Our research unites the molecular aspects of biology with the ecological to understand behavior evolution:
identify genes that have evolved across different timescales
dissect location and timing of gene expression and how that differently sculpts the neural circuits that generate divergent behaviors
test how behavior evolution structures eco-evolutionary dynamics in nature
study system
Drosophila are poised at an intersection among rich ecology with a wealth of genetic and neural tools that make possible the study of behavior at multiple levels of biological organization—from genes to neurons to behaviors to community assemblages—across different evolutionary timescales—within a species over time to among populations across space to across different species.
The lab focuses on courtship behavior as a model to study behavior evolution. Courtship behaviors that arbitrate mating are ecologically important because they determine reproductive success and have direct effects on fitness. Drosophila courtship rituals are composed of a series of discrete behaviors that have rapidly diversified within and among species to signify identity and discourage interspecies mating. Drosophila courtship behaviors are a model for studying the neural circuits underlying behavior. Comparing the same circuit between different species reveals the successful ways that circuits can be modified. This combination makes Drosophila an incredibly powerful system to dissect the genomic mechanisms producing behavior in the lab and apply that in naturalistic settings to understand how behavior shapes evolution in real time in natural populations.
The male mate choice initial reproductive barrier occurs when a male tastes female pheromone to decide if she is an appropriate mate and, if so, he vibrates his wings to sing a species-specific song that presumably evolved by female mate choice sexual selection.
Research Directions
Genetic & neural mechanisms
how does the same stimulus produce different behavior?
Our lab deconstructs behavior evolution using a combination of gene editing and omics approaches to identify what genes—the ultimate source of new behavior—have evolved across different timescales. Identification of specific genes guides us to the specific cells where and when neural circuits can be modified successfully. We combine microscopy and molecular techniques to identify how the genes modify anatomical and physiological properties of homologous neurons to generate divergent behavior.
Evolutionary ecology
how does behavior change the rate of evolution?
Behavior both evolves and acts as a pacemaker of evolution. We use courtship to study the feedback between behavior and evolution using field collections at increasing levels of environmental complexity in laboratory experiments complemented with experimental evolution in naturalistic mesocosms.
Previous Research
Tempo and mode of evolution in wild Drosophila
Emily’s PhD dissertation helped establish seasonal evolution in D. melanogaster as a powerful system to study ecological interactions and contemporary evolutionary dynamics in natural populations. Combining field collections across geographic space and seasonal time with common garden laboratory experiments and whole genome resequencing revealed that wild D. melanogaster are dynamic with many traits and genes evolving across short timescales. I disentangled the relationships among genotype, phenotype, and the environment by identifying specific environmental factors associated with seasonal evolution and dissecting the complex genetic architecture of the genetic variants that oscillate with seasonal time. The rapid evolution research program has ignited interest in this system to study different aspects of the dynamics of seasonal adaptation.
A major gap that left unexplored is how behavior evolution factors into evolutionary dynamics on this time scale; the feedback loop of how genetic evolution shapes neural evolution to shape behavior and, in turn, how behavior evolution affects evolutionary dynamics in the wild.
Major publications:
Bergland, AO, EL Behrman, KR O’Brien, PS Schmidt and DA Petrov. 2014. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genetics 10(11), 19p. DOI:10.1371/journal.pgen.1004775
Paaby, AB, AO Bergland, EL Behrman and PS Schmidt. 2014. An amino acid polymorphism in the Drosophila insulin receptor demonstrates pleiotropic and adaptive function in life history traits. Evolution. 68(12)3395-3409. DOI:10.1111/evo.12546
Behrman, EL, S Watson, KR O’Brien, MS Heshel and PS Schmidt. 2015. Seasonal life history adaptation in two species of Drosophila. Journal of Evolutionary Biology, 28 (9) 1691-1704. DOI:10.1111/jeb.12690
Machado, H, AO Bergland, KR O’Brien, EL Behrman, P Schmidt and D Petrov. 2016. Comparative population genomics of latitudinal variation in Drosophila simulans and Drosophila melanogaster. Molecular Ecology, 5(3):723-40. DOI:10.1111/mec.13446
Rajpurohit, S, R Hanus, V Vrkoslav, EL Behrman, J Cvacka and PS Schmidt. Adaptive dynamics of cuticular hydrocarbons in Drosophila. 2017. Journal of Evolutionary Biology, 30(1):66-80. DOI:10.1111/jeb.12988
Behrman, EL, VM Howick, F Staubach, AO Bergland, DA Petrov, BP Lazzaro, and PS Schmidt. 2018. Genetic basis of seasonal change in innate immune response in Drosophila melanogaster. Proceedings of the Royal Society B, 285: 20172599 DOI:10.1098/rspb.2017.2599
Behrman, EL, T Kawecki, and PS Schmidt. Natural variation in couch potato mediates rapid evolution of learning and reproduction in natural populations of Drosophila melanogaster. 2020. BioRxiv DOI:10.1101/288696
HE Machado et al. [including EL Behrman]. 2021. Broad geographic sampling reveals predictable and pervasive seasonal adaptation in Drosophila. eLife 2021;10:e67577 DOI:10.7554/eLife.67577
M Kapun, et al. [including EL Behrman]. Drosophila Evolution over Space and Time (DEST) – A New Population Genomics Resource. 2021. Molecular Biology and Evolution 38 (12), 5782-5805. DOI:10.1093/molbev/msab259
Behrman, EL, and P Schmidt How predictable is Rapid Evolution? 2023. BioRxiv DOI:10.1101/2022.10.27.514123
Genetic and neural mechanisms of behavior evolution between Drosophila species
Connectomes that map all neural connections combined with the ability to label homologous neurons in different species provide access to complex neural circuits underlying behavior evolution, but little is known about how genes pattern those circuits to produce different behavior. As a Postdoctoral Associate, Emily built genetic and neural tools in different Drosophila species as well as high-throughput behavior assays and analysis pipelines required to identify subtle behavior differences. I implemented those tools to identify a gene that has evolved between the close relatives D. melanogaster and D. simulans that changes male attraction to a species-specific female pheromone. I then dissected how this gene changes the anatomical and physiological properties of courtship neural circuit. This unique mechanistic understanding of behavior evolution explores missing links from gene to neural circuit to behavior. This system provides future opportunities to study convergent evolution across different timescales and to test how genetic evolution shapes evolutionary dynamics.
Major publications:
Stern, DL, Kim, E, and Behrman, EL, The Janelia Atalanta plasmids provide a simple and efficient CRISPR/Cas9-mediated homology directed repair platform for Drosophila. 2023. BioRxiv DOI:10.1101/2023.06.17.545412 [High efficiency CRISPR-HDR plasmid]
Sawtelle, S., L Narayan, Y Ding, E Kim, EL Behrman, J Lillvis, and DL Stern. Song Torrent: A modular, open-source 96-chamber audio and video recording apparatus with optogenetic activation and inactivation capabilities for Drosophila. DOI:10.1101/2024.01.09.574712v1.full [High throughput 96 chamber audio & video rig]