Genetic mechanisms of axial patterning in Apeltes quadracus

Abstract

Abstract The genetic mechanisms underlying striking axial patterning changes in wild species are still largely unknown. Previous studies have shown that Apeltes quadracus fish, commonly known as fourspine sticklebacks, have evolved multiple different axial patterns in wild populations. Here, we revisit classic locations in Nova Scotia, Canada, where both high-spined and low-spined morphs are particularly common. Using genetic crosses and quantitative trait locus (QTL) mapping, we examine the genetic architecture of wild differences in several axial patterning traits, including the number and length of prominent dorsal spines, the number of underlying median support bones (pterygiophores), and the number and ratio of abdominal and caudal vertebrae along the anterior–posterior body axis. Our studies identify a highly significant QTL on chromosome 6 that controls a substantial fraction of phenotypic variation in multiple dorsal spine and pterygiophore traits (~15%–30% variance explained). An additional smaller-effect QTL on chromosome 14 contributes to the lengths of both the last dorsal spine and anal spine (~9% variance explained). 1 or no QTL were detected for differences in the numbers of abdominal and caudal vertebrae. The major-effect patterning QTL on chromosome 6 is centered on the HOXDB gene cluster, where sequence changes in a noncoding axial regulatory enhancer have previously been associated with prominent dorsal spine differences in Apeltes. The QTL that have the largest effects on dorsal spine number and length traits map to different chromosomes in Apeltes and Gasterosteus, 2 distantly related stickleback genera. However, in both genera, the major-effect QTL for prominent skeletal changes in wild populations maps to linked clusters of powerful developmental control genes. This study, therefore, bolsters the body of evidence that regulatory changes in developmental gene clusters provide a common genetic mechanism for evolving major morphological changes in natural species.