Differential regulation of msx genes in the development of the gonopodium, an intromittent organ, and of the “sword,” a sexually selected trait of swordtail fishes (Xiphophorus)

Abstract

SUMMARY The possession of a conspicuous extension of colored ventral rays of the caudal fin in male fish of swordtails (genus Xiphophorus) is a prominent example for a trait that evolved by sexual selection. To understand the evolutionary history of this so-called sword molecularly, it is of interest to unravel the developmental pathways responsible for extended growth of sword rays during development of swordtail males. We isolated two msx genes and showed that they are differentially regulated during sword outgrowth. During sword growth in juvenile males, as well as during testosteroneinduced sword development and fin ray regeneration in the sword after amputation, expression of msxC is markedly upregulated in the sword forming fin rays. In contrast, msxE/1 is not differentially expressed in ventral and dorsal male fin rays, suggesting a link between the development of male secondary sexual characters in fins and up-regulation of msxC expression. In addition, we showed that msx gene expression patterns differ significantly between Xiphophorus and zebrafish. We also included in our study the gonopodium, a testosteronedependent anal fin modification that serves as a fertilization organ in males of live-bearing fishes. Our finding that increased levels of msxC expression are associated with the testosterone-induced outgrowth of the gonopodium might suggest either that at least parts of the signaling pathways that pattern the evolutionary older gonopodium have been coopted to evolve a sexually selected innovation such as the sword or that increased msxC expression may be inherent to the growth process of long fin rays in general.

Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species

“…That is, swords, due to their resemblance to gonopodia in overall shape, might effectively represent gonopodium mimics and exploit a preexisting sensory bias in females. Support for this hypothesis comes from the fact that female preference for swords arose before the evolution of swords (30,46), the gonopodium is evolutionarily older than the sword, and both gonopodium and sword development are associated with expression of the same gene (47). Further, males from predator-free environments exhibit larger swords than males from predatory environments in Xiphophorus helleri (48), a pattern parallel to that observed with gonopodium size in the present study.…”

An organizer controls the development of the “sword,” a sexually selected trait in swordtail fish

“…Initial efforts to identify sword-specific genes relied on analyzing the expression profiles of candidate genes known to be involved in zebrafish fin regeneration. Using this approach, the muscle segment homeobox gene C (msxC) was shown to be up-regulated in developing sword rays of the green swordtail, Xiphophorus helleri, and in Xiphophorus montezumae (Zauner et al 2003). Moreover, the gene was also found to be expressed in the anal fin of maturing males, which is transformed from a normal fin with a set of typical fin rays into an intromittent, sperm-transferring organ with individually different ray shapes, termed the gonopodium.…”

The genetics of sexual behavior in Drosophila

“…For example, msxC expression is associated with the development of the male "sword" of the sword tail fish. 63 Only relatively few investigations have specifically considered the evolution of sexual dimorphism, covering a wide range of study systems including the skull in primates, [64][65][66][67] body properties of lizards, 68,69 newts, 70 the head shape of Chironomous larvae, 71 and lycium flowers and insects including Drosophila. Examples of sexual dimorphism in Drosophila include abdominal bristle number, abdominal tip pigmentation in males and females, sex comb pattern of males, brain differentiation of male and female, body size, shape, and genital architecture.…”

“…In the genus Drosophila, both the sexes exhibit differences in several aspects of behavior. [61][62][63][64][65][66][67][68][69][70][71][72][73][74] In D. melanogaster, 15%-70% of known genes have sexually dimorphic expression. [75][76][77][78] In several animals, sexual dimorphism is not only restricted to reproductive organs but also present in certain morphological structures.…”