Heterochronic shifts explain variations in a sequentially developing repeated pattern: palatal ridges of muroid rodents

Abstract

Metazoans are largely made of repeated parts, and metazoan evolution is marked by changes in the number of these parts, called meristic evolution. Understanding the mechanisms associated with meristic changes is thus a critical issue to evolutionary developmental biology. Palatal rugae are sensory ridges regularly arranged on the hard palate of mammals. They develop sequentially following mesio-distal growth of the palate, and activation-inhibition mechanisms very likely control spacing and timing of this sequential addition. In this study, we characterized trends in rugae number evolution among muroid rodents, showing that most species display 8+/-1 rugae, changes by one being very frequent in the phylogeny. We then compared development of three muroid species: mouse (nine rugae), rat (eight), and golden hamster (seven). We showed that palatal growth rate, spacing, and addition rate in mouse/rat were remarkably similar (with respect to the embryo size difference), and that increase to nine rugae in mouse is achieved by postponing the end of the addition process (hypermorphosis). Such a heterochronic shift may be typical of +/-1 variations observed among muroid rodents. In contrast, decrease to seven rugae in golden hamster is attributed to early growth termination (progenesis) of the palate, which correlates with the severe shortening of gestation in this species. Our results provide an experimental support to the intuitive view that heterochronies are especially relevant to meristic evolution of traits that rely on a sequential addition process. We also interpret our results in the light of developmental constraints specifically linked to this kind of process.