Neuroendocrine profiles associated with discrete behavioural variation in Symphodus ocellatus, a species with male alternative reproductive tactics

Abstract

The molecular mechanisms underlying phenotypic plasticity are not well understood. Identifying mechanisms underlying alternative reproductive tactics (ARTs) in species for which the behavioural and fitness consequences of this variation are well characterized provides an opportunity to integrate evolutionary and mechanistic understanding of the maintenance of variation within populations. In the ocellated wrasse Symphodus ocellatus, the behavioural phenotypes of three distinct male morphs (sneakers, satellites and nesting males), which arise from a single genome, have been thoroughly characterized. To determine the neuroendocrine and genomic mechanisms associated with discrete phenotypic variation and ARTs in S. ocellatus in their natural environment, we constructed a whole-brain de novo transcriptome and compared global patterns of gene expression between sexes and male morphs. Next, we quantified circulating cortisol and 11-ketotestosterone (11-kt), mediators of male reproductive behaviours, as well as stress and gonadal steroid hormone receptor expression in the preoptic area, ventral subpallial division of the telencephalon and dorsolateral telencephalon, critical brain regions for social and reproductive behaviours. We found higher levels of 11-kt in nesting males and higher levels of cortisol in sneaker males relative to other male morphs and females. We also identified distinct patterns of brain region-specific hormone receptor expression between males such that most hormone receptors are more highly expressed in satellites and nesting males relative to sneakers and females. Our results establish the neuroendocrine and molecular mechanisms that underlie ARTs in the wild and provide a foundation for experimentally testing hypotheses about the relationship between neuromolecular processes and reproductive success.

Temporal variation in brain transcriptome is associated with the expression of female mimicry as a sequential male alternative reproductive tactic in fish

“…We found that each peacock blenny phenotype has a distinct transcriptomic profile (Figure a), indicating that distinct behavioural repertoires are associated with distinct neurogenomic states, which differentiate not only sex but also male morphs. These results are consistent with previous studies that have already described this parallel between specific behavioural states and neurogenomic states at different timescales (reviewed in Zayed & Robinson, ; Harris & Hofmann, ; Cardoso, Teles, & Oliveira, ), and with previous reports of specific brain transcriptomic profiles among species with ARTs for alternative male morphs, particularly in teleost fishes (Aubin‐Horth et al., ; Fraser et al., ; Nugent et al., ; Partridge et al., ; Schunter et al., ; Stiver et al., ). For example, in bluegill sunfish ( Lepomis macrochirus ), the three male ARTs, encompassing two distinct life histories, presented distinct neurogenomic profiles, with sneaker males having the most divergent expression profile, while parental males were further discriminated in the analysis relatively to their reproductive state (i.e., spawning vs. nonspawning; Partridge et al., ).…”

“…with ARTs for alternative male morphs, particularly in teleost fishes (Aubin-Horth et al, 2005;Fraser et al, 2014;Nugent et al, 2016;Partridge et al, 2016;Schunter et al, 2014;Stiver et al, 2015). For example, in bluegill sunfish (Lepomis macrochirus), the three male ARTs, encompassing two distinct life histories, presented distinct neurogenomic profiles, with sneaker males having the most divergent expression profile, while parental males were further discriminated in the analysis relatively to their reproductive state (i.e., spawning vs. nonspawning; Partridge et al, 2016).…”

“…Within teleosts, the variability of reproductive systems is vast, and most studies have focused on the characterization of whole‐brain gene expression patterns associated with discrete reproductive phenotypes. In all studies, gene expression differences between members of the same species that differ in plasticity of mating tactics reflect how they differ in behaviour and life history (Aubin‐Horth, Landry, Letcher, & Hofmann, ; Fraser, Janowitz, Thairu, Travis, & Hughes, ), and these differences are more pronounced among male tactics than between sexes (Nugent, Stiver, Alonzo, & Hofmann, ; Partridge, MacManes, Knapp, & Neff, ; Schunter, Vollmer, Macpherson, & Pascual, ; Stiver, Harris, Townsend, Hofmann, & Alonzo, ).…”

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour, sperm characteristics and social interactions

“…Differences in 11‐kt between flutamide‐ and vehicle‐injected nesting males were assessed by two‐tailed t test in r (R Development Core Team, ) with α < 0.05. We focus here on 11‐kt and did not measure testosterone in this study, as testosterone does not appear to play a major role in nesting male‐specific behaviours (Nugent et al, ; Stiver et al, ), consistent with 11‐kt as the dominant androgen in teleosts (Kindler, Philipp, Gross, & Bahr, ; Rodgers, Earley, & Grober, ). Ocellated wrasses are relatively small (e.g., nesting males are ~7–9 cm standard length).…”

Unravelling the evolution of complex reproductive traits with phenotypic engineering

“…Flutamide competitively inhibits the natural ligands of the AR, and when AR inhibition occurs in the testes, it is associated with a decrease in testicular androgen production. Nesting males have naturally elevated levels of 11‐ketotestosterone, the primary testicular androgen in teleost fishes, compared to satellite or sneaker males (Nugent, Stiver, Alonzo, & Hofmann, ). However, nesting males injected with flutamide in this study showed reduced circulating 11‐ketotestosterone compared to control males only injected with the vehicle.…”