Six million years of vole dental evolution driven by tooth development

Abstract

Morphological change occurs over macroevolutionary timescales under the action of natural selection and genetic drift combined with developmental processes shaping organogenesis1-3. Although determining their relative weight is made difficult by discrepancies between palaeontological and neontological data4, mammalian tooth morphology may bridge the gap between fossil record and laboratory observations. Fossils indicate that placentals and marsupials diversified after evolving molars bearing more cusps5-7, which emerge through the iterative signalling of enamel knots8,9. However, this theoretical evo-devo model of mammalian tooth evolution has not been explicitly assessed on empirical data. Here, by combining the fossil record with laboratory experiments, we identify a shared developmental basis for the convergent, ratcheted evolution of increasingly complex molars in arvicoline rodents (voles, lemmings, muskrats). Longer, narrower molars lead to more cusps throughout development and deep time, suggesting a developmental driver for tooth evolution. Both the arvicoline fossil record and vole tooth development show slower transitions toward the highest cusp counts. This newly identified pattern suggests that the developmental processes fuelling the evolution of increasingly complex molars may also limit the potential for further complexity increases. Integrating palaeontological and developmental data shows that long-term evolutionary trends can be accurately explained by the simple tinkering of developmental pathways.