Divergence in androgen sensitivity contributes to population differences in sexual dimorphism of electrocommunication behavior.
ABSTRACT: Weakly-electric fish (Apteronotidae) produce highly diverse electrocommunication signals. Electric organ discharges (EODs) vary across species, sexes, and in the magnitude and direction of their sexual dimorphism. Gonadal steroid hormones can modulate EODs, and differences in androgen sensitivity are hypothesized to underlie variation in the degree of sexual dimorphism across species. In this study, we asked whether variation in androgen sensitivity explained variation in sexual dimorphism of EODs within species, at the population level. We examined two populations of black ghost knifefish (Apteronotus albifrons), one from the Orinoco and the other from the Amazon River Basin. EOD frequency (EODf) and chirp rates were measured to characterize diversity in sexual dimorphism across populations. The magnitude of sexual dimorphism in EODf differed significantly across populations, and was more pronounced in the Orinoco population than in the Amazon population. Chirp rates were sexually monomorphic in both populations. 11-Ketotestosterone (11-kT) was administered over a two-week period to assess population differences in sensitivity to androgens. 11-kT masculinized EODf significantly more in the population with the greater degree of sexual dimorphism. 11-kT had no effect on the sexually monomorphic chirping rates. We conclude that population divergence in androgen sensitivity contributes to variation in sexual dimorphism of EODf in A. albifrons.
Project description: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 5?-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 ?1 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.
Project description:Animal communication signals that simultaneously share the same sensory channel are likely to co-evolve to maximize the transmission of each signal component. Weakly electric fish continuously produce a weak electric field that functions in communication. Fish modulate the electric organ discharge (EOD) on short timescales to produce context-specific signals called chirps. EODs and chirps are simultaneously detected by electroreceptors and processed in the electrosensory system. We analyzed these signals, first to explore whether EOD waveform is encoded in the signal received by electroreceptors and then to examine how EODs and chirps interact to influence conspicuousness. Our findings show that gross discrimination of sinusoidal from complex EOD waveforms is feasible for all species, but fine discrimination of waveform may be possible only for species with waveforms of intermediate complexity. The degree of chirp frequency modulation and chirp relative decay strongly influenced chirp conspicuousness, but other chirp parameters were less influential. The frequency difference between the interacting EODs also strongly impacted chirp conspicuousness. Finally, we developed a method for creating hybrid chirp/EOD combinations to independently analyze the impact of chirp species, EOD species, and EOD difference frequency on chirp conspicuousness. All three components and their interactions strongly influenced chirp conspicuousness, which suggests that evolutionary changes in parameters of either chirps or EODs are likely to influence chirp detection. Examining other environmental factors such as noise created by fish movement and species-typical patterns of sociality may enrich our understanding of how interacting EODs affect the detection and discrimination of chirps across species.
Project description:The neuroplastic mechanisms in the fish brain that underlie sex reversal remain unknown. Gonadotropin-releasing hormone 3 (GnRH3) neurons control male reproductive behaviours in Mozambique tilapia and show sexual dimorphism, with males having a greater number of GnRH3 neurons. Treatment with androgens such as 11-ketotestosterone (KT), but not 17?-estradiol, increases the number of GnRH3 neurons in mature females to a level similar to that observed in mature males. Compared with oestrogen, the effect of androgen on neurogenesis remains less clear. The present study examined the effects of 11-KT, a non-aromatizable androgen, on cellular proliferation, neurogenesis, generation of GnRH3 neurons and expression of cell cycle-related genes in mature females. The number of proliferating cell nuclear antigen-positive cells was increased by 11-KT. Simultaneous injection of bromodeoxyuridine and 11-KT significantly increased the number of newly-generated (newly-proliferated) neurons, but did not affect radial glial cells, and also resulted in newly-generated GnRH3 neurons. Transcriptome analysis showed that 11-KT modulates the expression of genes related to the cell cycle process. These findings suggest that tilapia could serve as a good animal model to elucidate the effects of androgen on adult neurogenesis and the mechanisms for sex reversal in the fish brain.
Project description: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.
Project description:The Jaera albifrons complex contains five species of marine isopods (J. albifrons, J. praehirsuta, J. ischiosetosa, J. forsmani, and J. posthirsuta). These species, occurring on the shores of the North-Atlantic Ocean, are partially reproductively isolated by barriers due to sexual isolation (mate choice), genetic incompatibilities, and ecological specialization. Microsatellite loci would be useful for parentage-based analyses of sexual selection and studies of genetic structure in the context of speciation.Twenty-four microsatellite markers were developed for J. albifrons using pyrosequencing of enriched libraries. Patterns of polymorphisms were analyzed in 49 J. albifrons adult males sampled in two populations from Brittany (Western France). The average number of alleles per locus was 4.73 ± 2.45 and the average gene diversity was 0.55 ± 0.23. Most markers also successfully amplified in the three sibling species J. praehirsuta, J. ischiosetosa, and J. forsmani.These polymorphic and cross-amplifiable markers will be useful for population genetics and parentage studies in the J albifrons complex.
Project description:There are numerous reports of sexual dimorphism in brain structure in children and adults, but data on sex differences in infancy are extremely limited. Our primary goal was to identify sex differences in neonatal brain structure. Our secondary goal was to explore whether brain structure was related to androgen exposure or sensitivity. Two hundred and ninety-three neonates (149 males) received high-resolution structural magnetic resonance imaging scans. Sensitivity to androgen was measured using the number of cytosine, adenine, guanine (CAG) triplets in the androgen receptor gene and the ratio of the second to fourth digit, provided a proxy measure of prenatal androgen exposure. There was a significant sex difference in intracranial volume of 5.87%, which was not related to CAG triplets or digit ratios. Tensor-based morphometry identified extensive areas of local sexual dimorphism. Males had larger volumes in medial temporal cortex and rolandic operculum, and females had larger volumes in dorsolateral prefrontal, motor, and visual cortices. Androgen exposure and sensitivity had minor sex-specific effects on local gray matter volume, but did not appear to be the primary determinant of sexual dimorphism at this age. Comparing our study with the existing literature suggests that sex differences in cortical structure vary in a complex and highly dynamic way across the human lifespan.
Project description:We have previously shown that sexual dimorphism in the expression of mouse renal cytochrome P450s is mediated by androgens, probably at a transcriptional level [Henderson, Scott, Yang & Wolf (1990), Biochem. J. 266, 675-681]. In the present study we show that this effect is already observed for most isoenzymes at only 2-3 weeks of age, as is the ability to induce or suppress expression with exogenous testosterone. The testosterone responsiveness did, however, exhibit age- as well as dose-dependency. Intriguingly, the effects of androgen took up to 8 days to become maximized, and the dose of testosterone needed to convert the female into the male phenotype was much higher than the circulating levels normally found in males. Studies using testicular feminized (Tfm) male mice, which carry an androgen receptor defect, showed them to have the female kidney cytochrome P450 phenotype, and these animals were not responsive to testosterone treatment. These data demonstrate the involvement of the androgen receptor in the regulation process. Taken together, our results indicate that the androgen receptor does not interact directly with the P450 genes, but initiates a cascade of events leading to the changes in cytochrome P450 gene expression. Significant differences were observed in the degree of sexual dimorphism in kidney P450 expression in other mammalian species. The significance of these findings in relation to the observed sexual dimorphism in other species is discussed.
Project description:The liver plays a crucial role in a variety of physiological processes. Sexual dimorphism is markedly defined in liver disorders, such as fatty liver diseases and liver cancer, but barely addressed in the normal liver. Distinct sex hormone signaling between male and female livers is the major driving factor for hepatic sexual dimorphism. Over 6000 genes are differently expressed between male and female livers in mice. Here we address how sex hormone receptors, estrogen receptor alpha (ER?) and androgen receptor (AR), mediate sexually dimorphic gene expression in mouse livers. We identified 5192 ER? target genes and 4154 AR target genes using ChIP-Seq. Using liver-specific ER? or AR knockout mice, we further identified direct and functional target genes of ER? (123 genes) and AR (151 genes) that contribute to hepatic sexual dimorphism. We also found that the most significant sexually dimorphic gene expression was initiated at birth by comparing hepatic gene expression data from the embryonic stage E10.5 to the postnatal stage P60 during liver development. Overall, our study indicates that sex hormone receptor signaling drives sexual dimorphism of hepatic gene expression throughout liver development.
Project description:Females and males have distinct trait optima, resulting in selection for sexual dimorphism. However, most traits have strong cross-sex genetic correlations, which constrain evolutionary divergence between the sexes and lead to protracted periods of maladaptation during the evolution of sexual dimorphism. While such constraints are thought to be costly in terms of individual and population fitness, it remains unclear how severe such costs are likely to be. Building upon classical models for the 'cost of selection' in changing environments (sensu Haldane), we derived a theoretical expression for the analogous cost of evolving sexual dimorphism; this cost is a simple function of genetic (co)variances of female and male traits and sex differences in trait optima. We then conducted a comprehensive literature search, compiled quantitative genetic data from a diverse set of traits and populations, and used them to quantify costs of sexual dimorphism in the light of our model. For roughly 90% of traits, costs of sexual dimorphism appear to be modest, and comparable to the costs of fixing one or a few beneficial substitutions. For the remaining traits (approx. 10%), sexual dimorphism appears to carry a substantial cost-potentially orders of magnitude greater than costs of selection during adaptation to environmental changes.
Project description:The outcome of natural selection depends on the demographic processes of birth, death, and development. Here, we derive conditions for protected polymorphism in a population characterized by age- or stage-dependent demography with two sexes. We do so using a novel two-sex matrix population model including basic Mendelian genetics (one locus, two alleles, random mating). Selection may operate on survival, growth, or fertility, any or all of which may differ between the sexes. The model can therefore incorporate genes with arbitrary pleiotropic and sex-specific effects. Conditions for protected polymorphism are expressed in terms of the eigenvalues of the linearization of the model at the homozygote boundary equilibria. We show that in the absence of sexual dimorphism, polymorphism requires heterozygote superiority in the genotypic population growth rate. In the presence of sexual dimorphism, however, heterozygote superiority is not required; an inferior heterozygote may invade, reducing the population growth rate and even leading to extinction (so-called evolutionary suicide). Our model makes no assumptions about separation of time scales between ecological and evolutionary processes, and can thus be used to project sex×stage×genotype dynamics of eco-evolutionary processes. Empirical evidence that sexual dimorphism affects extinction risk is growing, yet sex differences are often ignored in evolutionary demography and in eco-evolutionary models. Our analysis highlights the importance of sexual dimorphism and suggests mechanisms by which an allele can be favored by selection, yet drive a population to extinction, as a result of the structure and interdependence of sex- and stage-specific processes.