Actinotrichia-independent developmental mechanisms of spiny rays facilitate the morphological diversification of Acanthomorpha fish fins

TL;DR

This study shows how spiny rays in fish fins evolved diverse shapes by using different cell and matrix mechanisms compared to soft rays.

Contribution

The paper reveals that spiny-ray development in fish is independent of actinotrichia, enabling morphological diversification.

Findings

Spiny-ray development does not rely on actinotrichia, unlike soft-ray development.

BMP-positive osteoblast condensation is associated with spiny-ray protrusions in filefish.

Cell distribution and signaling intensity contribute to spiny-ray modification and diversification.

Abstract

Skeletal forms in vertebrates have been regarded as good models of morphological diversification. Fish fins show great diversity in form, with their supporting skeletal structure being classified into soft rays and spiny rays. In fish evolution, spiny-ray morphologies are known to be sometimes extremely modified; however, it remains unknown how the developmental mechanisms of spiny rays have contributed to their morphological diversification. By using the rainbowfish Melanotaenia praecox for examination of the extracellular matrix (ECM) and cell dynamics of spiny-ray development, we demonstrate that spiny-ray development is independent of the actinotrichia (needle-shaped collagen polymers at the tip of fins), which are known as an important ECM in soft-ray morphogenesis. Furthermore, we found that in the thorny spiny ray of the filefish Stephanolepis cirrhifer, the lateral protrusions are associated with BMP-positive osteoblast condensation, as in the spiny-ray tips in M. praecox and S. cirrhifer. Taken together, our findings reveal that osteoblast distribution and signaling-molecule intensity would contribute to spiny-ray modification. In comparison to soft ray development, the independence from actinotrichia in spiny rays would facilitate growth direction change, leading to their morphological diversification. This suggests that variation in cell distribution and ECM usage may be important contributors to morphological diversification, not only in Acanthomorpha, but also in other animal taxa.

Fish fins are a good model for studying the evolutionary basis for morphological diversity. Here, they show that variation in cell distribution, signaling intensity, and ECM assembly all contribute to spiny ray diversification in Acanthomorpha fins.

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