From primates to bees, social status regulates reproduction. In the cichlid fish Astatotilapia (Haplochromis) burtoni, subordinate males have reduced fertility and must become dominant to reproduce. This increase in sexual capacity is orchestrated by neurons in the preoptic area, which enlarge in response to dominance and increase expression of gonadotropin-releasing hormone 1 (GnRH1), a peptide critical for reproduction. Using a novel behavioral paradigm, we show for the first time that subordinate males can become dominant within minutes of an opportunity to do so, displaying dramatic changes in body coloration and behavior. We also found that social opportunity induced expression of the immediate-early gene egr-1 in the anterior preoptic area, peaking in regions with high densities of GnRH1 neurons, and not in brain regions that express the related peptides GnRH2 and GnRH3. This genomic response did not occur in stable subordinate or stable dominant males even though stable dominants, like ascending males, displayed dominance behaviors. Moreover, egr-1 in the optic tectum and the cerebellum was similarly induced in all experimental groups, showing that egr-1 induction in the anterior preoptic area of ascending males was specific to this brain region. Because egr-1 codes for a transcription factor important in neural plasticity, induction of egr-1 in the anterior preoptic area by social opportunity could be an early trigger in the molecular cascade that culminates in enhanced fertility and other long-term physiological changes associated with dominance.
Androgens are an important output of the hypothalamic-pituitary-gonadal (HPG) axis that controls reproduction in all vertebrates. In male teleosts two androgens, testosterone and 11-ketotestosterone, control sexual differentiation and development in juveniles and reproductive behavior in adults. Androgenic signals provide feedback at many levels of the HPG axis, including the hypothalamic neurons that synthesize and release gonadotropin-releasing hormone 1 (GnRH1), but the precise cellular site of androgen action in the brain is not known. Here we describe two androgen receptor subtypes, ARα and ARβ, in the cichlid Astatotilapia burtoni and show that these subtypes are differentially located throughout the adult brain in nuclei known to function in the control of reproduction. ARα was expressed in the ventral part of the ventral telencephalon, the preoptic area (POA) of the hypothalamus and the ventral hypothalamus, whereas ARβ was more widely expressed in the dorsal and ventral telencephalon, the POA, and the ventral and dorsal hypothalamus. We provide the first evidence in any vertebrate that the GnRH1-releasing neurons, which serve as the central control point of the HPG axis, express both subtypes of AR. Using quantitative real-time PCR, we show that A. burtoni AR subtypes have different expression levels in adult tissue, with ARα showing significantly higher expression than ARβ in the pituitary, and ARβ expressed at a higher level than ARα in the anterior and middle brain. These data provide important insight into the role of androgens in regulating the vertebrate reproductive axis. Keywordsin situ hybridization; gonadotropin-releasing hormone; androgen receptor subtypes; teleost Androgens are one endocrine output of the hypothalamic-pituitary-gonadal (HPG) axis that controls reproduction in all vertebrates. In male fish, the major androgens testosterone and 11-ketotestosterone (11-KT) are important for regulating sexual differentiation and functional development at all levels of the HPG axis (Borg, 1994). For example, exogenous androgens accelerate gonadal differentiation, spermatogenesis, and maturation of the hypothalamic and pituitary cells that synthesize and release the signaling peptides to mediate reproductive function (Amano et al., 1994;Goos et al., 1986;Miura et al., 1991a;Montero et al., 1995;Piferrer et al., 1993;Schreibman et al., 1986). If administered early enough in development in some teleost species, sex steroids can induce complete gonadal sex inversion in either direction (Hunter and Donaldson, 1983). In addition androgens also influence the adult HPG axis, mediating important social and reproductive behaviors, including courtship, territoriality, and aggression (Borg, 1994;Breton and Sambroni, 1996;Trudeau et al., 1991).Many physiological actions of androgens are mediated by the androgen receptor (AR) family. As with other steroid hormone receptors, ARs are ligand-dependent transcription factors, containing a highly conserved DNA-binding domain (DBD) and a moderately well cons...
In Astatotilapia burtoni, dominant males have higher levels of sex steroid hormones than subordinate males. Because of the complex regulatory interactions between steroid hormones and receptors, we asked whether dominance is also associated with variation in sex steroid receptor gene expression. Using quantitative PCR, we compared the expression of specific subtypes of androgen (AR) and estrogen (ER) receptor genes between dominant and subordinated males in 3 divisions of the brain, the pituitary, and the testes. We measured mRNA levels of AR-α, AR-β, ER-α, ER-βa, and ER-βb, gonadotropin releasing hormone 1 (GnRH1), and GnRH receptor 1 (GnRH-R1) relative to 18S rRNA. In the anterior part of the brain, we found that dominant males had higher mRNA expression of AR-α, AR-β, ER-βa, and ER-βb, but not ER-α, compared to subordinate males. This effect of dominance was reflected in a positive correlation between testes size and AR-α, AR-β, ER-βa, and ER-βb in the anterior brain. In addition, mRNA levels of all ARs and ERs in the anterior brain were positively correlated with mRNA level of GnRH1. In the middle and posterior portions of the brain, as well as the testes, steroid receptor mRNA levels were similar among dominants and subordinates. In the pituitary, ER-α mRNA level was positively correlated with testes size and AR-α mRNA was positively correlated with GnRH-R1 mRNA level. These data suggest that dominant male brains could be more sensitive to sex steroids, which may contribute to the increased complexity of the behavioral repertoires of dominant males. Keywordssteroid hormone receptor; testosterone; estradiol; social dominance; evolution; cichlid; teleost; fish In the cichlid fish Astatotilapia (Haplochromis) burtoni, social status regulates male fertility by controlling the brain-pituitary-gonad (BPG) axis. Consequently, dominant males have 40% larger testes relative to body size compared with subordinate males. Ultimately, dominance affects testes size through regulation of gonadotropin-releasing hormone 1 (GnRH1) production by neurons in the anterior parvocellular preoptic nucleus (aPPn) of the hypothalamus (Davis and Fernald, 1990;Francis et al., 1993;White et al., 2002). The enlarged testes of dominant males contain a higher proportion of mature sperm (Fraley and Fernald, 1982), and produce higher levels of testicular hormones, including 11-ketotestosterone and testosterone (Parikh et al., 2006). The higher levels of circulating androgens in dominant males have behavioral (Francis et al., 1992) and physiological (Soma et al., 1996) consequences. ToCorrespondence to SSB at current address: Department of Biology, University of North Carolina, Chapel Hill, NC 27599, phone: 919-843-5105; fax: 919-962-1625, sburmeister@unc.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting pro...
We examined patterns of neural activity as assayed by changes in gene expression to localize representation of acoustic mating signals in the auditory midbrain of frogs. We exposed wild-caught male Physalaemus pustulosas to conspecific mating calls that vary in their behavioral salience, nonsalient mating calls, or no sound. We measured expression of the immediate early gene egr-1 (also called ZENK, zi/268, NGFI-A, and krox-lA) throughout the torus semicircularis, the auditory midbrain homolog of the inferior coUiculus. Differential egr-1 induction in response to the acoustic stimuli occurred in the laminar, midline, and principal nuclei of the torus semicircularis, whereas the ventral region did not show significant effects of stimulus. The laminar nucleus differentially responded to conspecific mating calls compared with nonsalient mating calls, whereas the midline and principal nuclei responded preferentially to one of two conspecific calls. These responses were not explained by simple acoustic properties of the stimuli, and they demonstrate a functional heterogeneity of auditory processing of complex biological signals within the frog midbrain. Moreover, using analyses that assess the ability of the torus semicircularis as a whole to discriminate among acoustic stimuli, we found that activity patterns in the four regions together provide more information about biologically relevant acoustic stimuli than activity in any single region.
Although the telencephalon of ray-finned fishes has garnered considerable attention from comparative neuroanatomists, detailed descriptions of telencephalic organization are available for only a few species. This necessarily limits our understanding of telencephalic evolution, particularly in light of the extraordinary diversity of ray-finned fishes. Thus, we have charted the cyctoarchitecture of the telencephalon of the African cichlid fish, Astatotilapia (Haplochromis) burtoni. We examined tissue sectioned in the transverse plane, and categorized cell groups based on size, shape, and staining intensity of cells, the density and distribution of cells, cell-poor zones, and relationship of cell groups to the anterior commissure and external sulci. In addition, to facilitate visualization of the transitions among cell groups, we aligned and animated a series of 100 sequential brain sections. We found that the A. burtoni telencephalon was similar to other percomorphs in being highly elaborated with many distinct cell groups. In the pallium, Dm, Dl, and Dc had a large number of cell groups, whereas Dd and Dp were more uniform. Although we recognized many similarities between the pallium of A. burtoni and other teleosts, we also recognized two cell groups (Dl-g and Dm-2) that might represent specializations of cichlids. We found that the subpallium had a similar organization to that of other ray-finned fishes.
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