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

Abstract

Distinct patterns of gene expression often underlie intra- and intersexual differences, and the study of this set of coregulated genes is essential to understand the emergence of complex behavioural phenotypes. Here, we describe the development of a de novo transcriptome and brain gene expression profiles of wild-caught peacock blenny, Salaria pavo, an intertidal fish with sex-role reversal in courtship behaviour (i.e., females are the courting sex) and sequential alternative reproductive tactics in males (i.e., larger and older nest-holder males and smaller and younger sneaker males occur). Sneakers mimic both female's courtship behaviour and nuptial coloration to get access to nests and sneak fertilizations, and later in life transition into nest-holder males. Thus, this species offers the unique opportunity to study how the regulation of gene expression can contribute to intersex phenotypes and to the sequential expression of male and female behavioural phenotypes by the same individual. We found that at the whole brain level, expression of the sneaker tactic was paralleled by broader and divergent gene expression when compared to either females or nest-holder males, which were more similar between themselves. When looking at sex-biased transcripts, sneaker males are intersex rather than being either nest-holder or female-like, and their transcriptome is simultaneously demasculinized for nest-holder-biased transcripts and feminized for female-biased transcripts. These results indicate that evolutionary changes in reproductive plasticity can be achieved through regulation of gene expression, and in particular by varying the magnitude of expression of sex-biased genes, throughout the lifetime of the same individual.

DNA methylation patterns in the round goby hypothalamus support an on-the-spot decision scenario for territorial behaviour

“…Previous studies identified distinct gene expression patterns associated with reproductive phenotypes in fish [32][33][34][35][36][37][38][39]65]. Similarly, we identified DNA methylation patterns that discriminate between non-territorial and territorial males.…”

“…To compare our results with previous studies, we searched the literature on fish alternative reproductive tactics and sex determination for genes that were reported as differentially expressed in alternative reproductive morphs by quantitative PCR, microarray analysis, or transcriptome sequencing[32][33][34][35][36][37][38][39][63][64][65]. Gene names were noted as reported in text, tables or figures and are listed inTable S2.To identify the corresponding genes in round goby, we first identified the zebrafish orthologue on ZFIN wherever possible and retrieved the gene symbol.…”

The ART of brain expression

“…Alternative reproductive tactics ( ART s) are widespread in the animal kingdom. In this issue of Molecular Ecology, Cardoso, Gonçalves, Goesmann, Canário, and Oliveira () investigate plastic ART s of the peacock blenny ( Salaria pavo ), in which males occur in three morphs: nestholders, sneakers and transitionals between the two former. They apply transcriptome sequencing to answer the question how brain gene expression contributes to sex role‐specific behaviour and to intersex phenotypes.…”

“…Males of the peacock blenny ( Salaria pavo ) population investigated by Cardoso et al. () can follow three different developmental strategies. Depending on their birth date, they either reproduce directly as territorial nestholder males or they reproduce shortly as parasitic sneaker males and change within their first breeding season to the nestholder morphology (transient strategy) or they reproduce their first season as sneakers and only in their second season as nestholders (sneaker strategy).…”

“…Nestholder males usually do not leave nests and hence have little access to new energy intake. The network analysis also revealed a downregulation of Gprotein-coupled-receptor (GPCR) pathway in sneakers, which might suggest that their brain is less susceptible to (steroidal) gonad signalling via these receptors.Gene-ontology (GO) analysis of female-biased genes that also show upregulation in sneakers but not in transitionals suggests a role for Males of the peacock blenny (Salaria pavo) population investigated byCardoso et al (2017) can follow three different developmental strategies. Depending on their birth date, they either reproduce directly as territorial nestholder males or they reproduce shortly as parasitic sneaker males and change within their first breeding season to the nestholder morphology (transient strategy) or they reproduce their first season as sneakers and only in their second season as nestholders (sneaker strategy).…”