Hormones and the Evolution of Complex Traits: Insights from Artificial Selection on Behavior

Garland, Theodore; Zhao, Meng; Saltzman, Wendy

doi:10.1093/icb/icw040

Cited by 66 publications

(34 citation statements)

References 196 publications

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“…VO 2 max was measured during forced exercise in a 900 ml enclosed wheel metabolic chamber as described previously [38,39]. Each trial lasted 5 minutes and each mouse was tested twice, with a rest day in between.…”

Section: Methodsmentioning

confidence: 99%

Maternal exposure to Western diet affects adult body composition and voluntary wheel running in a genotype-specific manner in mice

Hiramatsu

Kay

Thompson

et al. 2017

Physiology & Behavior

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Some human diseases, including obesity, Type II diabetes, and numerous cancers, are thought to be influenced by environments experienced in early life, including in utero. Maternal diet during the perinatal period may be especially important for adult offspring energy balance, potentially affecting both body composition and physical activity. This effect may be mediated by the genetic background of individuals, including, for example, potential “protective” mechanisms for individuals with inherently high levels of physical activity or high basal metabolic rates. To examine some of the genetic and environmental factors that influence adult activity levels, we used an ongoing selection experiment with 4 replicate lines of mice bred for high voluntary wheel running (HR) and 4 replicate, non-selected control lines (C). Dams (half HR and half C) were fed a “Western” diet (WD, high in fat and sucrose) or a standard diet (SD) from 2 weeks prior to mating until their pups could feed on solid food (14 days of age). We analyzed dam and litter characteristics from birth to weaning, and offspring mass and physical activity. One male offspring from each litter received additional metabolic and behavioral tests. Maternal WD caused pups to eat solid food significantly earlier for C litters, but not for HR litters (interaction of maternal environment and genotype). With dam mass as a covariate, mean pup mass was increased by maternal WD but litter size was unaffected. HR dams had larger litters and tended to have smaller pups than C dams. Home-cage activity of juvenile focal males was increased by maternal WD. Juvenile lean mass, fat mass, and fat percent were also increased by maternal WD, but food consumption (with body mass as a covariate) was unaffected (measured only for focal males). Behavior in an elevated plus maze, often used to indicate anxiety, was unaffected by maternal WD. Maximal aerobic capacity (VO2max) was also unaffected by maternal WD, but HR had higher VO2max than C mice. Adult lean, fat, and total body masses were significantly increased by maternal WD, with greater increase for fat than for lean mass. Overall, no aspect of adult wheel running (total distance, duration, average running speed, maximum speed) or home-cage activity was statistically affected by maternal WD. However, analysis of the 8 individual lines revealed that maternal WD significantly increased wheel running in one of the 4 HR lines. On average, all groups lost fat mass after 6 days of voluntary wheel running, but the absolute amount lost was greater for mice with maternal WD resulting in no effect of maternal WD on absolute or % body fat after wheel access. All groups gained lean and total body mass during wheel access, regardless of maternal WD or linetype. Measured after wheel access, circulating leptin, adiponectin, and corticosterone concentrations were unaffected by maternal WD and did not differ between HR and C mice. With body mass as a covariate, heart ventricle mass was increased by maternal WD in both HR and C mice, but fat pad...

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Section: Methodsmentioning

confidence: 99%

Maternal exposure to Western diet affects adult body composition and voluntary wheel running in a genotype-specific manner in mice

Hiramatsu

Kay

Thompson

et al. 2017

Physiology & Behavior

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“…The structure of the mouse cranium is similar to that of primates in that it is trilaminar and has similar attachment sites for the temporalis and masseter muscles, the primary muscles of mastication (Hallgrímsson, Willmore, Dorval, & Cooper, ). In addition, our use of the unique High Runner (HR) mouse lines, allowed us to increase the levels of voluntary exercise much above those of ordinary mice (Copes et al, ; Garland, Zhao, & Saltzman, ; Swallow, Carter, & Garland, ; Wallace & Garland, ), in an attempt to imitate the increased activity of Lieberman's pigs and armadillos (1996), although the activity in the mice here was voluntary, while that in Lieberman's study was forced.…”

Section: Introductionmentioning

confidence: 99%

Locomotor activity, growth hormones, and systemic robusticity: An investigation of cranial vault thickness in mouse lines bred for high endurance running

Copes

Schutz

Dlugsoz

et al. 2018

American J Phys Anthropol

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“…An ongoing artificial selection experiment (currently in generation 81) has produced four replicate high-runner (HR) lines while also maintaining four non-selected control (C) lines (Swallow et al 1998; Wallace and Garland, Jr. 2016; Garland, Jr. et al 2017). In the routine breeding protocol, mice are allowed access to wheels for six days as young adults, and mice in the HR lines are selected to breed based on the average number of wheel revolutions on days five and six.…”

Section: Introductionmentioning

confidence: 99%

Circulating levels of endocannabinoids respond acutely to voluntary exercise, are altered in mice selectively bred for high voluntary wheel running, and differ between the sexes

Thompson

Argueta

Garland

et al. 2017

Physiology & Behavior

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The endocannabinoid system serves many physiological roles, including in the regulation of energy balance, food reward, and voluntary locomotion. Signaling at the cannabinoid type 1 receptor has been specifically implicated in motivation for rodent voluntary exercise on wheels. We studied four replicate lines of high runner (HR) mice that have been selectively bred for 81 generations based on average number of wheel revolutions on days five and six of a six-day period of wheel access. Four additional replicate lines are bred without regard to wheel running, and serve as controls (C) for random genetic effects that may cause divergence among lines. On average, mice from HR lines voluntarily run on wheels three times more than C mice on a daily basis. We tested the general hypothesis that circulating levels of endocannabinoids (i.e., 2-arachidonoylglycerol [2-AG] and anandamide [AEA]) differ between HR and C mice in a sex-specific manner. Fifty male and 50 female mice were allowed access to wheels for six days, while another 50 males and 50 females were kept without access to wheels (half HR, half C for all groups). Blood was collected by cardiac puncture during the time of peak running on the sixth night of wheel access or no wheel access, and later analyzed for 2-AG and AEA content by ultra-performance liquid chromatography coupled to tandem mass spectrometry. We observed a significant three-way interaction among sex, linetype, and wheel access for 2-AG concentrations, with females generally having lower levels than males and wheel access lowering 2-AG levels in some but not all subgroups. The number of wheel revolutions in the minutes or hours immediately prior to sampling did not quantitatively predict plasma 2-AG levels within groups. We also observed a trend for a linetype-by-wheel access interaction for AEA levels, with wheel access lowering plasma concentrations of AEA in HR mice, while raising them in C mice. In addition, females tended to have higher AEA concentrations than males. For mice housed with wheels, the amount of running during the 30 minutes before sampling was a significant positive predictor of plasma AEA within groups, and HR mice had significantly lower levels of AEA than C mice. Our results suggest that voluntary exercise alters circulating levels of endocannabinoids, and further demonstrate that selective breeding for voluntary exercise is associated with evolutionary changes in the endocannabinoid system.

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Hormones and the Evolution of Complex Traits: Insights from Artificial Selection on Behavior

Cited by 66 publications

References 196 publications

Maternal exposure to Western diet affects adult body composition and voluntary wheel running in a genotype-specific manner in mice

Maternal exposure to Western diet affects adult body composition and voluntary wheel running in a genotype-specific manner in mice

Locomotor activity, growth hormones, and systemic robusticity: An investigation of cranial vault thickness in mouse lines bred for high endurance running

Circulating levels of endocannabinoids respond acutely to voluntary exercise, are altered in mice selectively bred for high voluntary wheel running, and differ between the sexes

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