Comprehensive molecular and cellular studies suggest avian scutate scales are secondarily derived from feathers, and more distant from reptilian scales

Ping Wu,Yung-Chih Lai,Cheng-Ming Chuong,Randall Widelitz

doi:10.1038/s41598-018-35176-y

Abstract

Amniote skin appendages such as feathers, hairs and scales, provide thermoregulation, physical protection and display different color patterns to attract a mate or frighten an adversary. A long-standing question is whether “reptile scale” and “avian leg scales” are of the same origin. Understanding the relation between avian feathers, avian scales and reptilian scales will enhance our understanding of skin appendage evolution. We compared the molecular and cellular profiles in chicken feather, chicken scales and alligator scales and found that chicken scutate scales are similar to chicken feathers in morphogenesis at the early placode stage. When we compared the expression of the recently identified feather-specific genes and scale-specific genes in these skin appendages, we found that at the molecular level alligator scales are significantly different from both chicken feathers and chicken scales. Furthermore, we identified a similarly diffuse putative stem cell niche in morphologically similar chicken and alligator scales. These putative stem cells participate in alligator scale regeneration. In contrast, avian feathers have a more condensed stem cell niche, which may be responsible for cycling. Thus, our results suggest that chicken and alligator scales formed independently through convergent evolution.

Highlights

Amniotes exhibit different types of skin appendages including scales, feathers, hairs, teeth, beaks and claws
We found that the development of chicken scutate scales is different from that of both chicken feathers and alligator scales, but the shape of chicken scutate scale placodes is more similar to chicken feathers (Fig. 1M–O)
We showed that both chicken scutate scale and alligator overlapping scale development have diffuse β-Catenin and Shh expression and form a diffuse localized growth zones (LoGZ), which is different from the observed focal pattern of gene expression and LoGZ formation in chicken feathers (Fig. 1D–R)

Summary

Introduction

Amniotes exhibit different types of skin appendages including scales, feathers, hairs, teeth, beaks and claws. Reptile scales represent the basal type of amniote skin appendages from which feathers and hairs were thought to have evolved (Fig. 1A)[1,2,3]. Molecular and cellular studies have been used to understand the evolution of amniote skin appendages in extant reptiles and birds. The stem cell compartment is localized within the bulge[22], whereas in the feather follicle, stem cells are located within the collar bulge[23] (Fig. 1A) In contrast both avian and reptilian scales are not follicular structures and some reptiles, such as snakes, will shed their skin all at once, while lizards shed their skin in patches as they grow.

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Conclusion