First Fossil Evidence for the Advance of Replacement Teeth Coupled with Life History Evolution along an Anagenetic Mammalian Lineage

Abstract

In mammals that grow up more slowly and live longer, replacement teeth tend to appear earlier in sequence than in fast growing mammals. This trend, known as ‘Schultz's Rule’, is a useful tool for inferring life histories of fossil taxa. Deviations from this rule, however, suggest that in addition to the pace of life history, ecological factors may also drive dental ontogeny. Myotragus balearicus is an extinct insular caprine that has been proved to be an excellent test case to correlate morphological traits with life history. Here we show that Myotragus balearicus exhibits a slow signature of dental eruption sequence that is in agreement with the exceptionally slow life history of this species, thus conforming to ‘Schultz's Rule’. However, our results also show an acceleration of the absolute pace of development of the permanent incisors in relation to that of the posterior teeth. The rodent-like incisors of Myotragus balearicus erupted early not only in relative but also in absolute terms (chronological age), suggesting that feeding characteristics also plays an important role in dental ontogeny. This is in agreement with ecological hypotheses based on primates. Our study documents a decoupling of the pace of development of teeth in mammals that is triggered by different selection pressures on dental ontogeny. Moreover, we show that Myotragus kopperi from the early Pleistocene (a direct ancestor of the late Pleistocene-Holocene M. balearicus) follows the pattern of first incisor replacement known in living bovids. Hence, the advance in the eruption sequence of the first incisors occurs along the Myotragus evolutionary lineage over a period of about 2.5 Myr. To our knowledge, this is the first fossil evidence of an advance of the emergence of the permanent first incisor along an anagenetic mammalian lineage.

On the relationship between hypsodonty and longevity in Myotragus balearicus–A comment on van der Geer (2014)

“…Nowhere throughout our paper have we related the incisor hypselodonty to longevity as suggested by van der Geer (). Instead, we wrote “the evergrowing incisor in M. balearicus is usually related to increased grinding force” (p. 3342), which is more or less the same as, though more precise than the statement of van der Geer () that “It is more likely that the incisors evolved their ever‐growing capability in response to something other than just longevity.” In fact, we later suggest something similar in Jordana et al (). In this latter study we provide evidence of the acceleration of the developmental rate of the rodent‐like incisor in relation to molars in M. balearicus , and suggest different selective pressures acting on dental ontogeny.…”

Unexpected evolutionary patterns of dental ontogenetic traits in cetartiodactyl mammals

“…These examples added to the current knowledge on mammals show that fine-tuning of specific changes in the dental eruption sequence are largely related to ecological factors, social behaviour, structural adjustments, and relaxed or neutral selections; and that life-history traits affect them to a lesser degree. Histological studies may provide data on life-history traits [61,62], but in the absence of such data, inferences of pace of life from dental ontogeny should be limited to higher macroevolutionary events (e.g. origin and diversification of high-level taxa).…”

Breaking the rules: Phylogeny, not life history, explains dental eruption sequence in primates

“…Smith's () work on Schultz's rule has been cited extensively in the interpretation of life history and dental eruption sequence in extant and, particularly, fossil primates (e.g., Franzen et al, ; Robson and Wood, ; Schwartz et al, ), as well as other mammals (e.g., Asher and Olbricht, ; Billet and Martin, ; Dirks, Anemone, Holroyd, Reid, and Walton, ; Loe, Meisingset, Mysterud, Langvatn, & Stenseth, ; Macho and Williamson, ; McGee and Turnbull, ; Townsend and Croft, ; Yamanaka, Yasui, Sonomura, Iwai, & Uemura, ), and even marsupials (van Nievelt and Smith, ). Researchers have also published support for Schultz's rule in the form of correlations between individual taxa, dental eruption sequence, and the pacing of life history and postnatal growth (e.g., Hellmund, ; Jordana et al, ).…”