Gene Expression Modularity Reveals Footprints of Polygenic Adaptation in Theobroma cacao

Separating footprints of adaptation from demography is challenging. When selection has acted on a single locus with major effect, this issue can be alleviated through signatures left by selective sweeps. However, as adaptation is often driven by small allele frequency shifts at many loci, studies focusing on single genes are able to identify only a small portion of genomic variants responsible for adaptation. In face of this challenge, we utilize coexpression information to search for signals of polygenetic adaptation in Theobroma cacao, a tropical tree species that is the source of chocolate. Using transcriptomics and a weighted correlation network analysis, we group genes with similar expression patterns into functional modules. We then ask whether modules enriched for specific biological processes exhibit cumulative effects of differential selection in the form of high F-ST and d(XY) between populations. Indeed, modules putatively involved in protein modification, flowering, and water transport show signs of polygenic adaptation even though individual genes that are members of those groups do not bear strong signatures of selection. Modeling of demography, background selection, and the effects of genomic features reveal that these patterns are unlikely to arise by chance. We also find that specific modules are enriched for signals of strong or relaxed purifying selection, with one module bearing signs of adaptive differentiation and an excess of deleterious mutations. Our results provide insight into polygenic adaptation and contribute to understanding of population structure, demographic history, and genome evolution in T. cacao.