Transcriptomics of two evolutionary novelties: how to make a sperm‐transfer organ out of an anal fin and a sexually selected “sword” out of a caudal fin

Abstract

Swords are exaggerated male ornaments of swordtail fishes that have been of great interest to evolutionary biologists ever since Darwin described them in the Descent of Man (1871). They are a novel sexually selected trait derived from modified ventral caudal fin rays and are only found in the genus Xiphophorus. Another phylogenetically more widespread and older male trait is the gonopodium, an intromittent organ found in all poeciliid fishes, that is derived from a modified anal fin. Despite many evolutionary and behavioral studies on both traits, little is known so far about the molecular mechanisms underlying their development. By investigating transcriptomic changes (utilizing a RNA-Seq approach) in response to testosterone treatment in the swordtail fish, Xiphophorus hellerii, we aimed to better understand the architecture of the gene regulatory networks underpinning the development of these two evolutionary novelties. Large numbers of genes with tissue-specific expression patterns were identified. Among the “sword genes” those involved in embryonic organ development, sexual character development and coloration were highly expressed, while in the gonopodium rather more morphogenesis-related genes were found. Interestingly, many genes and genetic pathways are shared between both developing novel traits derived from median fins: the sword and the gonopodium. Our analyses show that a larger set of gene networks was co-opted during the development and evolution of the “older” gonopodium than in the “younger,” and morphologically less complex trait, the sword. We provide a catalog of candidate genes for future efforts to dissect the development of those sexually selected exaggerated male traits in swordtails.

A gene expression study of ornamental fin shape in Neolamprologus brichardi, an African cichlid species

“…Hence, little is known about whether these gene regulatory networks determine fin shape traits, such as regional outgrowth, as well. In swordtail fish, where males grow a sword-like elongation on the ventral part of their caudal fin, sword-specific gene expression patterns were detected for a number of genes 14 , 25 , 26 .…”

“…Contrasting with the extensive work in fish models (mainly zebrafish), little use has so far been made of the natural diversity among fishes 12 – 14 . The resources created in zebrafish open countless possibilities to investigate genes, regulatory networks, signalling cascades, etc., for their role in fin shape diversification and to test for molecular convergence of fin shape determination across species.…”

Transcriptome analysis reveals the genetic basis underlying the seasonal development of keratinized nuptial spines in Leptobrachium boringii

“…Thus, SSTs typically evolved in male individuals [1–3]. The best studied SSTs are elaborate ornaments or weapons, such as the peacock’s tail [4], horns of scarab beetles [5], swords of the swordtail fish [6], and antlers of the deer [7]. Among SSTs, weapons have evolved multiple times across the animal kingdom [8].…”

The developmental and genetic architecture of the sexually selected male ornament of swordtails

“…S2). Because immature fish and adult females also develop a sword indistinguishable from the male structure following treatment with androgens [3,4] we generated (iii) one RNA-seq dataset from testosterone-treated adult females; and added (iv) our previous dataset from testosteroneinduced swords in pre-pubertal juveniles [3]. Small biopsies from the dorsal and ventral fin margin during a timed series of growth and of regeneration and from the hormone induced and naturally developed swords from 15-20 individuals were pooled and used for transcriptome sequencing.…”

“…Its morphogenesis is instructed by the ventral proximal caudal fin rays, called the "sword organizer" [2]. The sword is a male restricted trait, but female swordtails develop swords like males when treated with testosterone [3,4]. This suggests that a potential sexual conflict has been solved by a strict androgen dependency for expression of the phenotype.…”