Mating behavior is controlled by acute changes in metabolic fuels

Abstract

. Mating behavior is controlled by acute changes in metabolic fuels. Am J Physiol Regulatory Integrative Comp Physiol 282: R782-R790, 2002; 10.1152/ajpregu.00383.2001.-Mild food restriction for 48 h inhibits mating behavior in female musk shrews (Suncus murinus). However, mating behavior is restored after a 90-min feeding bout. In this series of experiments, we examined the role of metabolic fuels in this behavioral restoration. First, drugs reported to block glycolysis or fatty acid oxidation were given 2 h before mating. Both treatments inhibited mating in food-restricted females that were refed after treatment. Blood glucose levels were assessed in females that were fed ad libitum, food restricted, or food restricted and refed for 90 min. Food restriction significantly lowered blood glucose compared with ad libitum feeding or food restriction in combination with 90 min of refeeding. However, neither glucose nor fat alone could substitute for food and promote mating behavior in food-restricted females. In addition, analysis of ketone bodies and body composition in females demonstrated low or undetectable levels of these energy substrates. Our data suggest that musk shrews have relatively little stored energy. Therefore, female musk shrews rely on continuous food intake and monitor multiple cues acutely, including glucose availability and fatty acid oxidation. This ensures that mating does not occur when adequate energy is unavailable. nutrition; glucose; fatty acids; anorexia; emesis SUCCESSFUL REPRODUCTION REQUIRES energy, typically attained by ingesting food consisting of proteins, fats, and carbohydrates. These macromolecules are broken down into amino acids, glycerol, fatty acids, and simple sugars. The brain almost exclusively uses glucose for energy production, while glucose and fatty acid oxidation are used in the periphery (18). In cases where glucose availability is inadequate (e.g., starvation and diabetes), ketone bodies can be used for neural energy. When food intake is limited, compensatory changes ensure that metabolic homeostasis is maintained (30). Initially, stored glycogen is broken down into glucose. With continued deprivation, the micromolecules in the liver are used to form glucose via gluconeogenesis. Next, fatty acid oxidation becomes the primary energy source in the periphery, and glucose or ketone bodies are shunted to the brain.During metabolic challenges, energy can be conserved by inhibition of processes that are unnecessary for immediate survival. For example, restricted food availability or limitations of specific metabolic fuels inhibit sexual behavior (5,14,17,20), hypothalamic gonadotropin-releasing hormone secretion (13), gonadotropin secretion (3, 4, 19), estrous cyclicity (22,23,28,29), and steroidogenesis (17, 19) in a wide variety of species (reviewed in Ref. 37). This is a reversible mechanism that allows females to maximize reproductive efficacy and synchronize reproduction with nutritional resources. Although estrous cycles and ovarian steroid secretion in Syrian hamst...

The Musk Shrew (Suncus murinus): A Model Species for Studies of Nutritional Regulation of Reproduction

“…These results are similar to the results with 2-DG in that the MA treatment prevented the refeeding-induced restoration of mating behavior ( Figure 4B). Treatment with the doses of metabolic inhibitors used (350 mg.kg of 2-DG and 20 mg/ kg of MA) had no effect on locomotor behavior or aggressive behavior during mating bouts (Temple et al 2002). In addition, neither glucose nor vegetable shortening could substitute for food and restore mating behavior.…”

“…Volume 45, Number 1 but the refed females treated with 2-DG before mating were significantly less likely to display mating behavior than ad libitum-fed females or refed females treated with saline (Temple et al 2002; Figure 4A). In our next study, we used the same experimental design, except that we used mercaptoacetate (MA 1 ), an inhibitor of fatty acid oxidation.…”

“…They are members of the order Insectivora, which is the third largest mammalian order, containing more than 450 species. Musk shrews have a very high metabolism, typical of insectivores, and they store very little fat (Ishii et al 2002;Temple et al 2002). In the wild, they breed at all times of the year, and their pregnancy rates vary with rainfall patterns (Barbehenn 1962;Harrison 1955;Louch et al 1966).…”

“…Based on this need, they are likely to be exquisitely sensitive to small reductions in food intake. (2) They have very little body fat (Temple et al 2002) and thus cannot rely on stored energy to carry them through periods of low food availability. (3) Mating behavior in musk shrews is not regulated by surges or peaks of steroid hormones (Fortman et al 1992;Rissman and Bronson 1987).…”

Regulating food intake

“…Urocortin, a member of the CRH family, is found both centrally and peripherally and inhibits food intake when administered in either location (31,33,34). There is evidence that urocortin acts in the paraventricular nucleus (15,33), although the lateral septum would appear to be a more important locus of urocortin action (32).…”