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

Abstract

Bluegill sunfish (Lepomis macrochirus) are one of the classic systems for studying male alternative reproductive tactics (ARTs) in teleost fishes. In this species, there are two distinct life histories: parental and cuckolder, encompassing three reproductive tactics, parental, satellite, and sneaker. The parental life history is fixed, whereas individuals who enter the cuckolder life history transition from sneaker to satellite tactic as they grow. For this study, we used RNAseq to characterize the brain transcriptome of the three male tactics and females during spawning to identify gene ontology (GO) categories and potential candidate genes associated with each tactic. We found that sneaker males had higher levels of gene expression differentiation compared to the other two male tactics. Sneaker males also had higher expression in ionotropic glutamate receptor genes, specifically AMPA receptors, compared to other males, which may be important for increased spatial working memory while attempting to cuckold parental males at their nests. Larger differences in gene expression also occurred among male tactics than between males and females. We found significant expression differences in several candidate genes that were previously identified in other species with ARTs and suggest a previously undescribed role for cAMP-responsive element modulator (crem) in influencing parental male behaviors during spawning.

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., ).…”

“…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., ). In sailfin mollies ( Poecilia latipinna ), differentially expressed transcripts were also associated with each ART: in which small males and large males have fixed alternative tactics, always displaying sneaking and courtship behaviour, respectively, whereas intermediate males display courtship or sneaking behaviour depending on the male composition of their social environment (Fraser et al., ).…”

“…However, when one compares the available brain RNA‐seq transcriptome data for teleost species with ARTs, no clear pattern emerges. Whereas in some species sneaker males exhibit the most distinctive transcriptome (e.g., L. macrochirus (Partridge et al., ); Tripterygion delaisi (Schunter et al., ); present study), in other species nest‐holder males are the most differentiated phenotype (e.g., Symphodus ocellatus Nugent et al., ). Similarly, the lists of differentially expressed genes for functionally equivalent phenotypes (e.g., sneakers) across species do not share significant numbers of transcripts, suggesting that ARTS may have evolved in different species through species‐specific genetic architectures.…”

“…For example, the use of whole brain samples may have masked regional differences in gene expression between phenotypes. Nevertheless, whole brain transcriptome analyses have been very informative as a first approach to characterize behavioural phenotypes namely in the ART literature (Aubin‐Horth et al., ; Fraser et al., ; Nugent et al., ; Partridge et al., ; Schunter et al., ; Stiver et al., ). Similarly, the use of sample pooled replicates offers the advantage of incorporating information from more individuals into DE analysis while still allowing for the estimation of biological variability (Todd, Black, & Gemmell, ), although greater power in the statistical analysis would have been gained using more biological replicates (Robles et al., ).…”

“…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, ).…”