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      Brain Transcriptional Profiles of Male Alternative Reproductive Tactics and Females in Bluegill Sunfish

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          Abstract

          Bluegill sunfish ( Lepomis macrochirus) are one of the classic systems for studying male alternative reproductive tactics (ARTs) in teleost fishes. In this species, there are two distinct life histories: parental and cuckolder, encompassing three reproductive tactics, parental, satellite, and sneaker. The parental life history is fixed, whereas individuals who enter the cuckolder life history transition from sneaker to satellite tactic as they grow. For this study, we used RNAseq to characterize the brain transcriptome of the three male tactics and females during spawning to identify gene ontology (GO) categories and potential candidate genes associated with each tactic. We found that sneaker males had higher levels of gene expression differentiation compared to the other two male tactics. Sneaker males also had higher expression in ionotropic glutamate receptor genes, specifically AMPA receptors, compared to other males, which may be important for increased spatial working memory while attempting to cuckold parental males at their nests. Larger differences in gene expression also occurred among male tactics than between males and females. We found significant expression differences in several candidate genes that were previously identified in other species with ARTs and suggest a previously undescribed role for cAMP-responsive element modulator ( crem) in influencing parental male behaviors during spawning.

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          Most cited references45

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          Alternative reproductive strategies and tactics: diversity within sexes.

          Mart Gross (1996)
          Not all members of a sex behave in the same way. Frequency- and statusdependent selection have given rise to many alternative reproductive phenotypes within the sexes. The evolution and proximate control of these alternatives are only beginning to be understood. Although game theory has provided a theoretical framework, the concept of the mixed strategy has not been realized in nature, and alternative strategies are very rare. Recent findings suggest that almost all alternative reproductive phenotypes within the sexes are due to alternative tactics within a conditional strategy, and, as such, while the average fitnesses of the alternative phenotypes are unequal, the strategy is favoured in evolution. Proximate mechanisms that underlie alternative phenotypes may have many similarities with those operating between the sexes.
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            A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories.

            The induction of long-term potentiation (LTP) in the dentate gyrus of the hippocampus is associated with a rapid and robust transcription of the immediate early gene Zif268. We used a mutant mouse with a targeted disruption of Zif268 to ask whether this gene, which encodes a zinc finger transcription factor, is required for the maintenance of late LTP and for the expression of long-term memory. We show that whereas mutant mice exhibit early LTP in the dentate gyrus, late LTP is absent when measured 24 and 48 hours after tetanus in the freely moving animal. In both spatial and non-spatial learning tasks, short-term memory remained intact, whereas performance was impaired in tests requiring long-term memory. Thus, Zif268 is essential for the transition from short- to long-term synaptic plasticity and for the expression of long-term memories.
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              Galanin neurons in the medial preoptic area govern parental behavior

              Mice display robust, stereotyped behaviors toward pups: virgin males typically attack pups, while virgin females and sexually experienced males and females display parental care. We show here that virgin males genetically impaired in vomeronasal sensing do not attack pups and are parental. Further, we uncover a subset of galanin-expressing neurons in the medial preoptic area (MPOA) that are specifically activated during male and female parenting, and a different subpopulation activated during mating. Genetic ablation of MPOA galanin neurons results in dramatic impairment of parental responses in males and females and affects male mating. Optogenetic activation of these neurons in virgin males suppresses inter-male and pup-directed aggression and induces pup grooming. Thus, MPOA galanin neurons emerge as an essential regulatory node of male and female parenting behavior and other social responses. These results provide an entry point to a circuit-level dissection of parental behavior and its modulation by social experience.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 December 2016
                2016
                : 11
                : 12
                : e0167509
                Affiliations
                [1 ]Annis Water Resources Institute, Grand Valley State University, Muskegon, Michigan, United States of America
                [2 ]Department of Biology, University of Western Ontario, London, Ontario, Canada
                [3 ]Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire, United States of America
                [4 ]Department of Biology, University of Oklahoma, Norman, Oklahoma, United States of America
                Ohio State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: CGP BDN RK.

                • Data curation: CGP.

                • Formal analysis: CGP MDM.

                • Funding acquisition: BDN RK.

                • Investigation: CGP MDM.

                • Methodology: CGP RK BDN.

                • Project administration: CP BDN.

                • Visualization: CGP MDM.

                • Writing – original draft: CGP.

                • Writing – review & editing: CGP MDM RK BDN.

                Article
                PONE-D-16-18282
                10.1371/journal.pone.0167509
                5132329
                27907106
                22075174-f1f9-4a5e-aeec-59af2e2f4d1f
                © 2016 Partridge et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 May 2016
                : 15 November 2016
                Page count
                Figures: 4, Tables: 3, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: #250071-2012
                Award Recipient :
                Funded by: Department of Biology, University of Oklahoma
                Award Recipient :
                Funding for this project was supported through the Natural Sciences and Engineering Research Council of Canada (NSERC) to B.D.N (#250071-2012) and the University of Oklahoma Department of Biology to R.K. The funders had no role in any study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Genetics
                Gene Expression
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                Computational Biology
                Genome Analysis
                Transcriptome Analysis
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                Custom metadata
                The datasets supporting the conclusions of this article are available on the Sequence Read Archive (SRA) through BioProject ID: PRJNA287763. Environmental data, RNA quality information, the assembled transcriptome, the transcript count matrix, and R code for differential gene analysis are available on Dryad (doi: 10.5061/dryad.82fd8).

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