Multiple Loci Control Eyespot Number Variation on the Hindwings of Bicyclus anynana Butterflies

• Published in: Genetics (Austin) 2020-04, Vol.214 (4), p.1059-1078
• Main Authors: Rivera-Colón, Angel G, Westerman, Erica L, Van Belleghem, Steven M, Monteiro, Antónia, Papa, Riccardo
• Format: Article
• Language: English
• Subjects: Abdomen; Animal behavior; Animals; Bicyclus anynana; Breeding; Butterflies & moths; Butterflies - genetics; Deoxyribonucleic acid; DNA; DNA sequencing; Evolution; Evolutionary genetics; Eyespot; Gene loci; Genes; Genes, Insect; Genetic diversity; Genetic Variation; Genetics; Genome-wide association studies; Genomes; Heritability; Homology; Hypotheses; Investigations; Laboratories; Multifactorial Inheritance; Mutation; Offspring; Pigmentation; Polygenic inheritance; Regulation; Wings, Animal - metabolism
• ISSN: 1943-2631; 0016-6731; 1943-2631
• DOI: 10.1534/genetics.120.303059

Abstract Body plans often evolve through changes in the number of repeated parts or serial homologs. Using the butterfly Bicyclus anynana, RiveraColón et al. studied the genetics underlying heritability... The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypothesis is that variation in genomic regions flanking master regulatory genes, also known as input–output genes, controls variation in trait number, making the locus of evolution almost predictable. Another hypothesis implicates genetic variation in up- or downstream loci of master control genes. Here, we use the butterfly Bicyclus anynana, a species that exhibits natural variation in eyespot number on the dorsal hindwing, to test these two hypotheses. We first estimated the heritability of dorsal hindwing eyespot number by breeding multiple butterfly families differing in eyespot number and regressing eyespot numbers of offspring on midparent values. We then estimated the number and identity of independent genetic loci contributing to eyespot number variation by performing a genome-wide association study with restriction site-associated DNA sequencing from multiple individuals varying in number of eyespots sampled across a freely breeding laboratory population. We found that dorsal hindwing eyespot number has a moderately high heritability of ∼0.50 and is characterized by a polygenic architecture. Previously identified genomic regions involved in eyespot development, and novel ones, display high association with dorsal hindwing eyespot number, suggesting that homolog number variation is likely determined by regulatory changes at multiple loci that build the trait, and not by variation at single master regulators or input–output genes.