Collaborative Research: Male-male competition and speciation: behavioral and neuromolecular mechanisms underlying aggression biases in cichlids

Competition is fact of life: all organisms are constantly engaged in competition for mates and other resources, and they often do so aggressively. These competitive interactions can have important consequences not just for the individuals that engage in them but also for the evolution and persistence of populations and species. For example, scientists have shown that new species can evolve when territory holders direct more aggression towards competitors that resemble themselves compared to those that are dissimilar. However, we know very little about the physiological and neurobiological processes that control this kind of aggression that is biased toward individuals that look more similar to oneself. The proposed research will use a combination of social learning experiments, genetic analysis, neural activity mapping, and brain gene expression analyses to investigate this question using two highly social cichlid fish species that differ in body coloration. This highly integrative approach will advance our understanding of how social competition influences evolutionary change and biodiversity. The multidisciplinary project will build collaborative relationships among institutions in the US (two R2 and one R1), Switzerland, and Tanzania. It will also provide research and training opportunities for undergraduate and graduate students. This project will promote STEM engagement through the development of an interactive exhibit on cichlid social behavior at a local children’s discovery museum. Together, these efforts will answer fundamental questions in organismal biology while having a significant societal impact by preparing students to enter STEM fields. Male-male competition for mates and breeding territories is thought to play an important role in population differentiation and speciation. If males bias territorial aggression towards males that resemble their own phenotype, rare male phenotypes would be involved in fewer costly fights. The resulting negative frequency-dependent selection could facilitate the evolution of distinct phenotypes and stabilize the speciation process. However, the underlying proximate mechanisms remain mostly unknown. The proposed research will assess the cognitive, genetic, and neural basis of aggression biases in the cichlid species pair Pundamilia nyererei (males are red) and P. pundamilia (males are blue). These two species co-occur at different locations in the East African Lake Victoria with varying degrees of reproductive isolation, allowing us to study the mechanistic basis of aggression biases at different stages of speciation. The project has the following objectives: First, this research will estimate the number of genetic loci regulating aggression biases and body coloration and their degree of linkage using quantitative genetics and quantitative trait locus mapping. Second, this research will assess how social experience and social context shape aggression biases. Finally, the project will determine the neural mechanisms regulating aggression biases using a combination of neural activity mapping, pharmacological manipulation of dopamine signaling, and neural transcriptome analysis. This highly integrative approach will provide insights into how male-male competition contributes to speciation, agonistic character evolution, and species coexistence. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.