1. Introduction Results
[1] Schlecht at al., CORR 2015. [2] Jepsen et al., CORR 2015
[3] Grinnell, Mammalian Species 1904.
Acknowledgments References
Secular changes in bone morphology and sexual dimorphism
of white-footed mice over 85 years
1Richard W Nakkula Jr., 1Lauren M Smith, 2Eva C Thompson, 1Bonnie T Nolan, 1Erin MR Bigelow,
2Katelyn R Vedolich, 1Melissa A Ramcharan, 2Cody W Thompson, 1Karl J Jepsen
1Department of Orthopaedic Surgery, University of Michigan, Ann Arbor, MI USA
2Department of Ecology & Evolutionary Biology and Museum of Zoology, University of Michigan, Ann Arbor, MI, USA
To determine if there has been a change in sexual dimorphism
(body size, bone shape, and/or strength) over the last 85 years in
wild-collected mice.
Methods
Male and female Peromyscus leucopus (white-footed mice)
§ Historical collection (circa 1920; n=32/sex), obtained from the University of Michigan
Museum of Zoology.
§ Modern collection (circa 2014-15; n=32 male, 32 female)
§ Mice were collected using Sherman live traps in fields in Washtenaw County, MI,
following a protocol approved by the University of Michigan’s Institutional Animal Care
and Use Committee
§ Specimens were prepared as standard vouchers for the Museum of Zoology.
Anthropometric traits (Fig.3):
Total body length, tail length, hind foot length, ear length, body mass (BM), femur length
(F.Le), humerus length (Hu.Le), hip length, zygomatic breadth, basal length, basilar
length, and cranial length as described[3]. AP and ML widths of the femur and humerus
were also taken.
Traits from nanoCT (8 µm voxel size):
Cortical area (Ct.Ar), total area (Tt.Ar), marrow area
(Ma.Ar), and tissue mineral density (TMD).
Calculated traits:
Robustness (Tt.Ar/F.Le) and bone strength index
(IAP x TMD, BSI)
Statistical Analysis:
All trait arrays were assessed for differences between sex,
era, and sex by era using two-way ANOVAs in GraphPad
Prism after linear regression method adjustments for body
mass within sex.
The authors wish to thank John Russell, David Read, Ed Mamarow, and Mark Levine for access to their
properties. We also thank Phil Myers for the tremendous guidance and knowledge of the white-footed mouse.
Conclusions
Sexual dimorphism underlies musculoskeletal injury and disease risk.
§ In humans, men have stronger bones for body size than women[1,2].
§ In mice, however, this phenomenon is not the same. Female mice have
stronger bones for size with little to no difference in bone morphology[2].
§ This phenomenon questions the usefulness of inbred mouse strains
when investigating mechanisms of sexual dimorphism as it contributes to
musculoskeletal injury and disease in humans.
Figure 3. Diagram of anthropometric measurements as described[3]. Performed using
digital calipers. Resolution of 0.01mm.
Bone diagrams adapted from http://stkctr.biol.sc.edu/wild-stock/p_calif.html.
Purpose
Figure 1. Sexual dimorphic differences in bone strength between humans and mice. Black
and white males have stronger bones than their female counterparts by 19% and 27%,
respectively, while female mice have 10% stronger bones than their male counterparts[2].
Figure 2. Peromyscus leucopus
in natural Michigan habitat.
Courtesy of Phil Myers
Figure 4. Differences in body mass, morphological features unadjusted (body mass and total body length) and body mass adjusted (all other traits) mean ± SD.
MaleFemale
Total body length (mm)
p = 0.66
p < 0.0001
p = 0.83
Sex:
Era:
Interaction:
Sex:
Era:
Interaction:
p = 0.45
p = 0.62
p = 0.80
p = 0.74
p < 0.0001
p = 0.61
Sex:
Era:
Interaction:
Total Area (mm2)
Cortical Area (mm2)
Historical Modern
0.0
0.2
0.4
0.6
0.8
0.4
0.6
0.8
1.0
1.2
1.4
Hip length (mm)
Historical Modern
p = 0.07
p = 0.73
p = 0.48
Sex:
Era:
Interaction:
Body mass (g)
p = 0.06
p = 0.03
p = 0.11
Sex:
Era:
Interaction:
Sex:
Era:
Interaction:
p = 0.35
p = 0.24
p = 0.02
Historical Modern
BSI (mm4 mgHA/cc)
Historical Modern
p = 0.64
p = 0.01
p = 0.68
Sex:
Era:
Interaction:
0
40
80
120
160
200
240
Robustness (mm)
p = 0.43
p < 0.0001
p = 0.97
Sex:
Era:
Interaction:
0.03
0.04
0.05
0.06
0.07
0.08
0.09
Femur length (mm)
Body size Post-cranial morphology Cranial morphology
Measurements:
Table 1. Summary of effects. Direction of trait change was confirmed with Student’s t-test.
§ This analysis has identified sex specific differences in body size and bone
morphology over the past 85 years.
§ A reversal of sexual dimorphism has occurred for body size: wild-caught female
white-footed mice are now larger compared to wild-caught males.
§ Femur morphology has changed significantly over the past century, modern
wild-caught deer mice have wider femora than historical populations.
§ After adjusting for body mass differences, there are no differences in estimated
bone strength between male and female white-footed mice. This is similar to
that seen for inbred mouse populations.
Future work:
Focus on identifying environmental and/or genetic factors that contribute to
these changes in sexual dimorphism.
Effect Males Females Traits
Sex specific
Body mass
Femur, basal, basilar, and
cranial lengths.
Zygomatic breadth
Not sex
specific
Robustness, Tt.Ar, and BSI
Total body length
No change Ct.Ar and hip length
Zygomatic breadth (mm)
Historical Modern
p = 0.006
p = 0.002
p = 0.01
Sex:
Era:
Interaction:
Sex:
Era:
Interaction:
p = 0.53
p = 0.03
p = 0.02
Basal length (mm)
Historical Modern
Basilar length (mm)
Cranial length (mm)
p = 0.78
p = 0.003
p = 0.01
Sex:
Era:
Interaction:
p = 0.37
p = 0.0005
p = 0.007
Sex:
Era:
Interaction:
100
120
140
160
180
200
10
11
12
13
14
15
17
19
21
23
25
12
14
16
18
5
10
15
20
25
16
17
18
19
20
21
22
18
20
22
24
26
28
11
13
15
17
19