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

   https://doi.org/10.1002/ajpa.23446  

   Copes, L. E. ; Schutz, H. ; Dlugsoz, E. M. ; Judex, S. ; Garland, Jr, T. ( February 2018 , American Journal of Physical Anthropology)

   To use a mouse model to investigate the relationships among the components of the systemic robusticity hypothesis (SRH): voluntary exercise on wheels, spontaneous physical activity (SPA) in cages, growth hormones, and skeletal robusticity, especially cranial vault thickness (CVT).

   Fifty female mice from lines artificially selected for high running (HR) and 50 from nonselected control (C) lines were housed in cages with (Active) or without wheels (Sedentary). Wheel running and SPA were monitored daily. The experiment began at 24–27 days of age and lasted 12 weeks. Food consumption was measured weekly. Mice were skeletonized and their interparietal, parietal, humerus, and femur were µCT scanned. Mean total thickness of the parietal and interparietal bones was determined, along with thickness of the cortical and diploe layers individually. Geometric cross‐sectional indicators of strength were calculated for the long bones. Blood samples were assayed for IGF‐1 and IGFBP‐3.

   Physical activity differed significantly among groups, based both on linetype (C vs. HR) and activity (A vs. S). However, contrary to our predictions, the ratio of IGF‐1 to IGFBP‐3 was higher in C mice than in HR mice. Neither CVT nor postcranial robusticity was affected by linetype or activity, nor were most measures of CVT and postcranial robusticity significantly associated with one another.

   Our results fail to provide support for the systemic robusticity hypothesis, suggesting it is important to rethink the long‐standing theory that increased CVT inHomo erectusreflects increased physical activity compared other hominin species.

    

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2. Effects of long‐term voluntary wheel running and selective breeding for wheel running on femoral nutrient canals

   https://doi.org/10.1111/joa.14021  

   Tan, Brandon B ; Schwartz, Nicole E ; Copes, Lynn E ; Garland, Theodore ( June 2024 , Journal of Anatomy)

   The nutrient artery provides ~50%–70% of the total blood volume to long bones in mammals. Studying the functional characteristics of this artery in vivo can be difficult and expensive, so most researchers have measured the nutrient foramen, an opening on the outer surface of the bone that served as the entry point for the nutrient artery during development and bone ossification. Others have measured the nutrient canal (i.e., the passage which the nutrient artery once occupied), given that the external dimensions of the foramen do not necessarily remain uniform from the periosteal surface to the medullary cavity. The nutrient canal, as an indicator of blood flow to long bones, has been proposed to provide a link to studying organismal activity (e.g., locomotor behavior) from skeletal morphology. However, although external loading from movement and activity causes skeletal remodeling, it is unclear whether it affects the size or configuration of nutrient canals. To investigate whether nutrient canals can exhibit phenotypic plasticity in response to physical activity, we studied a mouse model in which four replicate high runner (HR) lines have been selectively bred for high voluntary wheel‐running behavior. The selection criterion is the average number of wheel revolutions on days 5 and 6 of a 6‐day period of wheel access as young adults (~6–8 weeks old). An additional four lines are bred without selection to serve as controls (C). For this study, 100 female mice (half HR, half C) from generation 57 were split into an active group housed with wheels and a sedentary group housed without wheels for 12 weeks starting at ~24 days of age. Femurs were collected, soft tissues were removed, and femora were micro‐computed tomography scanned at a resolution of 12 μm. We then imported these scans into AMIRA and created 3D models of femoral nutrient canals. We tested for evolved differences in various nutrient canal traits between HR and C mice, plastic changes resulting from chronic exercise, and the selection history‐by‐exercise interaction. We found few differences between the nutrient canals of HR versus C mice, or between the active and sedentary groups. We did find an interaction between selection history and voluntary exercise for the total number of nutrient canals per femur, in which wheel access increased the number of canals in C mice but decreased it in HR mice. Our results do not match those from an earlier study, conducted at generation 11, which was prior to the HR lines reaching selection limits for wheel running. The previous study found that mice from the HR lines had significantly larger total canal cross‐sectional areas compared to those from C lines. However, this discrepancy is consistent with studies of other skeletal traits, which have found differences between HR and C mice to be somewhat inconsistent across generations, including the loss of some apparent adaptations with continued selective breeding after reaching a selection limit for wheel‐running behavior.

    

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3. Low temperature decreases bone mass in mice: Implications for humans

   https://doi.org/10.1002/ajpa.23684  

   Robbins, Amy ; Tom, Christina A. T. M. B. ; Cosman, Miranda N. ; Moursi, Cleo ; Shipp, Lillian ; Spencer, Taylor M. ; Brash, Timothy ; Devlin, Maureen J. ( September 2018 , American Journal of Physical Anthropology)

   Humans exhibit significant ecogeographic variation in bone size and shape. However, it is unclear how significantly environmental temperature influences cortical and trabecular bone, making it difficult to recognize adaptation versus acclimatization in past populations. There is some evidence that cold‐induced bone loss results from sympathetic nervous system activation and can be reduced by nonshivering thermogenesis (NST) via uncoupling protein (UCP1) in brown adipose tissue (BAT). Here we test two hypotheses: (1) low temperature induces impaired cortical and trabecular bone acquisition and (2) UCP1, a marker of NST in BAT, increases in proportion to degree of low‐temperature exposure.

   We housed wildtype C57BL/6J male mice in pairs at 26 °C (thermoneutrality), 22 °C (standard), and 20 °C (cool) from 3 weeks to 6 or 12 weeks of age with access to food and water ad libitum (N= 8/group).

   Cool housed mice ate more but had lower body fat at 20 °C versus 26 °C. Mice at 20 °C had markedly lower distal femur trabecular bone volume fraction, thickness, and connectivity density and lower midshaft femur cortical bone area fraction versus mice at 26 °C (p< .05 for all). UCP1 expression in BAT was inversely related to temperature.

   These results support the hypothesis that low temperature was detrimental to bone mass acquisition. Nonshivering thermogenesis in brown adipose tissue increased in proportion to low‐temperature exposure but was insufficient to prevent bone loss. These data show that chronic exposure to low temperature impairs bone architecture, suggesting climate may contribute to phenotypic variation in humans and other hominins.

    

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4. Evolution of hindlimb bone dimensions and muscle masses in house mice selectively bred for high voluntary wheel-running behavior

   https://doi.org/10.1002/jmor.20809  

   Castro, Alberto A. ; Garland, Theodore ( March 2018 , Journal of Morphology)

   We have used selective breeding with house mice to study coadaptation of morphology and physiology with the evolution of high daily levels of voluntary exercise. Here, we compared hindlimb bones and muscle masses from the 11th generation of four replicate High Runner (HR) lines of house mice bred for high levels of voluntary wheel running with four non‐selected control (C) lines. Mass, length, diameter, and depth of the femur, tibia‐fibula, and metatarsal bones, as well as masses of gastrocnemius and quadriceps muscles, were compared by analysis of covariance with body mass or body length as the covariate. Mice from HR lines had relatively wider distal femora and deeper proximal tibiae, suggesting larger knee surface areas, and larger femoral heads. Sex differences in bone dimensions were also evident, with males having thicker and shorter hindlimb bones when compared with females. Several interactions between sex, linetype, and/or body mass were observed, and analyses split by sex revealed several cases of sex‐specific responses to selection. A subset of the HR mice in two of the four HR lines expressed the mini‐muscle phenotype, characterized mainly by an ∼50% reduction in hindlimb muscle mass, caused by a Mendelian recessive mutation, and known to have been under positive selection in the HR lines. Mini‐muscle individuals had elongated distal elements, lighter and thinner hindlimb bones, altered 3rd trochanter muscle insertion positions, and thicker tibia‐fibula distal widths. Finally, several differences in levels of directional or fluctuating asymmetry in bone dimensions were observed between HR and C, mini‐ and normal‐muscled mice, and the sexes. This study demonstrates that skeletal dimensions and muscle masses can evolve rapidly in response to directional selection on locomotor behavior. 

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5. Ontogenetic biomechanics of tufted ( Sapajus ) and untufted ( Cebus ) capuchin mandibles

   https://doi.org/10.1002/ajpa.25006  

   Polvadore, Taylor_A ; Yoakum, Caitlin_B ; Taylor, Parker_M ; Holmes, Megan_A ; Laird, Myra_F ; Chalk‐Wilayto, Janine ; Kanno, Cláudia_Misue ; de_Oliveira, José_Américo ; Terhune, Claire_E ( July 2024 , American Journal of Biological Anthropology)

   Cortical bone geometry is commonly used to investigate biomechanical properties of primate mandibles. However, the ontogeny of these properties is less understood. Here we investigate changes in cortical bone cross‐sectional properties throughout capuchin ontogeny and compare captive versus wild, semi‐provisioned groups. Tufted capuchins (Sapajusspp.) are known to consume relatively hard/tough foods, while untufted capuchins (Cebusspp.) exploit less mechanically challenging foods. Previous research indicates dietary differences are present early in development and adultSapajusmandibles can resist higher bending/shear/torsional loads.

   This study utilized microCT scans of 22Cebusand 45Sapajusfrom early infancy to adulthood from three sample populations: one captiveCebus, one captiveSapajus, and one semi‐provisioned, free‐rangingSapajus. Mandibular cross‐sectional properties were calculated at the symphysis, P₃, and M₁. If the tooth had not erupted, its position within the crypt was used. A series of one‐way ANOVAs were performed to assess differences between and within the sample populations.

   Mandible robusticity increases across ontogeny for all three sample populations.Sapajuswere better able to withstand bending and torsional loading even early in ontogeny, but no difference in shear resistance was found. Semi‐provisioned, free‐rangingSapajustend to show increased abilities to resist bending and torsional loading but not shear loading compared to captiveSapajus.

   This study helps advance our understanding of the primate masticatory system development and opens the door for further studies into adaptive plasticity in shaping the masticatory apparatus of capuchins and differences in captive versus free‐ranging sample populations.

    

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