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. 2018 Jun 20;13(6):e0198511.
doi: 10.1371/journal.pone.0198511. eCollection 2018.

Limb bone histology records birth in mammals

Carmen Nacarino-Meneses  1 , Meike Köhler  1   2
Affiliations

Limb bone histology records birth in mammals

Carmen Nacarino-Meneses et al. PLoS One. .

Abstract

The annual cyclicality of cortical bone growth marks (BGMs) allows reconstruction of some important life history traits, such as longevity, growth rate or age at maturity. Little attention has been paid, however, to non-cyclical BGMs, though some record key life history events such as hatching (egg-laying vertebrates), metamorphosis (amphibians), or weaning (suggested for Microcebus and the hedgehog). Here, we investigate the relationship between non-cyclical BGMs and a stressful biological event in mammals: the moment of birth. In the present study, we histologically examine ontogenetic series of femora, tibiae and metapodia in several extant representatives of the genus Equus (E. hemionus, E. quagga and E. grevyi). Our analysis reveals the presence of a non-cyclical growth mark that is deposited around the moment of birth, analogous to the neonatal line described for teeth. We therefore refer to it as neonatal line. The presence of this feature within the bone cross-section agrees with a period of growth arrest in newborn foals regulated by the endocrine system. The neonatal line is accompanied by modifications in bone tissue type and vascularization, and has been identified in all bones studied and at different ontogenetic ages. Our discovery of a non-cyclical BGM related to the moment of birth in mammals is an important step towards the histological reconstruction of life histories in extant and fossil equids.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Presence and absence of the neonatal line (NL) in the limb bones of extant Equus.
From up to down: Femur–IPS92343 (E. quagga), IPS101798 (E. quagga), IPS101800 (E. quagga), IPS101804 (E. grevyi), IPS83876 (E. hemionus); Tibia–IPS83152 (E. hemionus), IPS101798 (E. quagga), IPS101801 (E. quagga), IPS101804 (E. grevyi), IPS84963 (E. grevyi); Metapodials–IPS83152 (Mc, E. hemionus), IPS84964 (Mt, E. grevyi), IPS83150 (Mt, E. hemionus), IPS83155 (Mc, E. hemionus), IPS83876 (Mt, E. grevyi). Mc = metacarpus; Mt = metatarsus. White arrows indicate the NL. Scale bars = 1 mm.
Fig 2
Fig 2. Neonatal line (NL) identified in the femoral and tibial cortex of a 1-month-old Grevy’s zebra.
(A) Femoral cortex of IPS101802. (B) Detail of the NL identified in the femur of IPS101802. (C) Tibial cortex of IPS101802. (D) Detail of the NL identified in the tibia of IPS101802. White arrows indicate NL. White dashed rectangles indicate areas of image magnification. White scale bars = 1mm; black scale bars = 200 μm.
Fig 3
Fig 3. Superimposition of foal’s and juvenile’s femur of E. grevyi.
Figure shows a high resorption of the medullary cavity in the juvenile (IPS101804) femur that has erased the neonatal line (NL) identified in the foal (IPS101802) (red line). A = anterior, L = lateral.
Fig 4
Fig 4. Correspondence between the perimeter of perinatal bones and the neonatal line (NL).
Figure shows a match between the perimeter of the perinatal Asiatic wild ass (dark images, IPS83152) and the NL (red dashed line) identified in different limb bones and ontogenetic stages of E. hemionus (light images). (A) Superimposition of newborn’s and yearling’s (IPS83149) femora. (B) Superimposition of newborn’s and foal’s (IPS83154) tibiae. (C) Superimposition of newborn’s and juvenile’s (IPS83155) metatarsi. (D) Superimposition of newborn’s and adult’s (IPS83876) metacarpi. Scale bars = 5 mm.
Fig 5
Fig 5. Histological changes associated to the presence of the neonatal line in extant Equus.
(A) Femoral cortex of E. hemionus IPS83153. (B) Femoral cortex of E. quagga IPS92345. (C) Femoral cortex of E. grevyi IPS84964. (D) Tibial cortex of E. hemionus IPS83154. (E) Tibial cortex of E. quagga IPS101801. (F) Tibial cortex of E. grevyi IPS101804. (G) Metacarpal cortex of E. hemionus IPS83150. (H) Metatarsal cortex of E. quagga IPS104356. (I) Metatarsal cortex of E. grevyi IPS84964. White dotted line indicates the neonatal line. AVC = area of the longitudinal VCs; FLC = fibrolamellar complex; LB = laminar bone; PFB = parallel-fibered bone. Scale bars = 1 mm.
Fig 6
Fig 6. Area of the vascular canals (VCs) at both sides of the neonatal line (NL).
(A) Femora. (B) Tibiae. (C) Metacarpi. (D) Metatarsi. White boxplot = Area of the VCs located before the deposition of the NL; grey boxplot = Area of the VCs located after the deposition of the NL.
Fig 7
Fig 7. Longitudinal vascular canals (VCs) formed after and before the neonatal line (NL) (yellow dotted line).
(A) VCs formed after deposition of the NL in the femur of E. quagga IPS92345. (B) VCs formed after deposition of the NL in the tibia of E. hemionus IPS83153. (C) VCs formed after deposition of the NL in the metacarpus of E. hemionus IPS83150. (D) VCs formed after deposition of the NL in the metatarsus of E. grevyi IPS84964. (E) VCs formed before deposition of the NL in the femur of E. quagga IPS92345. (F) VCs formed before deposition of the NL in the tibia of E. hemionus IPS83153. (G) VCs formed before deposition of the NL in the metacarpus of E. hemionus IPS83150. (H) VCs formed before deposition of the NL in the metatarsus of E. grevyi IPS84964. Scale bars = 200 μm.
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Grants and funding

This work has received the support from the Spanish Ministry of Economy and Competitiveness (CGL-2015-63777, PI: M.K.) and the Government of Catalonia (2014-SGR-1207, PI: M.K.; CERCA Programme, M.K.). C.N.-M. is supported with a FPI grant from the Spanish Ministry of Economy and Competitiveness (BES-2013-066335). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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