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      Maternal Programming of Sexual Behavior and Hypothalamic-Pituitary-Gonadal Function in the Female Rat

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          Abstract

          Variations in parental care predict the age of puberty, sexual activity in adolescence and the age at first pregnancy in humans. These findings parallel descriptions of maternal effects on phenotypic variation in reproductive function in other species. Despite the prevalence of such reports, little is known about potential biological mechanisms and this especially true for effects on female reproductive development. We examined the hypothesis that parental care might alter hypothalamic-pituitary-ovarian function and thus reproductive function in the female offspring of rat mothers that vary pup licking/grooming (LG) over the first week postpartum. As adults, the female offspring of Low LG mothers showed 1) increased sexual receptivity; 2) increased plasma levels of luteinizing hormone (LH) and progesterone at proestrus; 3) an increased positive-feedback effect of estradiol on both plasma LH levels and gonadotropin releasing-hormone (GnRH) expression in the medial preoptic region; and 4) increased estrogen receptor α (ERα) expression in the anterioventral paraventricular nucleus, a system that regulates GnRH. The results of a cross-fostering study provide evidence for a direct effect of postnatal maternal care as well as a possible prenatal influence. Indeed, we found evidence for increased fetal testosterone levels at embryonic day 20 in the female fetuses of High compared to Low LG mothers. Finally, the female offspring of Low LG mothers showed accelerated puberty compared to those of High LG mothers. These data suggest maternal effects in the rat on the development of neuroendocrine systems that regulate female sexual behaviour. Together with studies revealing a maternal effect on the maternal behavior of the female offspring, these findings suggest that maternal care can program alternative reproductive phenotypes in the rat through regionally-specific effects on ERα expression.

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          Most cited references 92

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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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            The impact of economic hardship on black families and children: psychological distress, parenting, and socioemotional development.

             V McLoyd (1990)
            Family processes affecting the socioemotional functioning of children living in poor families and families experiencing economic decline are reviewed. Black children are of primary interest in the article because they experience disproportionate shares of the burden of poverty and economic loss and are at substantially higher risk than white children of experiencing attendant socioemotional problems. It is argued that (a) poverty and economic loss diminish the capacity for supportive, consistent, and involved parenting and render parents more vulnerable to the debilitating effects of negative life events, (b) a major mediator of the link between economic hardship and parenting behavior is psychological distress deriving from an excess of negative life events, undesirable chronic conditions, and the absence and disruption of marital bonds, (c) economic hardship adversely affects children's socioemotional functioning in part through its impact on the parent's behavior toward the child, and (d) father-child relations under conditions of economic hardship depend on the quality of relations between the mother and father. The extent to which psychological distress is a source of race differences in parenting behavior is considered. Finally, attention is given to the mechanisms by which parents' social networks reduce emotional strain, lessen the tendency toward punitive, coercive, and inconsistent parenting behavior, and, in turn, foster positive socioemotional development in economically deprived children.
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              Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress.

              Variations in maternal care affect the development of individual differences in neuroendocrine responses to stress in rats. As adults, the offspring of mothers that exhibited more licking and grooming of pups during the first 10 days of life showed reduced plasma adrenocorticotropic hormone and corticosterone responses to acute stress, increased hippocampal glucocorticoid receptor messenger RNA expression, enhanced glucocorticoid feedback sensitivity, and decreased levels of hypothalamic corticotropin-releasing hormone messenger RNA. Each measure was significantly correlated with the frequency of maternal licking and grooming (all r's > -0.6). These findings suggest that maternal behavior serves to "program" hypothalamic-pituitary-adrenal responses to stress in the offspring.
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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
                2008
                21 May 2008
                : 3
                : 5
                Affiliations
                Sackler Program for Epigenetics & Psychobiology at McGill University and the Douglas Mental Health University Institute, McGill University, Montréal, Canada
                The Rockefeller University, United States of America
                Author notes

                Conceived and designed the experiments: MM NC JD. Performed the experiments: NC Ad JD KM SS. Analyzed the data: NC JD KM. Wrote the paper: MM NC.

                Article
                07-PONE-RA-03062R1
                10.1371/journal.pone.0002210
                2374899
                18493313
                Cameron 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.
                Page count
                Pages: 12
                Categories
                Research Article
                Pediatrics and Child Health
                Developmental Biology/Neurodevelopment
                Evolutionary Biology/Animal Behavior
                Neuroscience/Behavioral Neuroscience
                Physiology/Endocrinology
                Physiology/Reproductive Physiology

                Uncategorized

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