Signatures of repeated genomic selection associated with human-modified landscapes in genetically independent populations of Rhinella horribilis

Abstract Human-modified environments constitute evolutionary scenarios where novel environmental conditions impose multiple selective pressures on wild species. Rapid adaptation to such environments is critical for species survival. Hence, deciphering the environmental factors associated with species tolerance to modified habitats is fundamental for understanding local adaptation processes across populations. We studied the Giant Toad Rhinella horribilis from two landscapes characterized by land-use changes resulting from combined traditional and intensive agriculture and livestock practices. We identified potential outlier loci, assessed genotype-environment associations, annotated candidate genes, and tested for signals of repeated genomic selection in the two landscapes. We used an integrative analytical approach and assessed patterns of genetic repeatability at the genome scale, which improve confidence in identifying true selection signals and provide insights into genetic responses contributing to adaptive evolution. We found positive genotype-environment associations (GEA) related to suboptimal climatic and water physiochemical conditions. Candidate genes were negatively and positively linked with different environmental variables (temperature, solar radiation, oxygen availability, potassium levels in water bodies). Our findings provide evidence of repeated genomic evolution at the functional level, with successful annotation of 34 shared (statistically overlapped) genes between landscapes. Seven genes were enriched for biological processes and metabolic pathways, associated mainly with embryonic development, sexual maturation, and immune responses. These repeated genomic GEA patterns likely reflect rapid local adaptive responses to stressful conditions imposed by these human-modified environments.