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Fgfr1 signalling in the development of a sexually selected trait in vertebrates, the sword of swordtail fish.

Offen N, Blum N, Meyer A, Begemann G - BMC Dev. Biol. (2008)

Bottom Line: Despite considerable interest in the evolution of the sword from a behavioural or evolutionary point of view, little is known about the developmental changes that resulted in the gain and secondary loss of the sword.Activation of a gene regulatory network that includes fgfr1 and msxC is positively correlated with fin ray growth rates and can be re-activated in platyfish to form small sword-like fin extensions.These findings point towards a disruption between the fgfr1/msxC network and its regulation by testosterone as a likely developmental cause for sword-loss in platyfish.

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Affiliation: Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, D-78457 Konstanz, Germany. nils.offen@uni-konstanz.de

ABSTRACT

Background: One of Darwin's chosen examples for his idea of sexual selection through female choice was the "sword", a colourful extension of the caudal fin of male swordtails of the genus Xiphophorus. Platyfish, also members of the genus Xiphophorus, are thought to have arisen from within the swordtails, but have secondarily lost the ability to develop a sword. The sustained increase of testosterone during sexual maturation initiates sword development in male swordtails. Addition of testosterone also induces sword-like fin extensions in some platyfish species, suggesting that the genetic interactions required for sword development may be dormant, rather than lost, within platyfish. Despite considerable interest in the evolution of the sword from a behavioural or evolutionary point of view, little is known about the developmental changes that resulted in the gain and secondary loss of the sword. Up-regulation of msxC had been shown to characterize the development of both swords and the gonopodium, a modified anal fin that serves as an intromittent organ, and prompted investigations of the regulatory mechanisms that control msxC and sword growth.

Results: By comparing both development and regeneration of caudal fins in swordtails and platyfish, we show that fgfr1 is strongly up-regulated in developing and regenerating sword and gonopodial rays. Characterization of the fin overgrowth mutant brushtail in a platyfish background confirmed that fin regeneration rates are correlated with the expression levels of fgfr1 and msxC. Moreover, brushtail re-awakens the dormant mechanisms of sword development in platyfish and activates fgfr1/msxC-signalling. Although both genes are co-expressed in scleroblasts, expression of msxC in the distal blastema may be independent of fgfr1. Known regulators of Fgf-signalling in teleost fins, fgf20a and fgf24, are transiently expressed only during regeneration and thus not likely to be required in developing swords.

Conclusion: Our data suggest that Fgf-signalling is involved upstream of msxC in the development of the sword and gonopodium in male swordtails. Activation of a gene regulatory network that includes fgfr1 and msxC is positively correlated with fin ray growth rates and can be re-activated in platyfish to form small sword-like fin extensions. These findings point towards a disruption between the fgfr1/msxC network and its regulation by testosterone as a likely developmental cause for sword-loss in platyfish.

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Expression of fgfr1 and msxC in the developing gonopodia of X. helleri and X. maculatus. fgfr1 and msxC are both expressed in developing gonopodia of X. helleri and X. maculatus. In X. helleri fgfr1 is up-regulated at 5 days (A) and 10 days (C) of treatment in mesenchymal cells (B) of the main gonopodium-forming rays 3–5 compared to control fins (G). In addition fgfr1 is strongly expressed in the interray tissue of those rays (A, C). As in developing swords, fgfr1 expression overlaps with msxC expression (D-F). In early stages of gonopodium development (5 dt) of the platyfish X. maculatus, the expression patterns of fgfr1 (H) and msxC (J) resemble that of X. helleri. Both genes are up-regulated in the same set of fin rays compared to untreated controls (L). Expression of both genes (I, K) at 10 dt is comparable to that of X. helleri with species-specific differences in the shape of growing rays. Black arrowheads indicate the expression in the distal part of the fin rays, white arrowheads indicate inter-ray expression. (X. helleri: n = 10 for every stage and probe; X. maculatus: 5 dt: n = 5; 10 dt and controls: n = 3; scale bars: A, C, D, F-L: 200 μm; B and E: 100 μm).
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Figure 4: Expression of fgfr1 and msxC in the developing gonopodia of X. helleri and X. maculatus. fgfr1 and msxC are both expressed in developing gonopodia of X. helleri and X. maculatus. In X. helleri fgfr1 is up-regulated at 5 days (A) and 10 days (C) of treatment in mesenchymal cells (B) of the main gonopodium-forming rays 3–5 compared to control fins (G). In addition fgfr1 is strongly expressed in the interray tissue of those rays (A, C). As in developing swords, fgfr1 expression overlaps with msxC expression (D-F). In early stages of gonopodium development (5 dt) of the platyfish X. maculatus, the expression patterns of fgfr1 (H) and msxC (J) resemble that of X. helleri. Both genes are up-regulated in the same set of fin rays compared to untreated controls (L). Expression of both genes (I, K) at 10 dt is comparable to that of X. helleri with species-specific differences in the shape of growing rays. Black arrowheads indicate the expression in the distal part of the fin rays, white arrowheads indicate inter-ray expression. (X. helleri: n = 10 for every stage and probe; X. maculatus: 5 dt: n = 5; 10 dt and controls: n = 3; scale bars: A, C, D, F-L: 200 μm; B and E: 100 μm).

Mentions: At 5 days of testosterone treatment, strong expression of fgfr1 was found in the distal part of the main gonopodial rays 3, 4 and 5, the so-called 3–4–5 complex [34] of X. helleri (Figure 4A). Because gene expression in deeper layers of fin rays may be shielded from detection during whole mount in situ hybridisation [35], we performed in situ hybridisation on longitudinal sections which reveal strongest expression of fgfr1 in mesenchymal cells at the tip of growing gonopodial rays (Figure 4B). This pattern persists during later stages of gonopodium development (Figure 4C). In addition, fgfr1 is up-regulated in the interray tissue (Figures 4A and 4C).


Fgfr1 signalling in the development of a sexually selected trait in vertebrates, the sword of swordtail fish.

Offen N, Blum N, Meyer A, Begemann G - BMC Dev. Biol. (2008)

Expression of fgfr1 and msxC in the developing gonopodia of X. helleri and X. maculatus. fgfr1 and msxC are both expressed in developing gonopodia of X. helleri and X. maculatus. In X. helleri fgfr1 is up-regulated at 5 days (A) and 10 days (C) of treatment in mesenchymal cells (B) of the main gonopodium-forming rays 3–5 compared to control fins (G). In addition fgfr1 is strongly expressed in the interray tissue of those rays (A, C). As in developing swords, fgfr1 expression overlaps with msxC expression (D-F). In early stages of gonopodium development (5 dt) of the platyfish X. maculatus, the expression patterns of fgfr1 (H) and msxC (J) resemble that of X. helleri. Both genes are up-regulated in the same set of fin rays compared to untreated controls (L). Expression of both genes (I, K) at 10 dt is comparable to that of X. helleri with species-specific differences in the shape of growing rays. Black arrowheads indicate the expression in the distal part of the fin rays, white arrowheads indicate inter-ray expression. (X. helleri: n = 10 for every stage and probe; X. maculatus: 5 dt: n = 5; 10 dt and controls: n = 3; scale bars: A, C, D, F-L: 200 μm; B and E: 100 μm).
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Figure 4: Expression of fgfr1 and msxC in the developing gonopodia of X. helleri and X. maculatus. fgfr1 and msxC are both expressed in developing gonopodia of X. helleri and X. maculatus. In X. helleri fgfr1 is up-regulated at 5 days (A) and 10 days (C) of treatment in mesenchymal cells (B) of the main gonopodium-forming rays 3–5 compared to control fins (G). In addition fgfr1 is strongly expressed in the interray tissue of those rays (A, C). As in developing swords, fgfr1 expression overlaps with msxC expression (D-F). In early stages of gonopodium development (5 dt) of the platyfish X. maculatus, the expression patterns of fgfr1 (H) and msxC (J) resemble that of X. helleri. Both genes are up-regulated in the same set of fin rays compared to untreated controls (L). Expression of both genes (I, K) at 10 dt is comparable to that of X. helleri with species-specific differences in the shape of growing rays. Black arrowheads indicate the expression in the distal part of the fin rays, white arrowheads indicate inter-ray expression. (X. helleri: n = 10 for every stage and probe; X. maculatus: 5 dt: n = 5; 10 dt and controls: n = 3; scale bars: A, C, D, F-L: 200 μm; B and E: 100 μm).
Mentions: At 5 days of testosterone treatment, strong expression of fgfr1 was found in the distal part of the main gonopodial rays 3, 4 and 5, the so-called 3–4–5 complex [34] of X. helleri (Figure 4A). Because gene expression in deeper layers of fin rays may be shielded from detection during whole mount in situ hybridisation [35], we performed in situ hybridisation on longitudinal sections which reveal strongest expression of fgfr1 in mesenchymal cells at the tip of growing gonopodial rays (Figure 4B). This pattern persists during later stages of gonopodium development (Figure 4C). In addition, fgfr1 is up-regulated in the interray tissue (Figures 4A and 4C).

Bottom Line: Despite considerable interest in the evolution of the sword from a behavioural or evolutionary point of view, little is known about the developmental changes that resulted in the gain and secondary loss of the sword.Activation of a gene regulatory network that includes fgfr1 and msxC is positively correlated with fin ray growth rates and can be re-activated in platyfish to form small sword-like fin extensions.These findings point towards a disruption between the fgfr1/msxC network and its regulation by testosterone as a likely developmental cause for sword-loss in platyfish.

View Article: PubMed Central - HTML - PubMed

Affiliation: Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, D-78457 Konstanz, Germany. nils.offen@uni-konstanz.de

ABSTRACT

Background: One of Darwin's chosen examples for his idea of sexual selection through female choice was the "sword", a colourful extension of the caudal fin of male swordtails of the genus Xiphophorus. Platyfish, also members of the genus Xiphophorus, are thought to have arisen from within the swordtails, but have secondarily lost the ability to develop a sword. The sustained increase of testosterone during sexual maturation initiates sword development in male swordtails. Addition of testosterone also induces sword-like fin extensions in some platyfish species, suggesting that the genetic interactions required for sword development may be dormant, rather than lost, within platyfish. Despite considerable interest in the evolution of the sword from a behavioural or evolutionary point of view, little is known about the developmental changes that resulted in the gain and secondary loss of the sword. Up-regulation of msxC had been shown to characterize the development of both swords and the gonopodium, a modified anal fin that serves as an intromittent organ, and prompted investigations of the regulatory mechanisms that control msxC and sword growth.

Results: By comparing both development and regeneration of caudal fins in swordtails and platyfish, we show that fgfr1 is strongly up-regulated in developing and regenerating sword and gonopodial rays. Characterization of the fin overgrowth mutant brushtail in a platyfish background confirmed that fin regeneration rates are correlated with the expression levels of fgfr1 and msxC. Moreover, brushtail re-awakens the dormant mechanisms of sword development in platyfish and activates fgfr1/msxC-signalling. Although both genes are co-expressed in scleroblasts, expression of msxC in the distal blastema may be independent of fgfr1. Known regulators of Fgf-signalling in teleost fins, fgf20a and fgf24, are transiently expressed only during regeneration and thus not likely to be required in developing swords.

Conclusion: Our data suggest that Fgf-signalling is involved upstream of msxC in the development of the sword and gonopodium in male swordtails. Activation of a gene regulatory network that includes fgfr1 and msxC is positively correlated with fin ray growth rates and can be re-activated in platyfish to form small sword-like fin extensions. These findings point towards a disruption between the fgfr1/msxC network and its regulation by testosterone as a likely developmental cause for sword-loss in platyfish.

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