Skeletal developmental anomalies (SDA) are a subject of constant interest across scientific disciplines, but still mostly as isolates and curiosities. The aim of this study was to find out to what extent the occurrence of SDA reflects documented biological relationships. The skeletal remains of 34 individuals with known genealogical data were available, members of one family over four generations (19th to 20th centuries, Bohemia, Czech Republic), including some inbred individuals. The occurrence of 89 SDA was assessed on the basis of scopic morphological evaluation and X-ray and CT examinations. The degree of similarity between individuals was calculated using a "similarity coefficient" (SC). A linear model was used to test the relationship between positive values of the SC and the relatedness of biologically related individuals. Simultaneously, based on population frequencies of the evaluated anomalies, those that could be considered familial were recorded. A statistically significant relationship between morphological similarity and the biological distance between individuals was found. The greatest similarity was found among close relatives such as parents and children, siblings, or grandparents and grandchildren. The effect of increased consanguinity on the occurrence of anomalies was not confirmed, however. Seventeen SDA shared by closely related individuals were found in the sample, supporting the documented family relationships among them. Eleven of these were selected as possibly familial, but only five were statistically significant: an elongated styloid process, a cervical block vertebrae (arch, facet joints), hamate hamulus aplasia, anteater nose sign, and incomplete fusion of the S1 spinous process. There were also 28 cases of individual occurrences of 17 different SDA, without connection to the documented relationships between individuals.

Department of Anthropology and Human Genetics Faculty of Science Charles University Prague 2 Czech Republic

Department of Anthropology National Museum Prague 20 Horní Počernice Czech Republic

Department of Radiology Homolka Hospital Prague 5 Czech Republic

Department of Zoology Faculty of Science Charles University Prague 2 Czech Republic

Institute of Anatomy 1st Faculty of Medicine Charles University Prague 2 Czech Republic

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Álvarez, G. & Ceballos, F.C. (2015) Royal inbreeding and the extinction of lineages of the Habsburg dynasty. Human Heredity, 80(2), 62–68. 10.1159/000440765 PubMed DOI

Barnes, E. (1994) Developmental defects of the axial skeleton in paleopathology. Niwot, Colo: University Press of Colorado.

Barnes, E. (2012) Atlas of developmental field anomalies of the human skeleton: a paleopathology perspective, 1st edition. Hoboken: Wiley‐Blackwell.

Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57(1), 289–300. 10.1111/j.2517-6161.1995.tb02031.x DOI

Brown, K.A. (2015) Placing children in society. Using DNA to identify sex and kinship of child skeletal remains, and implications for gender and social organization. In: Coscunsu, G. (Ed.) The archaeology of childhood, interdisciplinary perspectives on an archaeological enigma. Albany: State University of New York Press, pp. 129–147.

Burnett, S.E. & Case, D.T. (2011) Bipartite medial cuneiform: new frequencies from skeletal collections and a meta‐analysis of previous cases. HOMO, 62, 109–125. 10.1016/j.jchb.2011.01.002 PubMed DOI

Cameriere, R. , Ferrante, L. , Molleson, T. & Brown, B. (2008) Frontal sinus accuracy in identification as measured by false positives in kin groups. Journal of Forensic Sciences, 53(6), 1280–1282. 10.1111/j.1556-4029.2008.00851.x PubMed DOI

Case, D.T. (2003) Who's related to whom? Skeletal kinship analysis in Medieval Danish cemeteries (Unpublished doctoral dissertation). Department of Anthropology, Arizona State University.

Case, D.T. & Burnett, S.E. (2010) Identification of tarsal coalition and frequency estimates from skeletal samples. International Journal of Osteoarchaeology, 22(6), 667–684. 10.1002/oa.1228 DOI

Case, D.T. , Jones, L.B. & Offenbecker, A.M. (2017) Skeletal kinship analysis using developmental anomalies of the foot. International Journal of Osteoarchaeology, 27(2), 192–205. 10.1002/oa.2529 DOI

Chapman, V.M. (2007) The anteater nose sign. Radiology, 245(2), 604–605. 10.1148/radiol.2452050010 PubMed DOI

Clark, R.A. , Catalan, G. , Diwan, A.D. & Kearsley, J.H. (1998) Heterogeneity in Klippel‐Feil syndrome: a new classification. Pediatric Radiology, 28(12), 967–974. 10.1007/s002470050511 PubMed DOI

Cvrček, J. , Rmoutilová, R. , Čechová, M. , Jor, T. , Velemínská, J. , Brůžek, J. et al. (2020) Biological relationships and frontal sinus similarity in skeletal remains with known genealogical data. Journal of Anatomy, 273(4), 798–809. 10.1111/joa.13246 PubMed DOI PMC

Cvrček, J. , Velemínský, P. , Dupej, J. , Vostrý, L. & Brůžek, J. (2018) Kinship and morphological similarity in the skeletal remains of individuals with known genealogical data (Bohemia, 19th to 20th centuries): a new methodological approach. American Journal of Physical Anthropology, 167(3), 541–556. 10.1002/ajpa.23683 PubMed DOI

de Leeuw, J. & Mair, P. (2009) Multidimensional scaling using majorization: SMACOF in R. Journal of Statistical Software, 31(3), 1–30.

Drozdová, E. (2006) Dietrichsteinové z Mikulova. Výsledky antropologického výzkumu vybraných příslušníků rodu (Dietrichsteins from Mikulov. The results of anthropological research of selected members of the family). In Czech. Brno: Masarykova univerzita.

Eagle, W.W. (1937) Elongated styloid process: report of two cases. Archives of Otolaryngology, 25(5), 584–587. PubMed

Falconer, D.S. & Mackay, T.F.C. (1996) Introduction into quantitative genetics, 4th edition. Harlow: Longman House.

Fisher, R.A. (1922) On the interpretation of X2 from contingency tables, and the calculation of P. Journal of the Royal Statistical Society, 85(1), 87–94.

Fornaciari, G. , Vitiello, A. , Giusiani, S. , Giuffra, V. , Fornaciari, A. & Villari, N. (2007) The Medici project first anthropological and paleopatological results of the exploration of the Medici tomb in Florence. Medicina nei Secoli, 19(2), 521–544. PubMed

Gemmerich‐Pfister, I.G.L. (1999) Création d´ une collection anthropologique de référence et application des caractères discrets dans le cas de généalogies connues (Unpublished doctoral dissertation). Département d´ Anthropologie et d´ Ecologie de l´. Université de Genève.

Giuffra, V. & Fornaciari, G. (2013) Developmental hip dysplasia in the Medici family: Giovanna from Austria (1548–1578) and her daughter Anna (1569–1584). HIP International, 23, 108–109. 10.5301/hipint.5000005 PubMed DOI

Giuffra, V. , Vitiello, A. , Giusiani, S. , Fornaciari, A. , Caramella, D. , Villari, N. et al. (2009) Rheumatoid arthritis, Klippel‐Feil syndrome, and Pott's disease in Cardinal Carlo de’ Medici (1595–1666). Clinical and Experimental Rheumatology, 27(4), 594–602. PubMed

Gunderson, C.H. , Greenspan, R.H. , Glaser, G.H. & Lubs, H.A. (1967) The Klippel‐Feil syndrome: genetic and clinical reevaluation of cervical fusion. Medicine (Baltimore), 46(6), 491–512. 10.1097/00005792-196711000-00003 PubMed DOI

Habicht, M.E. , Henneberg, M. , Öhrström, L.M. , Staub, K. & Rühli, F.J. (2015) Brief communication: body height of mummified pharaohs supports historical suggestion of sibling marriages. American Journal of Physical Anthropology, 157(3), 519–525. PubMed

Henderson, C.Y. & Cardoso, F.A. (2018) Identified skeletal collections ‐ the testing ground of anthropology?. 1st edition. Oxford: Archaeopress Publishing Ltd.

Kjaer, I. , Pallisgaard, C. & Brock‐Jacobsen, M.T. (2012) Frontal sinus dimensions can differ significantly between individuals within a monozygotic pair, indicating environmental influence on sinus size. Acta Otolaryngologica, 132, 988–994. PubMed

Lemarie, J. (1909) Malformations congénitales, familiales, hereditaires des mains et des pieds. Revue d'Orthopédie, 10, 267–273.

Leonard, M.A. (1974) The inheritance of tarsal coalition and its relationship to spastic flat foot. Journal of Bone and Joint Surgery, 56B, 520–526. 10.1302/0301-620X.56B3.520 PubMed DOI

Macaluso, P.J. & Lucena, J. (2014) Morphological variations of the anterior thoracic skeleton and their forensic significance: Radiographic findings in a Spanish autopsy sample. Forensic Science International, 241, 220.e1–220.e7. 10.1016/j.forsciint.2014.05.009 PubMed DOI

Masnicová, S. & Beňuš, R. (2003) Developmental anomalies in skeletal remains from the Great Moravia and Middle Ages cemeteries at Devín (Slovakia). International Journal of Osteoarchaeology, 13(5), 266–274.

Morrison, P.J. , Morrison, R.J. & Mckinstry, C.S. (2012) Familial ossification of the stylohyoid ligament in a three generation family – a new clinical entity displaying autosomal dominant inheritance. The British Journal of Radiology, 85, 458–459. 10.1259/bjr/21631652 PubMed DOI PMC

Offenfecker, A.M. & Case, D.T. (2012) Accessory navicular: a heritable accessory bone of the human foot. International Journal of Osteoarchaeology, 22, 158–167. 10.1002/oa.1193 DOI

Ortner, D.J. (2003) Identification of pathological conditions in human skeletal remains. Amsterdam: Academic Press.

Pachner, P. (1937) Pohlavní rozdíly na lidské pánvi (Sex differences in the human pelvis). In Czech. Praha: Česká akademie věd a umění.

Palancar, C.A. , García‐Martínez, D. , Radovčić, D. , Llidó, S. , Mata‐Escolano, F. , Bastir, M. et al. (2020) Krapina atlases suggest a high prevalence of anatomical variations in the first cervical vertebra of Neanderthals. Journal of Anatomy, 273(3), 579–586. 10.1111/joa.13215 PubMed DOI PMC

Partiot, C. , Guillon, M. , Peressinotto, D. , Castex, D. & Maureille, B. (2020) Cervical ribs in human early life: morphological variability and first identification as a morbidity criterion in a past population. Journal of Anatomy, 273(1), 119–132. 10.1111/joa.13178 PubMed DOI PMC

Paul, K.S. & Stojanowski, C.M. (2017) Comparative performance of deciduous and permanent dental morphology in detecting biological relatives. American Journal of Physical Anthropology, 164(1), 97–116. 10.1002/ajpa.23260 PubMed DOI

R Core Team . (2018) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Richer, E.J. & Pawley, B.K. (2016) Multiple unilateral tarsal coalitions in a non‐syndromic patient. Journal of Clinical Imaging, 40(2), 247–250. 10.1016/j.clinimag.2015.10.004 PubMed DOI

Ríos, L. & Cardoso, H.F.V. (2020) Comment on ‘Krapina atlases suggest a high prevalence of anatomical variations in the first cervical vertebra of Neanderthals’. Journal of Anatomy, 237(6), 1185–1188. 10.1111/joa.13268 PubMed DOI PMC

Ríos, L. , Kivell, T.L. , Lalueza‐Fox, C. , Estalrrich, A. , García‐Tabernero, A. , Huguet, R. et al. (2019) Skeletal anomalies in the neandertal family of El Sidrón (Spain) support a role of inbreeding in neandertal extinction. Scientific Reports, 9(1), 1697. 10.1038/s41598-019-38571-1 PubMed DOI PMC

Ríos, L. , Rosas, A. , Estalrrich, A. , García‐Tabernero, A. , Bastir, M. , Huguet, R. et al. (2015) Possible further evidence of low genetic diversity in the El Sidrón (Asturias, Spain) Neandertal group: congenital clefts of the atlas. PLoS One, 10(9), e0136550. 10.1371/journal.pone.0136550 PubMed DOI PMC

Rösing, F.W. (1986). Group report – Kinship analysis. In Herrmann B. (Ed.), Innovative Trends in der Prähistorischen Anthropologie, vol. 7. Berlin: Berliner Gessellschaft für Anthropologie, Ethnologie und Urgeschichte, pp. 95–98.

Seeger, L.L. , Bassett, L.W. & Gold, R.H. (1988) Case report 464: bilateral congenital absence of the hook of the hamate. Skeletal Radiology, 17(1), 85–86. 10.1007/BF00361463 PubMed DOI

Shepherd, F.J. (1893) Symmetrical depressions on the exterior surface of the parietal bones (with notes of three cases). Journal of Anatomy and Physiology, 27(4), 501–504. PubMed PMC

Siegel, S. (1956) Non‐parametric statistics for the behavioral sciences. New York: McGraw‐Hill, pp. 75–83.

Stloukal, M. (2013) Kosterní pozůstatky z krypty kostela Panny Marie Vítězné v Praze (Church remains of the crypt of the Church of Our Lady Victorious in Prague. In Czech. Prague: Department of Anthropology, National museum; (Unpublished).

Stojanowski, C.M. & Schillaci, M.A. (2006) Phenotypic approaches for understanding patterns of intracemetery biological variation. Yearbook of Physical Anthropology, 49, 49–88. 10.1002/ajpa.20517 PubMed DOI

Symmers, W.S.C. (1895) A skull with enormous parietal foramina. Journal of Anatomy and Physiology, 29(2), 329–330. PubMed PMC

Tayebi, N. , Yazdani, K. & Naghshin, N. (2010) The prevalence of congenital malformations and its correlation with consanguineous marriages. Oman Medical Journal, 25(1), 37–40. 10.5001/omj.2010.9 PubMed DOI PMC

Thomsen, M.N. , Schneider, U. , Weber, M. , Johannisson, R. & Niethard, F.U. (1997) Scoliosis and congenital anomalies associated with Klippel‐Feil syndrome types I‐III. Spine, 22(4), 396–401. 10.1097/00007632-199702150-00008 PubMed DOI

Thurzo, M. & Beňuš, R. (2003) Palatine George Thurzo and his family: skeletal pathologies. Slovenská Antropológia, 6(1), 155–162.

Titelbaum, A.R. (2020) Developmental anomalies and South American paleopathology: A comparison of block vertebrae and co‐occurring axial anomalies among three skeletal samples from the El Brujo archaeological complex of northern coastal Peru. International Journal of Paleopathology, 29, 76–93. 10.1016/j.ijpp.2019.07.001 PubMed DOI

Tracy, M.R. , Dormans, J.P. & Kusumi, K. (2004) Klippel‐Feil syndrome: clinical features and current understanding of etiology. Clinical Orthopaedics and Related Research, 424, 183–190. 10.1097/01.blo.0000130267.49895.20 PubMed DOI

Trinkaus, E. (2018) An abundance of developmental anomalies and abnormalities in Pleistocene people. Proceedings of the National Academy of Sciences, 115(47), 11941–11946. 10.1073/pnas.1814989115 PubMed DOI PMC

Tur, S.S. , Svyatko, S.V. & Rykun, M.R. (2019) Transverse basilar cleft: Two more probable familial cases in an archaeological context. International Journal of Osteoarchaeology, 29, 144–148. 10.1002/oa.2692 DOI

VanRaden, P.M. (1992) Accounting for inbreeding and crossbreeding in genetic evaluation of large populations. Journal of Dairy Science, 75(11), 3136–3144. 10.3168/jds.S0022-0302(92)78077-1 DOI

Velemínský, P. (2000) Mikulčice‐Kostelisko: některé kostní projevy nespecifické zátěže a možnosti stanovení pokrevně příbuzenských vztahů na základě morfologické podobnosti (Mikulčice‐Kostelisko. Some skeletal manifestations of non‐specific stress and the possibility to determine consanguineous relationships according to the morphological similarity. In Czech. Praha: Unpublished doctoral dissertation, Department of Anthropology and Human Genetics, Faculty of Science, Charles University, pp. 500.

Velemínský, P. & Dobisíková, M. (2005) Morphological likeness of the skeletal remains in a Central European family from 17th to 19th century. HOMO, 56(2), 173–196. 10.1016/j.jchb.2005.05.005 PubMed DOI

Verna, E. , Piercecchi‐Marti, M.D. , Chaumoitre, K. & Adalian, P. (2015) Relevance of discrete traits in forensic anthropology: from the first cervical vertebra to the pelvic girdle. Forensic Science International, 253, 134.e1–134.e7. 10.1016/j.forsciint.2015.05.005 PubMed DOI

Verna, E. , Piercecchi‐Marti, M.D. , Chaumoitre, K. , Bartoli, C. , Leonetti, G. & Adalian, P. (2013) Discrete traits of the sternum and ribs: a useful contribution to identification in forensic anthropology and medicine. Journal of Forensic Sciences, 58(3), 571–577. 10.1111/1556-4029.12111 PubMed DOI

Vlček, E. (2000) Čeští králové I. Atlas kosterních pozůstatků českých králů přemyslovské a lucemburské dynastie s podrobným komentářem a historickými poznámkami (Czech kings I. Atlas of skeletal remains of Czech kings of the Premyslid and Luxembourg dynasties with detailed commentary and historical notes. In Czech. Praha: Vesmír.

The influence of biological relatedness on sexual dimorphism and sex classification based on external morphology of the frontal bone