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Femoral bone structure and mechanics at the edge and core of an expanding population of the invasive frog Xenopus laevis.
Dumont M
,
Herrel A
,
Courant J
,
Padilla P
,
Shahar R
,
Milgram J
.
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Understanding how living tissues respond to changes in their mechanical environment is a key question in evolutionary biology. Invasive species provide an ideal model for this as they are often transplanted between environments that differ drastically in their ecological and environmental context. Spatial sorting, the name given to the phenomenon driving differences between individuals at the core and edge of an expanding range, has been demonstrated to impact the morphology and physiology of Xenopus laevis from the invasive French population. Here, we combined a structural analysis using micro-CT scanning and a functional analysis by testing the mechanical properties of the femur to test whether the increased dispersal at the range edge drives differences in bone morphology and function. Our results show significant differences in the inner structure of the femur as well as bone material properties, with frogs from the centre of the range having more robust and resistant bones. This is suggestive of an energy allocation trade-off between locomotion and investment in bone formation, or alternatively, may point to selection for fast locomotion at the range edge. Overall, our results provide insights on the growth of the long bones and the formation of trabecular bone in frogs.
Fig. 1. Reconstructions of selected representative femurs from individual Xenopus laevis of increasing size. (A–D) female core; (E–G) male core; (H–K) female edge; (L–N) male edge). Corresponding cross sections show details of cortical bone at three locations in each bone indicated by the white horizontal stripes. Female core: (A) C15 (femora length, 25 mm), (B) C24 (32.42 mm), (C) C26 (36.34 mm), (D) C8 (42.22 mm); male core: (E) C44 (25.58 mm), (F) C29 (26.24 mm), (G) C38 (33.3 mm); female edge: (H) E6 (28.55 mm), (I) E7 (31.7 mm), (J) E15 (33.47 mm), (K) E16 (43.27 mm); male edge: (L) E25 (24.69 mm), (M) E28 (28.8 mm), (N) E14 (33.33 mm). Scale bars: 1 mm (white), corresponding to the images of the bones; 2 mm (black), corresponding to the bone cross-sections.
Fig. 2.Comparison of cortical bone parameters as a function of femoral length. (A) Cross-sectional bone area (CSAbone; mm2), (B) Cortical thickness (Lcortex; mm), (C) Mean polar second moment of area (Ipolar; mm4), (D) bone mineral density (BMD; g cm−3) between the edge (square) and core (circle) populations for males (black) and females (white). Trend lines have been added to the graphs.
Fig. 3.Illustration of the trabecular bone present in a longitudinal cut of X. laevis femora epiphyses. The proximal (left) and distal (right) epiphyses of selected femora for the core population (A–H) and edge (I–P) for each sex, ranked by increasing femur length (from left to right). Female core: (A) C15 (femur length, 26.82 mm), (B) C24 (32.42 mm), (C) C23 (33.9 mm), (D) C8 (42.22 mm); male core: (E) C44 (25.58 mm), (F) C29 (26.24 mm), (G) C11 (32 mm), (H) C38 (33.3 mm). Female edge: (I) E6 (28.55 mm), (J) E7 (31.7 mm), (K) E15 (33.47 mm), (L) E16 (43.27 mm); male edge: (M) E25 (24.69 mm), (N) E17 (27.39 mm), (O) E28 (28.8 mm), (P) E14 (33.33 mm).
Fig. 4.Scatterplot of bone volume relative to total tissue volume against femur length for the distal epiphyses of X. laevis femora. Bone volume fraction (Vbone/Vtissue, in %) in edge individuals is represented by squares and core individuals by circles. Males are indicated in black and females in white. Raw data can be found in Table S6.
Fig. 5.Measurement of strain and stress of X. laevis femora in a three-point bending test. (A) Three-point bending test of a femur harvested from a male (left: individual C44; femur length of 25.6 mm) and female (right: individual C26; femur length of 36.34 mm). (B) Graph of the strain–stress curves for four representative femora: males are indicated in grey, females in black. The dashed lines represent larger individuals and the solid lines smaller ones. Arrows indicate fracture of the sample. Femur lengths are indicated below the individual number. C, core; E, edge. Raw data can be found in Table 3.
Fig. S1. Bone volume relative to total tissue volume in the proximalepiphysis of Xenopus laevis in function of femur length. Black
symbols represent males, white symbols represent females. Squares represent edge individuals, circles represent core individuals.
Fig. S2. Trabecular thickness in the proximal (A) and distal (B) epiphyses of Xenopus laevis in function of femur length. Black
symbols represent males, white symbols represent females. Squares represent edge individuals, circles represent core individuals.
