Evolutionary differentiation of androgen receptor ohnologs is responsible for the development of androgen-dependent unique sexual characteristics in a teleost fish

Abstract Teleost fishes exhibit complex unique sexual characteristics, such as fin enlargement and courtship display, in response to androgens. However, the molecular mechanisms underlying their evolutionary acquisition remain largely unknown. To address this question, we analysed medaka (Oryzias latipes) mutants deficient in androgen receptor ohnologs (ara and arb) generated by the teleost-specific whole-genome duplication event (TSGD). We discovered that both ar ohnologs are not required for spermatogenesis and appear to be functionally redundant for courtship display in males, while both copies were necessary for their reproductive success; ara was required for tooth enlargement and behavioural attractiveness, while arb for male-specific fin morphogenesis and sexual motivation. We further showed that the differences in both the transcription of the two ars, cellular localisation of their encoded proteins and their downstream genetic programs could be responsible for the phenotypic diversity between the ara and arb mutants. These findings suggest that the ar ohnologs have diverged in the teleost lineage in two different ways: First through the loss of their roles in spermatogenesis and second through the gene duplication followed by functional differentiation that has likely resolved the pleiotropic roles derived from their ancestral gene. Thus, our results provide insights into how genome duplication impacts the massive diversification of sexual characteristics in the teleost lineage.