Abstract In many multicellular organisms, male and female developmental fates are not determined by the classic XX/XY or ZW/ZZ systems but rather by a third type of sex chromosomes, the U/V sex chromosomes. In U/V systems, sex is expressed in the haploid phase, with U chromosomes confined to females and V chromosomes to males. Here, we explore several male, female and partially sex- reversed male lines of a giant kelp with a U/V system, to decipher the role of U/V sex chromosomes and autosomes in the initiation of male versus female developmental programs. Using comparative transcriptomics and experimental approaches, we identify a small set of genes located on the V- and U sex chromosomes that play a role in triggering the male versus female developmental programs, and we uncover a subset of autosomal effector genes. We describe the transcriptomic pathways underlying sexual differentiation and show that male, but not female, developmental fate involves large-scale transcriptome reorganization with pervasive enrichment in regulatory genes affecting the expression of more than half of the giant kelp genome. Furthermore, male-biased genes are more species-specific and exhibit faster evolutionary rates than unbiased genes, whereas genes underlying female developmental fate are more evolutionary conserved. Our observations imply that a female- like phenotype is the “ground state” of the giant kelp morphology, which is complemented by the presence of a U-chromosome, but overridden by a dominant male developmental program in the presence of a V-chromosome.

Developmental pathways underlying sexual differentiation in a U/V sex chromosome system