Nicole E Schwartz, Margaret P Schmill, Marcell D Cadney, Alberto A Castro, David A Hillis, Monica P McNamara, Jaanam O Rashid, William Lampman, Dorothea F DeLaCruz, Bao D Tran, Natalie L Trutalli, Theodore Garland
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We used mice from a long-term artificial selection experiment for high voluntary wheel-running behavior to determine whether maternal exercise opportunity affected (1) maternal physical activity, (2) maternal care behavior, or (3) offspring physical activity and body composition. Eighty prospective dams (40 from 4 selectively bred High Runner [HR] lines and 40 from 4 non-selected Control [CON] lines) were housed with continuous wheel access starting two weeks prior to breeding and ending 10 days postpartum, after which dams were housed without wheels until offspring weaning (21 days postpartum). An additional 100 dams (50 HR, 50 CON) were housed without wheels. Prospective dams from HR lines ran more revolutions/day (mainly by running faster) than those from CON lines when individually housed and in the days leading up to, but not after, birth. During postpartum days 1-5, HR and CON dams with wheels tended to exhibit less maternal behavior than those without (P<sub>Wheel</sub> = 0.0672). During post-partum days 6-10, HR dams with wheels continued to exhibit less maternal behavior than those without, whereas CON dams with wheels exhibited more than those without (P<sub>Linetype*Wheel</sub> = 0.0218). The proportion of dams giving birth did not differ among groups. However, CON dams with wheels were less likely to have litter death between birth and weaning than those without wheels, whereas the opposite was true for HR dams (P<sub>Linetype*Wheel</sub> = 0.0447). Both HR and CON dams with wheels had litters with a higher proportion of females at weaning than those without wheels (P<sub>Wheel</sub> = 0.0129). Maternal wheel access had few statistically significant effects on offspring, but may have resulted in developmental delays (e.g., delayed eye opening and decreased lean mass at weaning and sexual maturity). Additionally, maternal wheel access and sex may have interacted to affect wheel-running distance (P<sub>Sex*Wheel</sub> = 0.0683) and duration (P<sub>Sex*Wheel</sub> = 0.0926); female offspring from dams with wheels ran fewer revolutions per day, by running fewer minutes per day, than from dams without wheels, whereas males ran more. However, maternal exercise had no statistically significant effects on offspring food consumption (mass-adjusted), home-cage activity, open-field behavior, the reproductive characteristics of offspring, their adult body composition, nor relative organ masses; nor did maternal wheel access have statistically significant effects on grand-offspring food consumption, body composition or voluntary exercise behavior. Overall, our results provide some support for maternal exercise opportunity altering maternal care behavior. Altered maternal care could explain the observed trends in offspring survival, development, and voluntary exercise behavior. However, these effects did not have apparent long-lasting impacts on offspring or grand-offspring body composition or reproductive characteristics.</p>","PeriodicalId":20201,"journal":{"name":"Physiology & Behavior","volume":" ","pages":"114752"},"PeriodicalIF":2.4000,"publicationDate":"2024-11-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Maternal exercise opportunity before, during, and after pregnancy alters maternal care behavior and offspring development and survival, but has few effects on offspring physical activity or body composition.\",\"authors\":\"Nicole E Schwartz, Margaret P Schmill, Marcell D Cadney, Alberto A Castro, David A Hillis, Monica P McNamara, Jaanam O Rashid, William Lampman, Dorothea F DeLaCruz, Bao D Tran, Natalie L Trutalli, Theodore Garland\",\"doi\":\"10.1016/j.physbeh.2024.114752\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Early-life experiences, especially during critical periods of development and growth, can have long-lasting effects on adult phenotypes. Parents are a crucial part of the offspring early-life environment, particularly in mammals (e.g., via pregnancy), and parental behaviors (e.g., maternal exercise) can modify the early-life environment experienced by offspring. Such changes might be beneficial or detrimental, depending on how they affect offspring development and growth or interact with other key parental behaviors (e.g., nursing). We used mice from a long-term artificial selection experiment for high voluntary wheel-running behavior to determine whether maternal exercise opportunity affected (1) maternal physical activity, (2) maternal care behavior, or (3) offspring physical activity and body composition. Eighty prospective dams (40 from 4 selectively bred High Runner [HR] lines and 40 from 4 non-selected Control [CON] lines) were housed with continuous wheel access starting two weeks prior to breeding and ending 10 days postpartum, after which dams were housed without wheels until offspring weaning (21 days postpartum). An additional 100 dams (50 HR, 50 CON) were housed without wheels. Prospective dams from HR lines ran more revolutions/day (mainly by running faster) than those from CON lines when individually housed and in the days leading up to, but not after, birth. During postpartum days 1-5, HR and CON dams with wheels tended to exhibit less maternal behavior than those without (P<sub>Wheel</sub> = 0.0672). During post-partum days 6-10, HR dams with wheels continued to exhibit less maternal behavior than those without, whereas CON dams with wheels exhibited more than those without (P<sub>Linetype*Wheel</sub> = 0.0218). The proportion of dams giving birth did not differ among groups. However, CON dams with wheels were less likely to have litter death between birth and weaning than those without wheels, whereas the opposite was true for HR dams (P<sub>Linetype*Wheel</sub> = 0.0447). Both HR and CON dams with wheels had litters with a higher proportion of females at weaning than those without wheels (P<sub>Wheel</sub> = 0.0129). Maternal wheel access had few statistically significant effects on offspring, but may have resulted in developmental delays (e.g., delayed eye opening and decreased lean mass at weaning and sexual maturity). Additionally, maternal wheel access and sex may have interacted to affect wheel-running distance (P<sub>Sex*Wheel</sub> = 0.0683) and duration (P<sub>Sex*Wheel</sub> = 0.0926); female offspring from dams with wheels ran fewer revolutions per day, by running fewer minutes per day, than from dams without wheels, whereas males ran more. However, maternal exercise had no statistically significant effects on offspring food consumption (mass-adjusted), home-cage activity, open-field behavior, the reproductive characteristics of offspring, their adult body composition, nor relative organ masses; nor did maternal wheel access have statistically significant effects on grand-offspring food consumption, body composition or voluntary exercise behavior. Overall, our results provide some support for maternal exercise opportunity altering maternal care behavior. Altered maternal care could explain the observed trends in offspring survival, development, and voluntary exercise behavior. 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引用次数: 0
摘要
早期生活经历,尤其是在发育和成长的关键时期,会对成年后的表型产生长期影响。父母是后代早期生活环境的重要组成部分,特别是在哺乳动物中(如通过怀孕),父母的行为(如母性运动)可以改变后代早期生活的环境。这种变化可能是有益的,也可能是有害的,这取决于它们如何影响后代的发育和成长或与其他关键的亲代行为(如哺乳)相互作用。我们利用长期人工选择实验中的小鼠的高自愿轮跑行为来确定母体运动机会是否会影响(1)母体的体力活动、(2)母体的护理行为或(3)后代的体力活动和身体成分。80只准母鼠(40只来自4个选择性培育的高奔跑者[HR]品系,40只来自4个非选择性对照[CON]品系)从配种前两周开始至产后10天,连续使用车轮饲养,之后母鼠不使用车轮饲养,直到后代断奶(产后21天)。另外 100 只母马(50 只 HR 系,50 只 CON 系)在饲养时不带车轮。HR品系的准母马在单独饲养时和出生前几天(但不是出生后)比CON品系的准母马跑得更快(主要是跑得更快)。在产后第 1-5 天,带轮子的 HR 和 CON 母鼠的母性行为往往少于不带轮子的母鼠(PWheel = 0.0672)。在产后第 6-10 天,带轮子的 HR 母鼠的母性行为仍然少于不带轮子的母鼠,而带轮子的 CON 母鼠的母性行为则多于不带轮子的母鼠(PLinetype*Wheel = 0.0218)。各组母马的分娩比例没有差异。然而,与无车轮的母羊相比,有车轮的CON母羊在出生到断奶期间出现窝产死亡的几率较低,而HR母羊的情况则相反(PLinetype*Wheel = 0.0447)。与无车轮的母鼠相比,有车轮的 HR 母鼠和 CON 母鼠在断奶时产下的雌性比例都更高(PWheel = 0.0129)。母体使用车轮对后代的影响在统计学上并不显著,但可能会导致发育延迟(如睁眼延迟、断奶和性成熟时瘦肉率下降)。此外,母体车轮的使用和性别可能会相互作用,影响车轮运行距离(PSex*车轮 = 0.0683)和持续时间(PSex*车轮 = 0.0926);与没有车轮的母体相比,有车轮的母体的雌性后代每天运行的圈数较少,每天运行的时间较短,而雄性后代则运行得更多。然而,母体运动对子代的食物消耗量(质量调整后)、家庭笼舍活动、野外行为、子代的生殖特征、成年后的身体成分和相对器官质量没有显著的统计学影响;母体车轮的使用对子代的食物消耗量、身体成分和自愿运动行为也没有显著的统计学影响。总之,我们的研究结果为母体运动机会改变母体照料行为提供了一些支持。母性照料行为的改变可以解释观察到的后代生存、发育和自主运动行为的趋势。然而,这些影响并没有对子代或孙代的身体成分或生殖特征产生明显的长期影响。
Maternal exercise opportunity before, during, and after pregnancy alters maternal care behavior and offspring development and survival, but has few effects on offspring physical activity or body composition.
Early-life experiences, especially during critical periods of development and growth, can have long-lasting effects on adult phenotypes. Parents are a crucial part of the offspring early-life environment, particularly in mammals (e.g., via pregnancy), and parental behaviors (e.g., maternal exercise) can modify the early-life environment experienced by offspring. Such changes might be beneficial or detrimental, depending on how they affect offspring development and growth or interact with other key parental behaviors (e.g., nursing). We used mice from a long-term artificial selection experiment for high voluntary wheel-running behavior to determine whether maternal exercise opportunity affected (1) maternal physical activity, (2) maternal care behavior, or (3) offspring physical activity and body composition. Eighty prospective dams (40 from 4 selectively bred High Runner [HR] lines and 40 from 4 non-selected Control [CON] lines) were housed with continuous wheel access starting two weeks prior to breeding and ending 10 days postpartum, after which dams were housed without wheels until offspring weaning (21 days postpartum). An additional 100 dams (50 HR, 50 CON) were housed without wheels. Prospective dams from HR lines ran more revolutions/day (mainly by running faster) than those from CON lines when individually housed and in the days leading up to, but not after, birth. During postpartum days 1-5, HR and CON dams with wheels tended to exhibit less maternal behavior than those without (PWheel = 0.0672). During post-partum days 6-10, HR dams with wheels continued to exhibit less maternal behavior than those without, whereas CON dams with wheels exhibited more than those without (PLinetype*Wheel = 0.0218). The proportion of dams giving birth did not differ among groups. However, CON dams with wheels were less likely to have litter death between birth and weaning than those without wheels, whereas the opposite was true for HR dams (PLinetype*Wheel = 0.0447). Both HR and CON dams with wheels had litters with a higher proportion of females at weaning than those without wheels (PWheel = 0.0129). Maternal wheel access had few statistically significant effects on offspring, but may have resulted in developmental delays (e.g., delayed eye opening and decreased lean mass at weaning and sexual maturity). Additionally, maternal wheel access and sex may have interacted to affect wheel-running distance (PSex*Wheel = 0.0683) and duration (PSex*Wheel = 0.0926); female offspring from dams with wheels ran fewer revolutions per day, by running fewer minutes per day, than from dams without wheels, whereas males ran more. However, maternal exercise had no statistically significant effects on offspring food consumption (mass-adjusted), home-cage activity, open-field behavior, the reproductive characteristics of offspring, their adult body composition, nor relative organ masses; nor did maternal wheel access have statistically significant effects on grand-offspring food consumption, body composition or voluntary exercise behavior. Overall, our results provide some support for maternal exercise opportunity altering maternal care behavior. Altered maternal care could explain the observed trends in offspring survival, development, and voluntary exercise behavior. However, these effects did not have apparent long-lasting impacts on offspring or grand-offspring body composition or reproductive characteristics.
期刊介绍:
Physiology & Behavior is aimed at the causal physiological mechanisms of behavior and its modulation by environmental factors. The journal invites original reports in the broad area of behavioral and cognitive neuroscience, in which at least one variable is physiological and the primary emphasis and theoretical context are behavioral. The range of subjects includes behavioral neuroendocrinology, psychoneuroimmunology, learning and memory, ingestion, social behavior, and studies related to the mechanisms of psychopathology. Contemporary reviews and theoretical articles are welcomed and the Editors invite such proposals from interested authors.