Neural Gene Expression Profiles and Androgen Levels Underlie Alternative Reproductive Tactics in the Ocellated Wrasse, Symphodus ocellatus

Abstract

Discrete variation in reproductive behavior and physiology is observed in diverse taxa. Although it is known that most within‐sex alternative reproductive tactics arise as a consequence of phenotypic plasticity, relatively little is known about differential neural gene expression among plastic alternative reproductive phenotypes. In the ocellated wrasse Symphodus ocellatus, males exhibit one of three alternative tactics (nesting, satellite, and sneaker) within a reproductive season, but switch tactics between years. Satellites and sneakers spawn parasitically in dominant (nesting) males' nests, but only nesting males provide parental care. Nesting and satellite males show transient cooperative defense of nests against sneakers. Here, we analyze circulating sex steroid hormone levels and neural gene expression profiles in these three male phenotypes and in females. 11‐ketotestosterone (but not testosterone) was highest in nesting males, while estradiol was highest in females. Brain transcriptomes of satellites and females were most similar to each other and intermediate to nesting and sneaker males. Sneakers showed more total expression differences, whereas nesting males showed higher magnitude expression differences. Our findings reveal the surprising extent to which neural gene expression patterns vary across reproductive tactics that vary in a number of social traits, including aggression, territoriality, and cooperation, providing important insights into the molecular mechanisms that may underlie variation in cooperative and reproductive behavior.

Sperm competition shapes gene expression and sequence evolution in the ocellated wrasse

“…Previous work in this system has revealed somatic variation in gene expression among the male morphs that may be important in premating sexual selection (Stiver et al . ). Here, we focus on the consequences of postmating sexual selection on transcriptome evolution in the gonads.…”

“…Satellites are in many ways intermediate, investing in premating behaviours as well as postmating competitive traits (Stiver & Alonzo ; Stiver et al . ). The three male types in this species therefore represent a continuum of pre‐ and postmating sexual selection.…”

Brain Transcriptional Profiles of Male Alternative Reproductive Tactics and Females in Bluegill Sunfish

“…However, within ARTs, differences in neural expression profiles can often be larger among male tactics than between males and females [18][19][20]. In bluegill, only two transcripts were consistently differentially expressed in females when compared to all male groups and these corresponded to gal and tac.…”

Brain Transcriptional Profiles of Male Alternative Reproductive Tactics and Females in Bluegill Sunfish

“…These studies have found a large number of genes that vary among tactics in expression in the brain during mating. In the ocellated wrasse ( Symphodus ocellatus ), 1,048 genes were differentially expressed when comparing sneakers to two other male tactics (nesting and satellite) and to females [19]. In the black-faced blenny ( Tripterygion delaisi ) and peacock blenny ( Salaria pavo ), RNAseq identified approximately 600 transcripts differentially expressed within the brains of ‘sneaker’ versus other male tactics [18,20].…”