Developmental tuning of mineralization drives morphological diversity of gill cover bones in sculpins and their relatives

Eli G Cytrynbaum,Ronald Y Kwon,Matthew L Knope,Thomas Desvignes,Clayton M Small,Ruth A Bremiller,Boaz Hung,Yi-Lin Yan,Danny Kent,Charles B Kimmel

doi:10.1002/evl3.128

Abstract

The role of osteoblast placement in skeletal morphological variation is relatively well understood, but alternative developmental mechanisms affecting bone shape remain largely unknown. Specifically, very little attention has been paid to variation in later mineralization stages of intramembranous ossification as a driver of morphological diversity. We discover the occurrence of specific, sometimes large, regions of nonmineralized osteoid within bones that also contain mineralized tissue. We show through a variety of histological, molecular, and tomographic tests that this “extended” osteoid material is most likely nonmineralized bone matrix. This tissue type is a significant determinant of gill cover bone shape in the teleostean suborder Cottoidei. We demonstrate repeated evolution of extended osteoid in Cottoidei through ancestral state reconstruction and test for an association between extended osteoid variation and habitat differences among species. Through measurement of extended osteoid at various stages of gill cover development in species across the phylogeny, we gain insight into possible evolutionary developmental origins of the trait. We conclude that this fine‐tuned developmental regulation of bone matrix mineralization reflects heterochrony at multiple biological levels and is a novel mechanism for the evolution of diversity in skeletal morphology. This research lays the groundwork for a new model in which to study bone mineralization and evolutionary developmental processes, particularly as they may relate to adaptation during a prominent evolutionary radiation of fishes.

Highlights

Understanding the genetic, developmental, and evolutionary mechanisms that underlie morphological variation is an overarching aim in many branches of biology
18 of the 19 genera we surveyed within the Cottoidei exhibited at least some flexible, membranous tissue within the three primary bones that make up the operculum, or “gill cover.”
We observed a remarkable degree of variation across the superfamily Cottoidea in the amount of extended osteoid present in the opercle (OP), ranging from a complete or nearly complete absence of this tissue type to a “fork” shape in which the entire central portion of the OP was unstained (Fig 1 B and A, respectively)

Summary

Introduction

Understanding the genetic, developmental, and evolutionary mechanisms that underlie morphological variation is an overarching aim in many branches of biology. An important goal is to identify developmental mechanisms that permit specific and less disruptive (but still morphologically significant) changes to bone shape relevant at the population and species levels. Such variants likely manifest during an extended period of development, resulting in a reshaping or resizing of bones we observe and recognize as homologous in different species. Another osteoblast-specific mechanism of number of osteoblasts shape modification occurs by increasing the in a region on the edge of the bone, which can be accomplished by cell recruitment through fate switching (Takada et al 2009), by cell migration (Fukuyama et al 2004), or by local osteoblast or pre-osteoblast proliferation (Huycke et al 2012; Kim et al 2012)

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Conclusion