Do developmental systems preferentially produce certain types of variation that orient phenotypic evolution along preferred directions? At different scales, from the intra-population to the interspecific, the murine first upper molar shows repeated anterior elongation. Using a novel quantitative approach to compare the development of two mouse strains with short or long molars, we identified temporal, spatial and functional differences in tooth signaling center activity, that arise from differential tuning of the activation-inhibition mechanisms underlying tooth patterning. By tracing their fate, we could explain why only the upper first molar reacts via elongation of its anterior part. Despite a lack of genetic variation, individuals of the elongated strain varied in tooth length and the temporal dynamics of their signaling centers, highlighting the intrinsic instability of the upper molar developmental system. Collectively, these results reveal the variational properties of murine molar development that drive morphological evolution along a line of least resistance.

Over time species develop random mutations in their genetic sequence that causes their form to change. If this new form increases the survival of a species it will become favored through natural selection and is more likely to get passed on to future generations. But, the evolution of these new traits also depends on what happens during development. Developmental mechanisms control how an embryo progresses from a single cell to an adult organism made of many cells. Mutations that alter these processes can influence the physical outcome of development, and cause a new trait to form. This means that if many different mutations alter development in a similar way, this can lead to the same physical change, making it ‘easy’ for a new trait to repeatedly occur. Most of the research has focused on finding the mutations that underlie repeated evolution, but rarely on identifying the role of the underlying developmental mechanisms. To bridge this gap, Hayden et al. investigated how changes during development influence the shape and size of molar teeth in mice. In some wild species of mice, the front part of the first upper molar is longer than in other species. This elongation, which is repeatedly found in mice from different islands, likely came from developmental mechanisms. Tooth development in mice has been well-studied in the laboratory, and Hayden et al. started by identifying two strains of laboratory mice that mimic the teeth seen in their wild cousins, one with elongated upper first molars and another with short ones. Comparing how these two strains of mice developed their elongated or short teeth revealed key differences in the embryonic structures that form the upper molar and cause it to elongate. Further work showed that variations in these embryonic structures can even cause mice that are genetically identical to have longer or shorter upper first molars. These findings show how early differences during development can lead to small variations in form between adult species of mice. This study highlights how studying developmental differences as well as genetic sequences can further our understanding of how different species evolved.

1st Department of Medicine 1st Faculty of Medicine Charles University and General University Hospital Prague Prague Czech Republic

Department of Developmental Biology Institute of Experimental Medicine The Czech Academy of Sciences Prague Czech Republic

Department of Histology and Embryology 3rd Faculty of Medicine Charles University Prague Czech Republic

Institut de Génomique Fonctionnelle de Lyon Université de Lyon CNRS UMR 5242 Ecole Normale Supérieure de Lyon Université Claude Bernard Lyon 1 Lyon France

Laboratoire de Biologie et Modélisation de la Cellule Université de Lyon CNRS UMR 5239 Ecole Normale Supérieure de Lyon Université Claude Bernard Lyon1 INSERM U1210 Lyon France

Laboratoire de Biométrie et Biologie Evolutive Université de Lyon Université Claude Bernard Lyon 1 CNRS UMR 5558 VetAgro Sup Villeurbanne France

Master de Biologie École Normale Supérieure de Lyon Université Claude Bernard Lyon 1 Université de Lyon Lyon France

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Elife. 2020 Mar 25;9:e55952. doi: 10.7554/eLife.55952. PubMed

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