress recapitulates, or even accelerates, the changes seen during normal aging. More broadly, identifying the molecular phenotypes on which natural selection acts will lead to a better understanding of both the evolution of affiliative social behaviors and the well-documented link between sociality and components of fitness.

Single cell atlas of the rhesus macaque brain.

New technologies are enabling molecular profiling of single brain cells at remarkable throughput. However, these new methods have yet to be extensively applied to the brains of model organisms that bridge the evolutionary distance between mouse and human, including the most common nonhuman primate model system – the rhesus macaque. As part of the Brain Initiative’s Cell Census Network, we are generating an anatomically resolved, single cell gene regulatory atlas of the rhesus macaque brain. This comprehensive atlas will allow us to characterize natural variation in chromatin accessibility and transcription within each cell type, between individuals, sexes, and across the natural lifespan of rhesus macaques. We anticipate that our atlas will be an essential resource, complementary to other efforts, for identifying the distribution and function of key cell types across the primate brain, allowing for the development of cell type- and region-specific molecular interventions that will help us understand brain function and the etiology, and potentially the treatment, of brain disorders.

Funding: NIH R00-AG051764; R01-AG060931, U01-MH121260

Collaborators: Lauren Brent, James Higham, Michael Platt, Jay Shendure, Mike Montague

Gelada monkeys

If you are ever in the Ethiopia, you might find yourself surrounded by thousands of some of the most unique primates on the planet – gelada monkeys. These monkeys are often erroneously called ‘bleeding heart baboons’. Not because they don’t have blazingly red chests (they do!), but because geladas are not actually baboons – just close relatives that diverged ~3-5 million years ago. Historically, monkeys from the geladas’ genus, Theropithecus, ranged across East Africa. Now, it’s just the gelada monkey, Theropithecus gelada, found only in the highlands of Ethiopia — one of our two primary study species.

The immunogenomic consequences of sociality

As part of the Simien Mountains Gelada Research Project, we study how the highly social lives of geladas influences their health, reproduction, and survival. To do so, we draw on over a decade of demographic and behavioral data and combine it with genomic analyses: from whole genome sequencing to quantifying the microbes in the gut. Here, we can take findings from captive populations and extend them to the field to see how social integration may buffer individuals against more naturalistic stressors in the wild.

High altitude adaptation

One of the primary reasons that geladas endured – unlike their extinct Theropithecus relatives – is due to a panoply of unique adaptations to their resource-scarce, high altitude environment. In the thin air of the gelada’s habitat (≥ 3,000m above sea level), there is a dearth of nutrient rich foods. So the geladas depend almost entirely on the grasses that fill the plateaus – much like a cow. Graminivory is just one of the many gelada adaptations to their high-altitude environment. Others include their ability to thrive so high above sea level. Have geladas converged on similar high altitude adaptions that are also found in the genomes of people living in the Andes or Himalayas? Or has selection led to unique changes specific only to the gelada? In this line of work we aim to identify signatures of high altitude adaptation in the gelada monkey genome using samples collected across Ethiopia.

Funding: NSF BCS-2013888, BCS-2010309

Collaborators: Thore Bergman, Jacinta BeehnerAmy Lu, Laurie Reitsema

Dogs

Who doesn’t love dogs? We’re part of the Dog Aging Project where we are trying to understand what makes dogs tick (and age). Our lab uses molecular tools to try and identify how age and the environment interact to alter the dog immune system. 

Funding: NIH U19-AG057377

Collaborators: Daniel Promislow, Evan MacLean

Publications

lab members highlighted in bold

Pre-prints

Baniel A, Amato KR, Beehner JC, Bergman TJ, Mercer A, Perlman RF, Petrullo L, Reitsema L, Sams S, Lu A, Snyder-Mackler N. “Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas.” bioRxiv, doi: 10.1101/2020.07.07.192336

Johnson CSC, Shively CA, Michalson KT, Lea AJ, DeBo RJ, Howard TD, Hawkins GA, Appt SE, Liu Y, McCall CE, Herrington D, Register TC*,  Snyder-Mackler N*. “Divergent effects of Western and Mediterranean diets on behavior and monocyte polarization.” bioRxiv, doi:10.1101/2020.01.27.917567.

Tinsley Johnson E*, Snyder-Mackler N*, Lu A, Bergman TJ, Beehner JC (2018). “The Goldilocks Effect: Female geladas in mid-sized groups have higher fitness.” 

Peer reviewed

Shively CA, Appt SE, Chen H, Day SM, Shaltout HA, Silverstein-Meltzer MG, Snyder-Mackler, Uberseder B, Vitolins MZ, Register TC “Mediterranean diet, stress resilience, and aging in a nonhuman primate.” Neurobiology of Stress, doi: 10.1016/j.ynstr.2020.100254

Lu A, Feder JA, Snyder-Mackler N, Bergman TJ, Beehner JC. “Male-mediated maturation in a wild primate.” Current Biology, accepted. preprint: 10.1101/2020.05.25.114934

Chiou KL, Montague MJ, Goldman EA, Watowich MM, Sams SN, Song J, Horvath JE, Sterner KN, Ruiz-Lambides AV, Martinez MI, Higham JP, Brent LJN, Platt ML, Snyder-Mackler N (2020). “Rhesus macaques as a tractable physiological model of human ageing.” Philosophical Transactions of the Royal Society B, 367:11. doi: 10.1098/rstb.2019.0612 preprint: 10.1101/2020.06.10.143669v1 

Emery Thompson M, Rosati AG, Snyder-Mackler N (2020). “Insights from evolutionarily relevant models of human ageing. ” Philosophical Transactions of the Royal Society B, 367:11. doi: 10.1098/rstb.2019.0605

Snyder-Mackler N, Burger JR, Gaydosh L, Belsky D, Noppert GA, Campos FA, Bartolomucci A, Yang YC, Aiello AE, O’Rand A, Mullan Harris K, Shively CA, Albert SC, Tung J (2020). “Social determinants of health and survival in humans and other animals.” Science, doi: 10.1126/science.aax9553

Gnanadesikan GE, Hare B, Snyder-Mackler N, MacLean EL (2020). “Estimating the heritability of cognitive traits across dog breeds reveals highly heritable inhibitory control and communication factors.” Animal Cognition, doi: 10.1007/s10071-020-01400-4

Gnanadesikan GE, Hare B, Snyder-Mackler N, Call J, Kaminski J, Miklosi A, MacLean EL (2020). “Breed differences in dog cognition associated with brain-expressed genes and neurological functions.” Integrative & Comparative Biology, doi: 10.1093/icb/icaa112

Schneider-Crease I, Beehner JC,  Bergman T, Gomery M, Koklic L, Lu A, Snyder-Mackler N (2020). “Ecology eclipses phylogeny as a major driver of nematode parasite community structure in an herbivorous primate.” Functional Ecology, doi: 10.1111/1365-2435.13603.

Amato KR, Kuthyar S, Ekanayake-Weber M, Salmi R, Snyder-Mackler N, Wijayathunga L, Vandercone R, Lu A (2020). “Gut Microbiome, Diet, and Conservation of Endangered Langurs in Sri Lanka.” Biotropica, doi: 10.1111/btp.12805.

Watowich MM, MacLean EL, Hare B, Call J, Kaminski J, Miklosi A, Snyder-Mackler N (2020). “Age influences domestic dog cognitive performance independent of average breed lifespan.” Animal Cognition, doi: 10.1007/s10071-020-01385-0

Ellis S, Snyder-Mackler N, Ruiz-Lambides A, Platt ML, Brent LJN (2019). “Deconstructing sociality: the types of social connections that predict longevity in a group-living primate.” Proceedings of the Royal Society B: Biological Sciences, doi: 10.1098/rspb.2019.1991

Fisher J, Higham JP, Alberts SC, Barrett L, Beehner JC, Bergman TJ, Carter AJ, Collins A, Elton S, Fagot J, Ferreira da Silva MJ, Hammerschmidt K, Henzi P, Jolly CJ, Knauf S, Kopp GH, Dogers J, Roos C, Ross C, Seyfarth RM, Silk J, Snyder-Mackler N, Staedele V, Swedell L, Wilson ML, Zinner D (2019). “Insights into the evolution of social systems and species from baboon studies.” eLife, 8:e50989. doi: 10.7554/eLife.50989

Schneider-Crease I, Chiou KL, Snyder-Mackler N, Bergman TJ, Beehner JC, Lu A (2019). “Beyond infant death: the hidden costs of male immigration in geladas.” Animal Behaviour, doi:10.1016/j.anbehav.2019.11.010

Sanz J, Maurizio PL, Snyder-Mackler N, Simons ND, Voyles TP, Kohn JN, Michopoulos V, Wilson ME, Tung J*, Barreiro LB* (2019). “Social history and exposure to pathogen signals modulate social status effects on gene regulation in rhesus macaques.” Proceedings of the National Academy of Sciences, doi:10.1073/pnas.1820846116.

MacLean E*, Snyder-Mackler N*,  vonHoldt B, Serpell J (2019). “Highly heritable and functionally relevant breed differences in dog behavior.” Proceedings of the Royal Society B: Biological Sciences, doi: 10.1098/rspb.2019.0716 (

Lu A, Petrullo L, Carerra S, Feder J, Schneider-Crease I, Snyder-Mackler N (2019). “Developmental Responses to Early-Life Adversity: Evolutionary and Mechanistic Perspectives.” Evolutionary Anthropology. Evolutionary Anthropology, doi:10.1002/evan.21791

Petrullo L, Jorgensen MJ, Snyder-Mackler N, Lu A (2019). “Composition and stability of the vervet monkey milk microbiome.” American Journal of Primatology. e22982; doi: 10.1002/ajp.22982

Debray R*, Snyder-Mackler N*, Kohn JN, Wilson ME, Barreiro LB, Tung J (2019). “Social integration predicts mitochondrial DNA copy number in rhesus macaques.” 

Snyder-Mackler N​, Sanz J, Kohn JN, Voyles TN, Pique-Regi R, Wilson ME, Barreiro LB, Tung J (2018) “Social status alters chromatin accessibility and the gene regulatory response to glucocorticoid stimulation in rhesus macaques.” Proceedings of the National Academy of Sciences.  doi:10.1073/pnas.1811758115

Snyder-Mackler N*  & Lea AJ* (2018). “Functional genomic insights into the environmental determinants of mammalian fitness.” Current Opinion in Genetics & Development. doi:10.1016/j.gde.2018.08.001

Ramos-Fernandez GKing AJ, Beehner JCBergman TJCrofoot MC, Di Fiore A, Lehmann JSchaffner CM, Snyder-Mackler N, Zuberbühler K, Aureli F, Boye D (2018). “Quantifying uncertainty due to fission–fusion dynamics as a component of social complexity.” Proceedings of the Royal Society B: Biological Sciences.  285; doi: 10.1098/rspb.2018.0532

Madlon-Kay S, Montague MJ, Brent LJN, Ellis S, Zhong B, Snyder-Mackler N, Horvath JE, Skene JHP, Platt ML (2018). “Weak effects of common genetic variation in oxytocin and vasopressin receptor genes on rhesus macaque social behavior.” American Journal of Primatology. doi:10.1002/ajp.22873

Tinsley Johnson E, Snyder-Mackler N, Lu A, Bergman TJ, Beehner JC (2018). “Social and ecological drivers of reproductive seasonality in geladas.” Behavioral Ecology. 29:3, 574–588. doi: 10.1093/beheco/ary008

Belsky D and Snyder-Mackler N (2017). “Invited Commentary: Integrating Genomics and Social Epidemiology—Analysis of Late-Life Low Socioeconomic Status and the Conserved Transcriptional Response to Adversity” American Journal of Epidemiology, doi: 10.1093/aje/kwx145

Snyder-Mackler N and Tung J (2017). “Vasopressin and the neurogenetics of parental care”(“Spotlight” article on Bendesky et al. 2017, NatureNeuron, 94:1, 9–11, doi: 10.1016/j.neuron.2017.06.027 (* not peer-reviewed)

Schneider-Crease I, Griffin RH, Gomery MA, Dorny P, Noh JC, Handali S, Chastain HM, Wilkins PP, Nunn CL, Snyder-Mackler N, Beehner JC, Bergman TJ (2017). “Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population” PLoS Neglected Tropical Diseases, doi: 10.1371/journal.pntd.0005709.

Snyder-Mackler N, Pappano DJ (2016). Gelada (Theropithecus). In The International Encyclopedia of Primatology.  John Wiley & Sons, doi:10.1002/9781119179313.wbprim0252

Snyder-Mackler N​*, Sanz J*, Kohn JN, Brinkworth JF, Morrow S, Shaver AO, Grenier J-C, Pique-Regi R, Johnson ZP, Wilson ME, Barreiro LB, Tung J (2016) “Social status alters immune regulation and response to infection in macaques” Science, 354:6315, 1041-1045, doi: 10.1126/science.aah3580.

Kohn JN, Snyder-Mackler N, Barreiro LB, Johnson ZP, Tung J, Wilson ME (2016) “Dominance rank causally affects personality and glucocorticoid regulation in female rhesus macaques” Psychoneuroendocrinology, 74, 179-188, doi: 10.1016/j.psyneuen.2016.09.005.

Wall JD, Schlebusch SA, Alberts SC, Cox L, Snyder-Mackler N, Nevonen K, Carbone L, Tung J (2016) “Genome-wide ancestry and divergence patterns from low-coverage sequencing data reveal a complex history of admixture in wild baboons” Molecular Ecology, 25:14, 3469-3483, doi: 10.1111/mec.13684.

Snyder-Mackler N, Majoros B, Yuan ML, Shaver AO, Gordon JB, Kopp GH, Schlebusch SA, Wall JD, Alberts SC, Mukherjee S, Zhou S, Tung J (2016) “Efficient genome-wide sequencing and low coverage pedigree analysis from non-invasively collected samples.” Genetics, 203:2, 699-714, doi: 10.1534/genetics.116.187492.

Charruau P, Johnston R, Stahler DR, Lea AJ, Snyder-Mackler N, Smith DW, vonHoldt BM, Cole SW, Tung J, Wayne RK (2016) “Pervasive effects of aging on gene expression in wild wolves” Molecular Biology and Evolution, 33:8, 1967-1978, doi: 10.1093/molbev/msw072.

Snyder-Mackler N, Kohn JN, Barreiro LB, Johnson ZP, Wilson ME, & Tung J (2016) – “Social status drives social relationships in groups of unrelated female rhesus macaques.” Animal Behaviour, 111, 307-317, doi: 10.1016/j.anbehav.2015.10.033.

Snyder-Mackler N, Alberts SC, & Bergman TJ (2014) – “The socio-genetics of a complex society: Female gelada monkey relatedness patterns mirror association patterns in a multi-level society” Molecular Ecology, 23:24, 6179-6191, doi: 10.1111/mec.12987.

Snyder-Mackler N, Somel M, & Tung J (2014) – “Shared signatures of social stress and aging in PBMC gene expression profiles.” Aging Cell,13:5, 954-957, doi: 10.1111/acel.12239.

Tinsley Johnson E*, Snyder-Mackler N*, Beehner JC & Bergman TJ (2014) – “Kinship and dominance rank influence the strength of social bonds in female geladas” International Journal of Primatology, 35:1, 288-304, doi:10.1007/s10764-013-9733-5.

Scheider-Crease I*, Snyder-Mackler N*, Jarvey JC & Bergman TJ (2013) – “Molecular identification of Taenia serialis coenurosis in a wild Ethiopian gelada (Theropithecus gelada)” Veterinary Parasitology, 198:1-2, 240-243, doi: 10.1016/j.vetpar.2013.08.015.

Le Roux, A, Snyder-Mackler N, Roberts EK, Beehner JC & Bergman TJ (2013) – “Evidence for tactical concealment in a wild primate” Nature Communications, 4:1462, doi: 10.1038/ncomms2468.

Snyder-Mackler N, Alberts SC & Bergman TJ (2012) – “Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups.” Proceedings of the Royal Society B: Biological Sciences, 279:1743, 3788-3795. doi: 10.1098/rspb.2012.0842.

Pappano DJ*, Snyder-Mackler N*, Bergman TJ & Beehner JC (2012) – “Social predators in a multi-level society” Animal Behaviour, 84:3, 653-658. doi: 10.1016/j.anbehav.2012.06.021.

Snyder-Mackler N, Beehner JC, Bergman TJ (2012) – “Defining higher levels in the multilevel societies of geladas (Theropithecus gelada)” International Journal of Primatology – 33:5, 1054:1068. doi: 10.1007/s10764-012-9584-5.

Gersick AS, Snyder-Mackler N, White DJ (2012) – “Ontogeny of social skills: social complexity improves mating and competitive strategies in male brown-headed cowbirds” Animal Behaviour, 83:5, 1171–1177. doi: 10.1016/j.anbehav.2012.02.005.

White DJ, Gersick AS & Snyder-Mackler N (2012) – “Social networks and the development of social skills in cowbirds.” Philosophical Transactions of the Royal Society of London B: Biological Sciences, 367:1597, 1892-1900. doi: 10.1098/rstb.2011.0223.

Snyder-Mackler N & White DJ (2011). “The developmental ecology of acoustic sensitivities: reactions to song playbacks by male cowbirds change across their first year of life.” Behaviour, 148:7, 747-764. doi: 10.1163/000579511X575951.

White DJ, Gersick AS, Freed-Brown SG & Snyder-Mackler N (2010). “The ontogeny of social skills: experimental increases in social complexity enhance reproductive success in adult cowbirds.” Animal Behavior, 79:2, 385-390. doi: 10.1016/j.anbehav.2009.11.014.

* denotes co-first authorship.