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      Male Accessory Gland Protein Reduces Egg Laying in a Simultaneous Hermaphrodite

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          Abstract

          Seminal fluid is an important part of the ejaculate of internally fertilizing animals. This fluid contains substances that nourish and activate sperm for successful fertilization. Additionally, it contains components that influence female physiology to further enhance fertilization success of the sperm donor, possibly beyond the recipient's optimum. Although evidence for such substances abounds, few studies have unraveled their identities, and focus has been exclusively on separate-sex species. We present the first detailed study into the seminal fluid composition of a hermaphrodite ( Lymnaea stagnalis). Eight novel peptides and proteins were identified from the seminal-fluid-producing prostate gland and tested for effects on oviposition, hatching and consumption. The gene for the protein found to suppress egg mass production, Ovipostatin, was sequenced, thereby providing the first fully-characterized seminal fluid substance in a simultaneous hermaphrodite. Thus, seminal fluid peptides and proteins have evolved and can play a crucial role in sexual selection even when the sexes are combined.

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          Most cited references17

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          Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products.

          Female Drosophila melanogaster with environmentally or genetically elevated rates of mating die younger than controls. This cost of mating is not attributable to receipt of sperm. We demonstrate here that seminal fluid products from the main cells of the male accessory gland are responsible for the cost of mating in females, and that increasing exposure to these products increases female death rate. Main-cell products are also involved in elevating the rate of female egg-laying, in reducing female receptivity to further matings and in removing or destroying sperm of previous mates. The cost of mating to females may therefore represent a side-effect of evolutionary conflict between males.
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            Sexually antagonistic male adaptation triggered by experimental arrest of female evolution.

            W. Rice (1996)
            Each sex is part of the environment of the other sex. This may lead to perpetual coevolution between the sexes, when adaptation by one sex reduces fitness of the other. Indirect evidence comes from experiments with Drosophila melanogaster indicating that seminal fluid reduces the competitive ability of sperm from other males, thereby increasing male fitness. It also reduces a female's propensity to remate and increase her egg-laying rate. In contrast to these benefits to males, seminal fluid has substantial toxic side effects in females, with increasing quantity leading to decreasing female survival. Here I show that when female D. melanogaster are experimentally prevented from coevolving with males, males rapidly adapt to the static female phenotype. This male adaptation leads to a reduction in female survivorship, which is mediated by an increased rate of remating and increased toxicity of seminal fluid.
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              Male accessory gland secretions: modulators of female reproductive physiology and behavior.

              Secretions of male accessory glands contain a variety of bioactive molecules. When transferred during mating, these molecules exert wide-ranging effects on female reproductive activity and they improve the male's chances of siring a significant proportion of the female's offspring. The accessory gland secretions may affect virtually all aspects of the female's reproductive activity. The secretions may render her unwilling or unable to remate for some time, facilitating sperm storage and ensuring that any eggs laid will be fertilized by that male's sperm. They may stimulate an increase in the number and rate of development of eggs and modulate ovulation and/or oviposition. Antimicrobial agents in the secretions ensure that the female reproductive tract is a hospitable environment during sperm transfer. In a few species the secretions include noxious chemicals. These are sequestered by developing eggs that are thereby protected from predators and pathogens when laid.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                12 April 2010
                : 5
                : 4
                : e10117
                Affiliations
                [1 ]Animal Ecology, Faculty of Earth and Life Sciences, VU University, Amsterdam, The Netherlands
                [2 ]School of Biological Sciences, University of Queensland, St. Lucia, Queensland, Australia
                [3 ]Biomolecular Resource Facility, University of Texas Medical Branch, Galveston, Texas, United States of America
                [4 ]Department of Cellular Biology and Anatomy, Medical College of Georgia-University of Georgia Medical Partnership Campus, Athens, Georgia, United States of America
                [5 ]Max-Planck-Institute for Ornithology, Behavioural Neurobiology, Seewiesen, Germany
                Temasek Life Sciences Laboratory, Singapore
                Author notes

                Conceived and designed the experiments: JMK AtM. Performed the experiments: JMK WS KMW JSS GTN. Analyzed the data: JMK SFC GTN. Contributed reagents/materials/analysis tools: JMK SFC BMD JSS GTN. Wrote the paper: JMK AtM. Provided main funding: JMK.

                Article
                09-PONE-RA-14424R2
                10.1371/journal.pone.0010117
                2853560
                20404934
                628cadb5-73f6-4f88-8ceb-7c5d92abf0fd
                Koene 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
                : 19 November 2009
                : 12 March 2010
                Page count
                Pages: 7
                Categories
                Research Article
                Ecology/Evolutionary Ecology
                Evolutionary Biology/Animal Behavior
                Evolutionary Biology/Evolutionary Ecology
                Evolutionary Biology/Sexual Behavior
                Physiology/Reproductive Physiology

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