Developmental genetic basis of dorsal spine reduction in acidic-adapted threespine stickleback fish

The repeated evolution of reduced skeletal armour in threespine stickleback provides an excellent model for understanding the genetic basis of morphological change. Here, we investigated the genetic and developmental mechanisms underlying the loss of the second dorsal spine in a freshwater stickleback population from North Uist, Scotland. Crosses between spineless freshwater and fully spined marine individuals confirmed a genetic basis for the trait, with inheritance patterns inconsistent with simple Mendelian expectations. A bulk segregant analysis of F3 hybrids revealed a strong genomic signal on chromosome VI, overlapping the hoxdb cluster, echoing previous findings in another spine-reduced stickleback population. Developmental series of the Scottish freshwater and marine populations using skeletal stainings and transcriptomic analyses of dorsal tissue showed delayed and incomplete cartilage formation and altered gene expression during critical stages of dorsal skeletal development in spineless fish, notably of several hoxdb genes. Our findings indicate that while the loss of dorsal spines has evolved repeatedly, it may involve distinct alleles across populations, with the same locus possibly playing a central role in this case.