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Plasticity of the reproductive axis caused by social status change in an african cichlid fish: I. Pituitary gonadotropins.

ABSTRACT: Social position in a dominance hierarchy is often tightly coupled with fertility. Consequently, an animal that can recognize and rapidly take advantage of an opportunity to rise in rank will have a reproductive advantage. Reproduction in all vertebrates is controlled by the brain-pituitary-gonad axis, and in males of the African cichlid fish Astatotilapia burtoni, GnRH1 neurons at the apex of this axis are under social control. However, little is known about how quickly social information is transformed into functional reproductive change, or about how socially controlled changes in GnRH1 neurons influence downstream actions of the brain-pituitary-gonad axis. We created an opportunity for reproductively suppressed males to ascend in status and then measured how quickly the perception of this opportunity caused changes in mRNA and protein levels of the pituitary gonadotropins. mRNA levels of the ?-subunits of LH and FSH rose rapidly in the pituitary 30 min after suppressed males perceived an opportunity to ascend. In contrast, mRNA levels of GnRH receptor-1 remained unchanged during social transition but were higher in stable dominant compared with subordinate males. In the circulation, levels of both LH and FSH were also quickly elevated. There was a positive correlation between mRNA in the pituitary and circulating protein levels for LH and FSH, and both gonadotropins were positively correlated with plasma 11-ketotestosterone. Our results show that the pituitary is stimulated extremely rapidly after perception of social opportunity, probably to allow suppressed males to quickly achieve reproductive success in a dynamic social environment.

SUBMITTER: Maruska KP

PROVIDER: S-EPMC3219043 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Plasticity of the reproductive axis caused by social status change in an african cichlid fish: I. Pituitary gonadotropins.

Maruska Karen P KP Levavi-Sivan Berta B Biran Jakob J Fernald Russell D RD

Endocrinology 20101110 1

Social position in a dominance hierarchy is often tightly coupled with fertility. Consequently, an animal that can recognize and rapidly take advantage of an opportunity to rise in rank will have a reproductive advantage. Reproduction in all vertebrates is controlled by the brain-pituitary-gonad axis, and in males of the African cichlid fish Astatotilapia burtoni, GnRH1 neurons at the apex of this axis are under social control. However, little is known about how quickly social information is tra ...[more]

PMID: 21068157

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Project description:BackgroundCichlid fishes have evolved remarkably diverse reproductive, social, and feeding behaviors. Cell-to-cell signaling molecules, notably neuropeptides and peptide hormones, are known to regulate these behaviors across vertebrates. This class of signaling molecules derives from prohormone genes that have undergone multiple duplications and losses in fishes. Whether and how subfunctionalization, neofunctionalization, or losses of neuropeptides and peptide hormones have contributed to fish behavioral diversity is largely unknown. Information on fish prohormones has been limited and is complicated by the whole genome duplication of the teleost ancestor. We combined bioinformatics, mass spectrometry-enabled peptidomics, and molecular techniques to identify the suite of neuropeptide prohormones and pituitary peptide products in Astatotilapia burtoni, a well-studied member of the diverse African cichlid clade.ResultsUtilizing the A. burtoni genome, we identified 148 prohormone genes, with 21 identified as a single copy and 39 with at least 2 duplicated copies. Retention of prohormone duplicates was therefore 41 %, which is markedly above previous reports for the genome-wide average in teleosts. Beyond the expected whole genome duplication, differences between cichlids and mammals can be attributed to gene loss in tetrapods and additional duplication after divergence. Mass spectrometric analysis of the pituitary identified 620 unique peptide sequences that were matched to 120 unique proteins. Finally, we used in situ hybridization to localize the expression of galanin, a prohormone with exceptional sequence divergence in cichlids, as well as the expression of a proopiomelanocortin, prohormone that has undergone an additional duplication in some bony fish lineages.ConclusionWe characterized the A. burtoni prohormone complement. Two thirds of prohormone families contain duplications either from the teleost whole genome duplication or a more recent duplication. Our bioinformatic and mass spectrometric findings provide information on a major vertebrate clade that will further our understanding of the functional ramifications of these prohormone losses, duplications, and sequence changes across vertebrate evolution. In the context of the cichlid radiation, these findings will also facilitate the exploration of neuropeptide and peptide hormone function in behavioral diversity both within A. burtoni and across cichlid and other fish species.

Project description:The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.

Project description:BackgroundThe patterns and processes linked to the host specificity of parasites represent one of the central themes in the study of host-parasite interactions. We investigated the evolution and determinants of host specificity in gill monogeneans of Cichlidogyrus and Scutogyrus species parasitizing African freshwater fish of Cichlidae.MethodsWe analyzed (1) the link between host specificity and parasite phylogeny, (2) potential morphometric correlates of host specificity (i.e. parasite body size and the morphometrics of the attachment apparatus), and (3) potential determinants of host specificity following the hypothesis of ecological specialization and the hypothesis of specialization on predictable resources (i.e. host body size and longevity were considered as measures of host predictability), and (4) the role of brooding behavior of cichlids in Cichlidogyrus and Scutogyrus diversification.ResultsNo significant relationships were found between host specificity and phylogeny of Cichlidogyrus and Scutogyrus species. The mapping of host specificity onto the parasite phylogenetic tree revealed that an intermediate specialist parasitizing congeneric cichlid hosts represents the ancestral state for the Cichlidogyrus/Scutogyrus group. Only a weak relationship was found between the morphometry of the parasites' attachment apparatus and host specificity. Our study did not support the specialization on predictable resources or ecological specialization hypotheses. Nevertheless, host specificity was significantly related to fish phylogeny and form of parental care.ConclusionsOur results confirm that host specificity is not a derived condition for Cichlidogyrus/Scutogyrus parasites and may reflect other than historical constraints. Attachment apparatus morphometry reflects only partially (if at all) parasite adaptation to the host species, probably because of the morphological similarity of rapidly evolved cichlids (analyzed in our study). However, we showed that parental care behavior of cichlids may play an important role linked to host specificity of Cichlidogyrus/Scutogyrus parasites.

Dataset Information

Plasticity of the reproductive axis caused by social status change in an african cichlid fish: I. Pituitary gonadotropins.

Publications

Plasticity of the reproductive axis caused by social status change in an african cichlid fish: I. Pituitary gonadotropins.

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