Differential expression of steroid-related genes across electrosensory brain regions in two sexually dimorphic species of electric knifefish.

The production of communication signals can be modulated by hormones acting on the brain regions that regulate these signals. However, less is known about how signal perception is regulated by hormones. The electrocommunication signals of weakly electric fishes are sexually dimorphic, sensitive to hormones, and vary across species. The neural circuits that regulate the production and perception of these signals are also well-characterized, and electric fishes are thus an excellent model to examine the neuroendocrine regulation of sensorimotor mechanisms of communication. We investigated (1) whether steroid-related genes are expressed in sensory brain regions that process communication signals; and (2) whether this expression differs across sexes and species that have different patterns of sexual dimorphism in their signals. Apteronotus leptorhynchus and Apteronotus albifrons produce continuous electric organ discharges (EODs) that are used for communication. Two brain regions, the electrosensory lateral line lobe (ELL) and the dorsal torus semicircularis (TSd), process inputs from electroreceptors to allow fish to detect and discriminate electrocommunication signals. We used qPCR to quantify the expression of genes for two androgen receptors (ar1, ar2), two estrogen receptors (esr1, esr2b), and aromatase (cyp19a1b). Four out of five steroid-related genes were expressed in both sensory brain regions, and their expression often varied between sexes and species. These results suggest that expression of steroid-related genes in the brain may differentially influence how EOD signals are encoded across species and sexes, and that gonadal steroids may coordinately regulate central circuits that control both the production and perception of EODs.

Electrocommunication signals and aggressive behavior vary among male morphs in an apteronotid fish, Compsaraia samueli.

Within-species variation in male morphology is common among vertebrates and is often characterized by dramatic differences in behavior and hormonal profiles. Males with divergent morphs also often use communication signals in a status-dependent way. Weakly electric knifefish are an excellent system for studying variation in male morphology and communication and its hormonal control. Knifefish transiently modulate the frequency of their electric organ discharge (EOD) during social encounters to produce chirps and rises. In the knifefish Compsaraia samueli, males vary extensively in jaw length. EODs and their modulations (chirps and rises) have never been investigated in this species, so it is unclear whether jaw length is related to the function of these signals. We used three behavioral assays to analyze EOD modulations in male C. samueli: (1) artificial playbacks, (2) relatively brief, live agonistic dyadic encounters, and (3) long-term overnight recordings. We also measured circulating levels of two androgens, 11-ketotestosterone and testosterone. Chirp structure varied within and across individuals in response to artificial playback, but was unrelated to jaw length. Males with longer jaws were more often dominant in dyadic interactions. Chirps and rises were correlated with and preceded attacks regardless of status, suggesting these signals function in aggression. In longer-term interactions, chirp rate declined after 1 week of pairing, but was unrelated to male morphology. Levels of circulating androgens were low and not predictive of jaw length or EOD signal parameters. These results suggest that communication signals and variation in male morphology are linked to outcomes of non-breeding agonistic contests.

Genes linked to species diversity in a sexually dimorphic communication signal in electric fish.

Sexually dimorphic behaviors are often regulated by androgens and estrogens. Steroid receptors and metabolism are control points for evolutionary changes in sexual dimorphism. Electric communication signals of South American knifefishes are a model for understanding the evolution and physiology of sexually dimorphic behavior. These signals are regulated by gonadal steroids and controlled by a simple neural circuit. Sexual dimorphism of the signals varies across species. We used transcriptomics to examine mechanisms for sex differences in electric organ discharges (EODs) of two closely related species, Apteronotus leptorhynchus and Apteronotus albifrons, with reversed sexual dimorphism in their EODs. The pacemaker nucleus (Pn), which controls EOD frequency (EODf), expressed transcripts for steroid receptors and metabolizing enzymes, including androgen receptors, estrogen receptors, aromatase, and 5α-reductase. The Pn expressed mRNA for ion channels likely to regulate the high-frequency activity of Pn neurons and for neuromodulator and neurotransmitter receptors that may regulate EOD modulations used in aggression and courtship. Expression of several ion channel genes, including those for Kir3.1 inward-rectifying potassium channels and sodium channel ß1 subunits, was sex-biased or correlated with EODf in ways consistent with EODf sex differences. Our findings provide a basis for future studies to characterize neurogenomic mechanisms by which sex differences evolve.

Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters.

Seasonally breeding animals exhibit profound physiological and behavioural responses to changes in ambient day length (photoperiod), including changes in reproductive function and territorial aggression.Species where aggression persists when gonads are regressed and circulating levels of gonadal hormones are low, such as Siberian hamsters (Phodopus sungorus) and song sparrows (Melospiza melodia), challenge the well-established framework that gonadal hormones are important mediators of aggression.A solution to this apparent paradox is that a season-specific increase in sensitivity to hormones in brain areas associated with aggression offsets low levels of gonadal hormones during periods of reproductive quiescence.To test this hypothesis, we manipulated photoperiod to induce natural fluctuations in seasonal phenotype across multiple stages of the annual reproductive cycle in female Siberian hamsters that display increased aggression during short-day reproductive quiescence, suggesting that behaviour persists independent of gonadal steroids.Females were housed in long "summer" days or short "winter" days for 10, 24 or 30 weeks to capture gonadal regression, transition back to a reproductively functional state and full gonadal recrudescence, respectively.Long-day animals maintained reproductive functionality and displayed low aggression across all time points. By week 10, short-day reproductively responsive females underwent gonadal regression and displayed increased aggression; non-responsive animals showed no such changes. At week 24, animals were in a transitional period and displayed an intermediate phenotype with respect to reproduction and aggression. By week 30, short-day females were fully recrudesced and returned to long-day-like levels of aggression.Consistent with our hypothesis, gonadally regressed females displayed decreases in 17ß-oestradiol (oestradiol) levels, but site-specific increases in the abundance of brain oestrogen receptor-alpha (ERα) in regions associated with aggression, but not reproduction. Increased site-specific ERα may function as a compensatory mechanism to allow increased responsiveness to oestradiol in regulating aggression in lieu of high circulating concentrations of hormones.Collectively, these results broaden our understanding of how breeding phenology maps onto social behaviour and the mechanisms that have evolved to coordinate behaviours that occur in non-breeding contexts.

Evolution of electric communication signals in the South American ghost knifefishes (Gymnotiformes: Apteronotidae): A phylogenetic comparative study using a sequence-based phylogeny.

The electric communication signals of weakly electric ghost knifefishes (Gymnotiformes: Apteronotidae) provide a valuable model system for understanding the evolution and physiology of behavior. Apteronotids produce continuous wave-type electric organ discharges (EODs) that are used for electrolocation and communication. The frequency and waveform of EODs, as well as the structure of transient EOD modulations (chirps), vary substantially across species. Understanding how these signals have evolved, however, has been hampered by the lack of a well-supported phylogeny for this family. We constructed a molecular phylogeny for the Apteronotidae by using sequence data from three genes (cytochrome c oxidase subunit 1, recombination activating gene 2, and cytochrome oxidase B) in 32 species representing 13 apteronotid genera. This phylogeny and an extensive database of apteronotid signals allowed us to examine signal evolution by using ancestral state reconstruction (ASR) and phylogenetic generalized least squares (PGLS) models. Our molecular phylogeny largely agrees with another recent sequence-based phylogeny and identified five robust apteronotid clades: (i) Sternarchorhamphus+Orthosternarchus, (ii) Adontosternarchus, (iii) Apteronotus+Parapteronotus, (iv) Sternarchorhynchus, and (v) a large clade including Porotergus, 'Apteronotus', Compsaraia, Sternarchogiton, Sternarchella, and Magosternarchus. We analyzed novel chirp recordings from two apteronotid species (Orthosternarchus tamandua and Sternarchorhynchus mormyrus), and combined data from these species with that from previously recorded species in our phylogenetic analyses. Some signal parameters in O. tamandua were plesiomorphic (e.g., low frequency EODs and chirps with little frequency modulation that nevertheless interrupt the EOD), suggesting that ultra-high frequency EODs and "big" chirps evolved after apteronotids diverged from other gymnotiforms. In contrast to previous studies, our PGLS analyses using the new phylogeny indicated the presence of phylogenetic signals in the relationships between some EOD and chirp parameters. The ASR demonstrated that most EOD and chirp parameters are evolutionarily labile and have often diversified even among closely related species.