Structural genomic variation and behavioral interactions underpin a balanced sexual mimicry polymorphism

Here, we uncover the genetic architecture of a balanced sexual mimicry
polymorphism and identify behavioral mechanisms that may be involved in
its maintenance in the swordtail fish Xiphophorus birchmanni. We
find that ~40% of X. birchmanni males develop a “false gravid spot”, a
melanic pigmentation pattern that mimics the “pregnancy spot” associated
with sexual maturity in female live-bearing fish. Using genome-wide
association mapping, we detect a single intergenic region associated with
variation in the false gravid spot, which is upstream of kitlga, a gene
involved in melanophore patterning. By performing long-read sequencing
within and across populations, we identify complex structural
rearrangements between alternate alleles at this locus. The false gravid
spot haplotype drives increased allele-specific expression of kitlga,
which provides a mechanistic explanation for the increased melanophore
abundance that causes the spot. We speculate that structural variants
affecting gene regulation may be an underappreciated driver of balanced
polymorphisms across diverse species.