Male ornamental traits of the guppy, Poecilia reticulata, provide an outstanding example of natural variation in sex-linked male-advantageous traits that are shaped by both sexual and environmental selection. A substantial fraction of the underlying genes is known to be genetically linked to the sex-determining region on the differentiating Y-chromosome. Intercrosses between parental populations originating from geographically distant locations in East Trinidad and Cumaná (Venezuela) were used to study segregation of ornamental traits in male progeny. In addition, we performed backcrosses to compare segregation of ornaments in presence or absence of prominent traits linked to the Y-chromosome. Another backcross strategy involving XY females from the laboratory strain zebrinus maculatus allowed studying additive and dominant effects of alleles on two different Y-chromosomes on pattern formation. For genetic mapping, we have previously developed nuclear SNP markers linked to expressed genes, including several genes known to be important for pattern formation in other species. Of these candidate genes 15 were placed on 11 different linkage groups. Our phenotypic and genotypic analysis of progeny from mapping crosses and backcrosses suggests several genetic mechanisms that enhance natural variation, namely, additive effects of codominant alleles, suppressive actions of dominant alleles, and a complex interplay between sex-linked and autosomal cofactors.