Skeletal muscles that actuate sexual displays are specialized for de novo androgen synthesis

Abstract

The gonads (testes) act as the primary organ where androgenic hormones are made to regulate reproductive behavior in male vertebrates. Yet many endocrinologists have also long suspected that other tissues in the body can autonomously synthesize their own androgens to support behavioral output. We examine this idea here by studying whether avian skeletal muscles that actuate elaborate socio-sexual displays are specialized to maintain the molecular machinery otherwise needed for de novo androgen synthesis. Our results show that the vocal organ, or syrinx (SYR), of two songbirds species does in fact express all transporters and enzymes necessary to create androgenic hormones from scratch. This includes genes that encode proteins to mediate rate-limiting steps of steroidogenesis, which are seldom found outside of the gonads. We also show that expression levels of these genes are far greater in the SYR than non-display muscles, matching expression levels found in another extra-gonadal site of steroidogenesis--the brain. Furthermore, we uncover a nearly identical gene expression signature in a woodpecker neck muscle, the longus colli ventralis (LC). This tissue actuates the birds social drum display, which serves the same functions as song. This same study also demonstrates that the elevated expression of steroidogenic genes persists in this neck muscle year-round, suggesting that the LCs capacity to make androgens is a constitutive trait. Altogether, our findings suggest that muscles involved in sexual display is uniquely specialized to locally make steroid hormones, likely supporting their own role in behavioral production.