Increased incidences of cervical ribs in deer indicate extinction risk

Abstract

Mammals as a rule have seven cervical vertebrae, a number which remains remarkably conserved. Occasional deviations of this number are usually due to the presence of cervical ribs on the seventh vertebra, indicating a homeotic transformation from a cervical rib-less vertebra into a thoracic rib-bearing vertebra. These transformations are often associated with major congenital abnormalities or pediatric cancers (pleiotropic effects) that are, at least in humans, strongly selected against. Based on data from Late Pleistocene mammoths (Mammuthus primigenius) and woolly rhinoceroses (Coelodonta antiquitatis) from the North Sea, we hypothesized that high incidences of cervical ribs in declining populations are due to inbreeding and/or adverse conditions impacting early pregnancies. In this study, we investigated the incidence of cervical ribs in an extinct Late Pleistocene megaherbivore, giant deer (Megaloceros giganteus) from Ireland and in the extant highly inbred Père David deer (Elaphurus davidianus) and in twenty other extant species. We show that the incidence of cervical ribs is exceptionally high in both the Irish giant deer and the Père David deer and much higher than in extant outbred deer. Our data support the hypothesis that inbreeding and genetic drift increase the frequencies of maladaptive alleles in populations at risk of extinction. The high incidence of cervical ribs indicates a vulnerable condition, which may have contributed to the extinction of megaherbivore species in the Late Pleistocene. We argue that cervical rib frequency may be a good proxy for extinction risk in inbred populations.

Keywords: Elaphurus davidianus; Late Pleistocene; Megaloceros giganteus; congenital abnormalities; inbreeding.

Fig. 1.

Bar plot showing the incidence of cervical ribs in large Late Pleistocene mammals. The upper three bars show the deer species analyzed in this study. The lower four bars show extinct Late Pleistocene species and their extant relatives analyzed in earlier studies (22, 23). A high incidence of cervical ribs was found in the (presumably inbred) Late Pleistocene species, significantly higher than in related extant outbred species and a similarly high incidence of cervical ribs was found in the extant inbred Père David’s deer.

Fig. 2.

Transitional cervicothoracic (C/T) vertebrae of different deer species showing incomplete and asymmetric homeotic transformations. (A) Right lateral view of an articulation facet of a large cervical rib in a C/T vertebra of an Irish giant deer (M. giganteus. specimen NMI 19:1968/313). On the left, articulation facet is missing (SI Appendix, Fig. S1A). (B) Anterior view of a transitional C7 vertebra with two small cervical ribs of Irish giant deer (specimen GE/135/1996). (C) Right lateral view of a transitional C7 vertebra with a small cervical rib of E. davidianus; specimen RMNH.MAM.1084). (D) Anterior view of a transitional C7 vertebra with a unilateral cervical rib of a roe deer (Capreolus capreolus, specimen MZB 98-0923). Red lines and arrows indicate the cervical ribs, or the articulation facets. Drawings by Erik-Jan Bosch.

Fig. 3.

Vertebral asymmetry and other abnormalities found in specimens of presumably inbred giant deer (A–D) and inbred Père David’s deer (E–H). (A) Posterior view of asymmetrical C6 of M. giganteus specimen NMI 19:1968/334. (B) Anterior view of transitional C6/C7 vertebra of M. giganteus, Dutch specimen st.124272 with asymmetric transverse foramen and reduced anterior tubercle. (C) Lateral view of partially fused 1st and 2nd thoracic vertebrae of M. giganteus specimen NMI 571:1904. (D) Ventral view of fused thoracic vertebrae and ribs of M. giganteus specimen NMING F:35123. (E) Ventral view of partially fused and irregularly shaped 5th and 6th cervical vertebrae of E. davidianus specimen RMNH.MAM.45180. (F) Dorsal view of a thoracolumbar transitional vertebra between the 12th and 13th thoracic vertebrae and the lumbar series of E. davidianus specimen MZB 94-1253. (G) Anterior view of an asymmetrical thoracolumbar transitional vertebra of E. davidianus specimen ZFMK MAM 1995-0042. (H) Ventral view of irregularly shaped and partially fused L4 and L5 of specimen MZB 94-1259 (with an abnormal lumbar count of 7).

Fig. 4.

Posterior views of C7 vertebrae in outbred (A and B) and inbred deer species (C and D), (A) an adult female of fallow deer D. dama (specimen MZB 96-0134b); (B) an adult female of red deer Cervus elaphus (specimen MZB 2010-0206), (C) an adult female of Pere David deer E. davidianus (specimen RMNH.MAM.45180), (D) an adult of Irish giant deer M. giganteus (specimen NMING F:14081). Arrows indicate left–right asymmetries in the inbred Père David’s deer (C) and Irish giant deer (D).

Fig. 5.

Molecular phylogeny of cervid species involved in our study. Bars to the right of each species indicate the number of individuals with an abnormal (red) and a normal cervical (gray) vertebral pattern. * Data for C. canadensis and C. hanglu included at the node for C. elaphus.