Two waves of anisotropic growth generate enlarged follicles in the spiny mouse.

Sophie A Montandon,António F Martins,Bastien Chopard,Michel C Milinkovitch,Athanasia C Tzika

doi:10.1186/2041-9139-5-33

Abstract

BackgroundMammals exhibit a remarkable variety of phenotypes and comparative studies using novel model species are needed to uncover the evolutionary developmental mechanisms generating this diversity. Here, we undertake a developmental biology and numerical modeling approach to investigate the development of skin appendages in the spiny mouse, Acomys dimidiatus.ResultsWe demonstrate that Acomys spines, possibly involved in display and protection, are enlarged awl hairs with a concave morphology. The Acomys spines originate from enlarged placodes that are characterized by a rapid downwards growth which results in voluminous follicles. The dermal condensation (dermal papilla) at the core of the follicle is very large and exhibits a curved geometry. Given its off-centered position, the dermal papilla generates two waves of anisotropic proliferation, first of the posterior matrix, then of the anterior inner root sheath (IRS). Higher in the follicle, the posterior and anterior cortex cross-section areas substantially decrease due to cortex cell elongation and accumulation of keratin intermediate filaments. Milder keratinization in the medulla gives rise to a foamy material that eventually collapses under the combined compression of the anterior IRS and elongation of the cortex cells. Simulations, using linear elasticity theory and the finite-element method, indicate that these processes are sufficient to replicate the time evolution of the Acomys spine layers and the final shape of the emerging spine shaft.ConclusionsOur analyses reveal how hair follicle morphogenesis has been altered during the evolution of the Acomys lineage, resulting in a shift from ancestral awl follicles to enlarged asymmetrical spines. This study contributes to a better understanding of the evolutionary developmental mechanisms that generated the great diversity of skin appendage phenotypes observed in mammals.

Highlights

Mammals exhibit a remarkable variety of phenotypes and comparative studies using novel model species are needed to uncover the evolutionary developmental mechanisms generating this diversity
Acomys spines are modified awl hairs To determine which of the hair types of the mouse coat is evolutionary homologous to Acomys spines, we collected hair (Figure 1A-J) from the ventral side as well as the upper and lower back of a subadult Acomys, and compared them to the known hair types of the laboratory mouse [16]
Three kinds of hairs were identified in Acomys (Figure 1I): (i) guard hairs, which are straight and are the longest of all hair types; (ii) awl hairs, that are the thickest of all hair types, but present a great variation in length and thickness depending on the body part they are found; and (iii) zigzag hairs that are approximately half the length of the guard hairs and are characterized by multiple bends

Summary

Introduction

Mammals exhibit a remarkable variety of phenotypes and comparative studies using novel model species are needed to uncover the evolutionary developmental mechanisms generating this diversity. Hair is one of the defining features of the Class Mammalia and is found in most of its species, mammalian skin appendages can take a diversity of other phenotypes such as the scales of pangolins, the scutes of armadillos, or the spines of echidnas and hedgehogs. These spectacular morphologies have not been reproduced in transgenic mice, there exist several strains with modified hair coat, such as Fgf mutants with longer hair [1], hairless mice (see [2] for a review), or multiple lines with coarse hair [3,4,5]. The volume of the spines makes the animal look bigger

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