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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.

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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Expression of fgfr1 and msxC in regenerating caudal fins of brushtail mutants. Compared to a wildtype platyfish (A), X. maculatus brushtail mutants possess elongated median caudal fin rays (B). Male brushtail mutants also develop a small ventral extension of the caudal fin (swordlet). fgfr1 and msxC show a graded expression pattern in regenerating caudal fins of brushtail mutants at different stages of regeneration with strongest expression in the median fin rays (C-J). fgfr1 (C-F) and msxC (G-J) are expressed in a similar pattern as in X. helleri regenerating caudal fins. At later stages of regeneration, fgfr1 (F) and msxC show stronger expression in the ventral-most caudal fin rays of males compared to females (J). White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. (n = 3 for every stage and probe; scale bars: A and B: 1 mm; C-J: 200 μm).
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Figure 7: Expression of fgfr1 and msxC in regenerating caudal fins of brushtail mutants. Compared to a wildtype platyfish (A), X. maculatus brushtail mutants possess elongated median caudal fin rays (B). Male brushtail mutants also develop a small ventral extension of the caudal fin (swordlet). fgfr1 and msxC show a graded expression pattern in regenerating caudal fins of brushtail mutants at different stages of regeneration with strongest expression in the median fin rays (C-J). fgfr1 (C-F) and msxC (G-J) are expressed in a similar pattern as in X. helleri regenerating caudal fins. At later stages of regeneration, fgfr1 (F) and msxC show stronger expression in the ventral-most caudal fin rays of males compared to females (J). White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. (n = 3 for every stage and probe; scale bars: A and B: 1 mm; C-J: 200 μm).

Mentions: To address the question whether enhanced fgfr1 and msxC expression are generally associated with extended growth of fin rays, we analysed gene expression in regenerating caudal fins of X. maculatus brushtail mutants (Figure 1D). Individuals carrying the dominant brushtail mutation are characterized by a life-long overgrowth of medial fin rays in the caudal fin (compare Figures 7A and 7B), which is independent of sex or sexual maturity [40]. The mutation causing this phenotype is not known. Mature male brushtail mutants also grow a swordlet, a small ventral fin extension (Figure 7B), similar to the ventral caudal fin extension that naturally occurs in two species of platyfish, X. andersi and X. xiphidium, and similar to that which can be artificially produced by high levels of exogenous testosterone in some species of platyfish such as X. maculatus [20,22]. However, it lacks the pigmentation pattern typical of swords in swordtails. Since brushtail mutants are already born with a brush [40] and developing embryos are not viable when extracted from their mothers, we asked whether fgfr1 and msxC are differently expressed in regenerating brush rays, compared to more dorsal or ventral caudal fin rays. Expression of fgfr1 and msxC is strongest in the median fin rays (Figures 7C–J), which becomes particularly obvious after 4 dpa. Both genes show a graded expression pattern with a decrease of expression levels towards the dorsal and ventral fin margins (Figures 7D–F, H–J). At later stages of regeneration fgfr1 and msxC are also stronger expressed in the ventral-most caudal fin rays of males that form the swordlet, but was absent in females (compare Figure 7F to 7J, and not shown).


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 regenerating caudal fins of brushtail mutants. Compared to a wildtype platyfish (A), X. maculatus brushtail mutants possess elongated median caudal fin rays (B). Male brushtail mutants also develop a small ventral extension of the caudal fin (swordlet). fgfr1 and msxC show a graded expression pattern in regenerating caudal fins of brushtail mutants at different stages of regeneration with strongest expression in the median fin rays (C-J). fgfr1 (C-F) and msxC (G-J) are expressed in a similar pattern as in X. helleri regenerating caudal fins. At later stages of regeneration, fgfr1 (F) and msxC show stronger expression in the ventral-most caudal fin rays of males compared to females (J). White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. (n = 3 for every stage and probe; scale bars: A and B: 1 mm; C-J: 200 μm).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 7: Expression of fgfr1 and msxC in regenerating caudal fins of brushtail mutants. Compared to a wildtype platyfish (A), X. maculatus brushtail mutants possess elongated median caudal fin rays (B). Male brushtail mutants also develop a small ventral extension of the caudal fin (swordlet). fgfr1 and msxC show a graded expression pattern in regenerating caudal fins of brushtail mutants at different stages of regeneration with strongest expression in the median fin rays (C-J). fgfr1 (C-F) and msxC (G-J) are expressed in a similar pattern as in X. helleri regenerating caudal fins. At later stages of regeneration, fgfr1 (F) and msxC show stronger expression in the ventral-most caudal fin rays of males compared to females (J). White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. (n = 3 for every stage and probe; scale bars: A and B: 1 mm; C-J: 200 μm).
Mentions: To address the question whether enhanced fgfr1 and msxC expression are generally associated with extended growth of fin rays, we analysed gene expression in regenerating caudal fins of X. maculatus brushtail mutants (Figure 1D). Individuals carrying the dominant brushtail mutation are characterized by a life-long overgrowth of medial fin rays in the caudal fin (compare Figures 7A and 7B), which is independent of sex or sexual maturity [40]. The mutation causing this phenotype is not known. Mature male brushtail mutants also grow a swordlet, a small ventral fin extension (Figure 7B), similar to the ventral caudal fin extension that naturally occurs in two species of platyfish, X. andersi and X. xiphidium, and similar to that which can be artificially produced by high levels of exogenous testosterone in some species of platyfish such as X. maculatus [20,22]. However, it lacks the pigmentation pattern typical of swords in swordtails. Since brushtail mutants are already born with a brush [40] and developing embryos are not viable when extracted from their mothers, we asked whether fgfr1 and msxC are differently expressed in regenerating brush rays, compared to more dorsal or ventral caudal fin rays. Expression of fgfr1 and msxC is strongest in the median fin rays (Figures 7C–J), which becomes particularly obvious after 4 dpa. Both genes show a graded expression pattern with a decrease of expression levels towards the dorsal and ventral fin margins (Figures 7D–F, H–J). At later stages of regeneration fgfr1 and msxC are also stronger expressed in the ventral-most caudal fin rays of males that form the swordlet, but was absent in females (compare Figure 7F to 7J, and not shown).

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.

Show MeSH
Related in: MedlinePlus