Abstract

In poeciliid fish the male anal fin has been transformed into a gonopodium, an intromittent organ required for internal fertilization. Elevated testosterone levels induce metamorphosis of a subset of anal fin rays to grow and form the specialized terminal structures of the gonopodium. The molecular mechanisms underlying these processes are largely unknown. Here, we investigated whether retinoic acid (RA) signaling is involved in gonopodium development in the swordtail Xiphophorus hellerii. We showed that aldh1a2, a RA synthesizing enzyme, and the RA receptors, rar-ga and rar-gb, are expressed in anal fins during metamorphosis. aldh1a2 expression is regulated by testosterone in a concentration-dependent manner and is up-regulated in both hormone-induced and naturally developing gonopodia. Androgen receptor (ar), a putative regulator of gonopodial development, is co-expressed with aldh1a2 and the RA receptors in gonopodial rays. Importantly, experimental increase of RA signaling promoted growth of the gonopodium and increased the number of new segments. Based on gene expression analyses and pharmacological manipulation of gonopodium development, we show that the RA signaling pathway is activated in response to androgen signaling and promotes fin ray growth and development during the metamorphosis of the anal fin into the gonopodium.

Highlights

  • A majority of all extant fish species (. 95%) belongs to the group of ray finned fish

  • Given retinoic acid (RA) signaling is required for the development of paired fins and fin regeneration, we explore the potential role of RA in the metamorphosis of an unpaired anal fin into the gonopodium in a green swordtail fish, Xiphophorus hellerii

  • We show that during anal fin metamorphosis of gonopodium outgrowth aldh1a2 is co-expressed with androgen receptors and aldh1a2 gene expression increases in a testosterone concentration-dependent manner, suggesting that RA synthesis might be controlled by androgen signaling

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Summary

Introduction

A majority of all extant fish species (. 95%) belongs to the group of ray finned fish. Given more than 23,000 species the diversity of this group represents approximately 50% of all living vertebrates Most of these fishes (98%) exhibit an oviparous mode of reproduction, while in at least 54 fish families ‘viviparous’ reproduction exists [1]. The intromittent organ found in poeciliid fish, called ‘gonopodium’ is sexually dimorphic and develops from the anal fin rays 3–5, the so-called 3–4–5 complex, during sexual maturation [4,5]. These rays are a modified structure in terms of ray length, segment thickness and distal structures like blades, claws, spines, hooks and serrae [6]. The final length of the gonopodium depends on the body size of the individual fish [7]

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