Homology, homoplasy and cusp variability at the enamel–dentine junction of hominoid molars

Abstract

Evolutionary studies of mammalian teeth have generally concentrated on the adaptive and functional significance of dental features, whereas the role of development on phenotypic generation and as a source of variation has received comparatively little attention. The present study combines an evolutionary biological framework with state-of-the-art imaging techniques to examine the developmental basis of variation of accessory cusps. Scholars have long used the position and relatedness of cusps to other crown structures as a criterion for differentiating between developmentally homologous and homoplastic features, which can be evaluated with greater accuracy at the enamel-dentine junction (EDJ). Following this approach, we collected digital models of the EDJ and outer enamel surface of more than 1000 hominoid teeth to examine whether cusp 5 of the upper molars (UM C5) and cusps 6 and 7 of the lower molars (LM C6 and LM C7) were associated each with a common developmental origin across species. Results revealed that each of these cusps can develop in a variety of ways, in association with different dental tissues (i.e. oral epithelium, enamel matrix) and dental structures (i.e. from different cusps, crests and cingula). Both within and between species variability in cusp origin was highest in UM C5, followed by LM C7, and finally LM C6. The lack of any species-specific patterns suggests that accessory cusps in hominoids are developmentally homoplastic and that they may not be useful for identifying phylogenetic homology. An important and unanticipated finding of this study was the identification of a new taxonomically informative feature at the EDJ of the upper molars, namely the post-paracone tubercle (PPT). We found that the PPT was nearly ubiquitous in H. neanderthalensis and the small sample of Middle Pleistocene African and European humans (MPAE) examined, differing significantly from the low frequencies observed in all other hominoids, including Pleistocene and recent H. sapiens. We emphasize the utility of the EDJ for human evolutionary studies and demonstrate how features that look similar at the external surface may be the product of different developmental patterns. This study also highlights the importance of incorporating both developmental and morphological data into evolutionary studies in order to gain a better understanding of the evolutionary significance of dental and skeletal features.

Evo-devo models of tooth development and the origin of hominoid molar diversity

“…Hence, bunodont molars should exhibit both lower cusp height differentials and higher frequencies of accessory cusps ( 8 , 9 , 13 , 14 ). Although the bunodont molars of Paranthropus and Australopithecus have higher frequencies of accessory cusps relative to later and higher-cusped hominin molars, high-cusped Gorilla molars do not have a distinctly high frequency of extra cusps ( 1 , 21 ). Given the limited differential variability for selection to act upon, it is believed that going from high-cusped to a bunodont configuration is easier than the reverse ( 15 ).…”

A distinguishing feature of Pongo upper molars and its implications for the taxonomic identification of isolated hominid teeth from the Pleistocene of Asia

“…We made no attempt to record the sex of the specimens given that our sample mainly comprises isolated teeth and that the sex is unknown for most fossils. However, previous studies have found that discrete traits do not significantly vary between sexes in great apes and hominins (Ortiz et al, ; Pilbrow, ; Uchida, ). Although some specimens in our sample exhibit moderate wear (up to Molnar's, , stage 5), this did not affect the accurate assessment of protoconule expression at the EDJ.…”

“…Specifically, we quantified patterns of intragroup and intergroup variation of these features in a large sample of upper molars encompassing a wide range of fossil and extant hominid taxa and examined how well they differentiate isolated teeth of Pongo from those of Homo and other hominids. To overcome the limitations introduced by dental wear, which can obliterate informative features at the level of the outer enamel surface (OES), data collection, and analyses were performed at the enamel‐dentine junction (EDJ; Olejniczak, Smith, Wang, et al, ; Ortiz, Bailey, Hublin, & Skinner, ; Skinner et al, ; Smith et al, ). The EDJ is the interface between the enamel cap and dentine crown and preserves the end point of growth of the inner enamel epithelium (Butler, ; Schour & Massler, ).…”

“…Unless they are the result of dental tissue mineralization, which occurs later in morphogenesis, cusps (including small cuspules, conules, and tubercles) and crests develop as folds of the inner enamel epithelium (Butler, ). Thus, the study of the EDJ not only allows to more clearly determine topological relationships among dental structures (compared to the OES where these relationships may be masked by enamel deposition), but also represents an important means to distinguish between hominid taxa, even at the infraspecific level (e.g., Hanegraef et al, ; Macchiarelli et al, ; Macchiarelli, Bayle, Bondioli, Mazurier, & Zanolli, ; Macchiarelli, Bondioli, & Mazurier, ; Ortiz et al, ; Skinner et al, ; Skinner, Gunz, Wood, Boesch, & Hublin, ; Zanolli et al, , , ).…”

A comparison of relief estimates used in three‐dimensional dental topography

“…Therefore, the effect of crenulations on slope and RFIs can be considered negligible in extant apes. Based on this outcome, we assume that both slope and RFIs can be used to accurately estimate dental relief in extinct hominoids, although their molars can be very convoluted, for example, Paranthropus boisei and P. robustus (Ortiz, Bailey, Hublin, & Skinner, ).…”