Six million years of vole dental evolution shaped by tooth development

Abstract

Morphological change occurs over macroevolutionary timescales under the action of natural selection and genetic drift combined with developmental processes shaping organogenesis. Although determining their relative weight is made difficult by discrepancies between paleontological and neontological data, mammalian tooth morphology may bridge the gap between fossil record and laboratory observations. Fossils indicate that mammals have frequently diversified after evolving molars bearing more cusps, while developmental biology shows these emerge through the iterative signaling of enamel knots. However, this theoretical evo-devo model of mammalian tooth evolution has not been tested with empirical data from both fossils and laboratory experiments. In doing so, 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 that tooth development directed morphological evolution. Both the arvicoline fossil record and vole tooth development show slower transitions toward the highest cusp counts. This pattern suggests that the developmental processes fueling the evolution of increasingly complex molars may also limit the potential for further complexity increases. Integrating paleontological and developmental data shows that long-term evolutionary trends can be accurately and mostly explained by the simple tinkering of developmental pathways.