Our research integrates evolutionary, genetic, and behavioral approaches to address the genetics and evolution of complex traits. We specifically study social behavior and social interactions, including communication, mating, parental care, aggression, and development of behavior.
Theoretical and empirical investigations of social behavior evolution – “interacting phenotypes”. I have been developing theory to describe how social behavior evolves. My initial interest was in maternal effects, or how genetically influenced phenotypes of parents influenced offspring characters. Standard quantitative genetic models partition influences into genetic and environmental, but maternal effects reflect an “inherited environment” effect and this leads to unusual evolutionary dynamics. My collaborators (E. D. Brodie III, University of Virginia; J. B. Wolf, Bath University; J. W. McGlothlin, Virginia Tech University; N. W. Bailey, St. Andrews University) and I realized that that quantitative genetic, maternal effect models could be generalized to any trait influenced by social interactions regardless of the level of relatedness among interacting individuals. The result is that both direct genetic effects and indirect genetic effects (IGE) can contribute to phenotypic expression and evolution. This has allowed us to explore how evolution is shaped by traits where the focal and the interacting phenotype both evolve. Along with our foundational research into evolutionary dynamics, studies incorporating IGE have now been conducted in agriculture, breeding, and in human medicine.
Moore, A.J., E.D. Brodie III & J.B. Wolf. 1997. Interacting phenotypes and the evolutionary process: I. direct and indirect genetic effects of social interactions. Evolution 51:1352-1362.
Wolf, J. B., E. D. Brodie III & A. J. Moore 1999. Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. American Naturalist 153:254-266.
Moore,A. J. & T. Pizzari 2005. Quantitative genetic models of sexual conflict based on interacting phenotypes. American Naturalist 165: S88-S97
Miller, C. W. & A. J. Moore 2007. A potential resolution to the lek paradox through indirect genetic effects. Proceedings of the Royal Society of London B 274: 1279-1286
McGlothlin, J. W., A. J. Moore, J. B. Wolf & E. D. Brodie III 2010. Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 64: 2558-2574.
Bailey, N. W. & A. J. Moore. 2012. Runaway sexual selection without genetic correlations: social environments and flexible mate choice initiate and enhance the Fisher process. Evolution 66: 2674-2684.
Head, M. L., L. K. Berry, N. J. Royle & A. J. Moore. 2012. Paternal care: direct and indirect genetic effects of fathers on offspring performance. Evolution 66: 3570-3581.
Bleakley, B. H., S. M. Welter, K. McCauley-Cole, S. M. Shuster & A. J. Moore. 2013. Cannibalism as an interacting phenotype: pre-cannibalistic aggression is influenced by social partners in the endangered Socorro isopod (Thermosphaeroma theromophilum). Journal of Evolutionary Biology, 26: 832-842.
McGlothlin, J. W, J. B. Wolf, E. D. Brodie III, A. J. Moore. 2014. Quantitative genetic versions of Hamilton’s rule with empirical applications. Philosophical Transactions of the Royal Society B 369: 20130358 (doi:10.1098/rstb.2013.0358)
Bacigalupe, L. D., A. J. Moore, R. F. Nespolo, E. L. Rezende & F. Bozinovic. 2017. Quantitative genetic modelling of the parental care hypothesis for the evolution of endothermy. Frontiers in Physiology 8: 1006. doi: 10.3389/fphys.2017.
Bailey, N. W., L. Marie-Orleach & A. J. Moore. 2018. Indirect genetic effects in behavioural ecology: Does behaviour play a special role in evolution? Behavioral Ecology 29: 1-11. doi:10.1093/beheco/arx127.
Bailey, N. W. & A. J. Moore. 2018. Evolutionary consequences of social isolation. Trends in Ecology & Evolution 33: 595-607.
Carter, M. J., A. J. Wilson, A. J. Moore & N. J. Royle. 2019. The role of indirect genetic effects in the evolution of interacting reproductive behaviors in the burying beetle, Nicrophorus vespilloides. Ecology and Evolution 9: 998-1009 (DOI:10.1002/ece3.4731).
McGlothlin, J.W., E. Akçay, E.D. Brodie III, A.J. Moore, & J. van Cleve. 2022. A synthesis of game theory and quantitative genetic models of social evolution. Journal of Heredity 113: 109-119.
Moore, A.J., J.W. McGlothlin & J.B. Wolf. 2021. Runaway evolution from male-male competition. Ecology Letters 25: 295-306.
De Lisle, S.P., D.I. Bolnick, E.D. Brodie III, A.J. Moore, & J.W. McGlothlin. 2022. Interacting phenotypes and the coevolutionary process: Interspecific indirect genetic effects alter coevolutionary dynamics. Evolution 76: 429-444.
The genetics and evolution of parental care. We have been studying burying beetle in the genus Nicrophorus, in which parents actively regurgitate food to begging offspring. This species has very extensive and elaborate parental care, but a larval generation time of 7-9 days (within which parental care occurs over 6 days) permitting detailed genetic studies of the parental behavior itself. Our original approach was to investigate the quantitative genetics underlying care, but more recently has shifted to define the genes that underly parental care. We have begun to identify a core set of “parenting genes” and pathways that are common across species.
Parker, D. J., C. B. Cunningham, C. A. Walling, C. E. Stamper, M. L. Head, E. M. Roy-Zokan, E. C., McKinney, M. G. Ritchie, A. J.Moore. 2015. Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle. Nature Communications 6:8449 doi: 10.1038/ncomms9449.
Benowitz, K. M., K. J. Moody & A. J. Moore. 2015. Are species differences in maternal effects arising from maternal care adaptive? Journal of Evolutionary Biology 28: 503-509.
Roy-Zokan, E. M., C. B. Cunningham, L. E. Hebb, E. C. McKinney & A. J. Moore. 2015. Vitellogenin and vitellogenin receptor gene expression is associated with male and female parenting in a subsocial insect. Proceedings of the Royal Society B, 20150787.
Royle, N. J., S. H. Alonzo & A. J. Moore. 2016. Co-evolution, conflict and complexity: what have we learned about the evolution of parental care behaviours? Current Opinion in Behavioral Sciences 12: 30-36.
Benowitz, K. M., E. C. McKinney, C. B. Cunningham & A. J. Moore. 2017. Relating quantitative variation within a behavior to variation in transcription. Evolution 71: 1999-2009.
Mehlferber, E. C., K. M. Benowitz, E. M. Roy-Zokan, E. C. McKinney, C. B. Cunningham & A. J. Moore. 2017. Duplication and sub/neofunctionalization of Malvolio, an insect equivalent of Nramp, in the subsocial beetle Nicrophorus vespilloides. G3 7:3393-3403.
Royle, N. J. & A. J. Moore 2019. Nature and nurture in parental care. Pp. 131-156 in: Hosken, D. J., J. Hunt & N. Weddell, (eds) Genes and Behaviour: Beyond Nature-Nurture. Wiley Press, Oxford.
Ziadie, M. A., F. Ebot-Ojong, E. C. McKinney & A. J. Moore. 2019. Evolution of personal and social immunity in the context of parental care. American Naturalist 193: 296-308.
Moss, J.B. and A.J. Moore. 2021. Constrained flexibility of parental cooperation limits adaptation to harsh conditions. Evolution 75: 1835-1849. https://doi.org/10.1111/evo.14285.
Cunningham, C.B., D. Khana, A. Carter, E. C. McKinney & A. J. Moore. 2021. Survey of neurotransmitter receptor gene expression into and out of parental care in the burying beetle, Nicrophorus vespilloides. Ecology and Evolution 11:14282-14292.
Moss, J.B., C.B. Cunningham, E.C. McKinney, & A.J. Moore. 2022. Gene expression underlying parenting and being parented shows limited plasticity in response to different ambient temperatures. Molecular Ecology 31: 5326-5338.
The role of CpG methylation in insects. In 2015 we published a sequenced and annotated genome of the second beetle species after the genetic model species Tribolium. In the course of this work we found that the genome was methylated, and functional dmnt1 and dmnt3 genes (neither Drosophila nor Tribolium have CpG methylation). Since then we have been investigating the function of methylation in insects, the diversity of dmnt genes, and pleiotropic functions for dmnt1 in insects. We have found that functional methylation does not necessarily correspond to gene regulation, and that dmnt1 may be required for generation of gametes without involving methylation. Our work has opened up new areas of research in both methylation and insects. We are collaborating with P. J. Moore (UGA Entomology) and Bob Schmitz (UGA Genetics) to expand our understanding of methylation beyond the beetle we study.
Cunningham, C. B., L. Ji, R. A. W. Wiberg, J. M. Shelton, E. C. McKinney, D. J. Parker, R. B. Meagher, K. M. Benowitz, E. M. Roy-Zokan, M. G. Ritchie, S. J. Brown, R. J. Schmitz, A. J. Moore. 2015. The genome and methylome of a beetle with complex social behavior, Nicrophorus vespilloides (Coleoptera: Silphidae). Genome Biology and Evolution 7:3383-3396.
Bewick, A. J., K. J. Vogel, A. J. Moore & R. J. Schmitz. 2017. Evolution of DNA methylation across insects. Molecular Biology & Evolution 34: 654-665: doi: 10.1093/molbev/msw264.
Cunningham, C. B., L. Ji, E. C. McKinney, K. M. Benowitz, R. J. Schmitz & A. J. Moore. 2019. Changes of gene expression but not cytosine methylation are associated with male parental care reflecting behavioural state, social context, and individual flexibility. Journal of Experimental Biology 222, jeb188649.
Bewick, A.J., Z. Sanchez, E. C. McKinney, A. J. Moore, R. J. Schmitz & P. J. Moore. 2019. Dnmt1 is essential for egg production and embryo viability in the large milkweed bug, Oncopeltus fasciatus. Epigenetics & Chromatin 12:6 doi:10.1186/s13072-018-0246-5.
Amukamara, A.U., J.T. Washington, Z. Sanchez, E.C. McKinney, A.J. Moore, R. J. Schmitz & P. J. Moore. 2020. More than DNA methylation: does pleiotropy drive the complex pattern of evolution of Dnmt1? Frontiers in Ecology and Evolution 8:4 doi:10.3389/fevo.2020.00004.
Shelby, E.A., E.C. McKinney, C.B. Cunningham, A.M. Simmons, A.J. Moore, & P.J. Moore. 2023. The role of Dmnt1 in oocyte development. Journal of Insect Physiology, in press.
Cunningham, C.B., E.A. Shelby, E.C. McKinney, R.J. Schmitz, A.J. Moore, & P.J. Moore. 2023. The role of Dmnt1 during spermatogenesis of insects. Epigenetics & Chromatin 16:28. https://doi.org/10.1186/s13072-023-00496-5.
Predicting genes and genetic pathways underlying parenting behavior. We have developed a framework for predicting the genes that will evolve, be co-opted, to influence parental care. Using ethological principles, we predicted that there would be behavioral precursors. Thus, a trait such as provisioning offspring involves switching from feeding self to feeding others, and thus evolution will co-opt genes that influence feeding behavior. Likewise, switching to social tolerance, necessary for parents to remain near their offspring, will involve genes in pathways influencing aggressive behavior. Our work has shown that while specific genes are not always predictable, the genetic pathways in which influential genes lie will reflect predictable behavioral precursors. This research opens the door to targeted functional studies that have not before been possible. While other research has suggested that a genetic toolkit will involve predictable candidate genes, our work and others suggest that genetic pathways are more predictable, and we show that the prediction is enhanced by considering likely evolutionary trajectories.
Cunningham, C. B., K. VanDenHeuvel, D. B. Khana, E. C. McKinney & A. J. Moore. 2016. The role of neuropeptide F in a transition to parental care. Biology Letters 12: 20160158.
Cunningham, C. B., M. J. Badgett, R. B. Meagher, R. Orlando & A. J. Moore. 2017. Ethological principles predict the neuropeptides co-opted to influence parenting. Nature Communications 8:14225 | DOI: 10.1038/ncomms14225.
Benowitz, K. M., E. C. McKinney, C. B. Cunningham & A. J. Moore. 2019. Predictable gene expression related to behavioural variation in the burying beetle Nicrophorus vespilloides. Behavioral Ecology 30: 402-407
Moore, A. J. & K. M. Benowitz. 2019. From phenotype to genotype: the precursor hypothesis predicts genetic influences that facilitate transitions to social behaviour. Current Opinion in Insect Science 34: 91-96.
Cunningham, C.B., D. Khana, A. Carter, E. C. McKinney & A. J. Moore. 2021. Survey of neurotransmitter receptor gene expression into and out of parental care in the burying beetle, Nicrophorus vespilloides. Ecology and Evolution 11:14282-14292.
Potticary, A.L., E.C. McKinney, P.J. Moore, & A.J. Moore. 2023. takeout gene expression is associated with temporal kin recognition. Royal Society Open Science, in press.
Potticary, A.L., C.B. Cunningham, E.C. McKinney, P.J. Moore, A.T. Belay, & A.J. Moore. 2023. Insect homolog of oxytocin/vasopressin is associated with parenting of males but not females in a subsocial beetle. Evolution, in press.
