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ABSTRACT In nature, multiple adaptive phenotypes often coevolve and can be controlled by tightly linked genetic loci known as supergenes. Dissecting the genetic basis of these linked phenotypes is a major challenge in evolutionary genetics. Multiple freshwater populations of threespine stickleback fish (Gasterosteus aculeatus) have convergently evolved two constructive craniofacial traits, longer branchial bones and increased pharyngeal tooth number, likely as adaptations to dietary differences between marine and freshwater environments. Prior QTL mapping showed that both traits are partially controlled by overlapping genomic regions on chromosome 21 and that a regulatory change in Bmp6 likely underlies the tooth number QTL. Here, we mapped the branchial bone length QTL to a 155 kb, eight-gene interval tightly linked to, but excluding the coding regions of Bmp6 and containing the candidate gene Tfap2a. Further recombinant mapping revealed this bone length QTL is separable into at least two loci. During embryonic and larval development, Tfap2a was expressed in the branchial bone primordia, where allele specific expression assays revealed the freshwater allele of Tfap2a was expressed at lower levels relative to the marine allele in hybrid fish. Induced loss-of-function mutations in Tfap2a revealed an essential role in stickleback craniofacial development and show that bone length is sensitive to Tfap2a dosage in heterozygotes. Combined, these results suggest that closely linked but genetically separable changes in Bmp6 and Tfap2a contribute to a supergene underlying evolved skeletal gain in multiple freshwater stickleback populations.
KEYWORDS QTL; fine mapping; skeletal evolution; genome editing; supergene
INTRASPECIFIC morphological variation offers the opportunity to dissect the genetic changes that underlie evolution, including adaptation to novel environments. Genetic mapping studies of naturally varying traits can reveal the genomic regions that contribute to evolutionary changes. When multiple phenotypes are controlled by the same region of a genome, a single pleiotropic locus could affect multiple traits, or separate but closely linked genes could affect each trait independently. Clustering of two or more QTL into supergenes is a commonly described feature of evolution (Schwander etai. 2014; Thompson and Jiggins 2014), likely because close linkage of loci allows advantageous combinations of traits to be inherited together. Supergenes have been shown to control pigmentation patterns in locusts (Nabours 1933); mimetic patterns in butterflies (Joron et ai. 2011; Kunte et ai. 2014); color and...