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.

Differential Evolvability Along Lines of Least Resistance of Upper and Lower Molars in Island House Mice

“…Developmental studies and results from quantitative genetics have strongly undermined the simplistic view of the genotype – phenotype relationship. Redundant genetic networks can lead to a similar phenotypic signature for different quantitative traits [35]; changes in regulatory regions can drive developmental pathways to produce dramatically different phenotypic outputs without much change at the genetic level [36], [37]; subtle genetic or epigenetic changes in the temporal dynamics of development can also lead to considerable phenotypic differences in genetically similar animals [6], [9], [10], [38]. Considering the phenotypic variance in wild populations integrates all these aspects that make a trait prone to vary.…”

Developmental variability channels mouse molar evolution

“…A combined "age/weight" staging has been recommended previously (Peterka et al, 2002). Embryonic body weight provides a much better numeric estimation than age in dpc alone (Pantalacci et al, 2009;Peterka et al, 2002). The embryonic body weight alone is especially reliable within litters (at the stages examined here) but less reliable between litters, presumably because the nutritional status differs from one pregnancy to the other, causing embryos of similar embryonic age to have smaller or larger body weight.…”

“…This demonstrates that our results are robust to noise in embryonic age estimation. We also used embryonic age directly estimated from body weight (a simplification of the previous model, similar to what we used in our previous studies, (Pantalacci et al, 2009)). All the results shown in this study were robust in relation to these estimations, although they differ slightly (Appendix Figures 2-9).…”

Morphometrics as an Insight Into Processes Beyond Tooth Shape Variation in a Bank Vole Population

“…Such a mechanism is known to produce intra-specific variation in other morphological features, e.g. the number of palatal ridges in some muroid rodents [31]. A slight change in the timing of the termination or in the size of the field where the sequential addition takes place (here the dental lamina) can easily achieve a marked phenotypic output by overriding the threshold necessary to the formation of an additional sequential feature.…”