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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 X. helleri fgf24 during fin regeneration. fgf24 is expressed in the wound epidermis at 3 dpa (A, B). Expression diminishes after 3 dpa and is almost absent by 4 dpa (C, D). fgf24 is not differentially expressed in sword rays (B) compared to non-sword rays (A). White arrowheads indicate the expression in wound epidermis and white arrows the level of amputation. (3 dpa fgf24: n = 6; 4 dpa fgf24: n = 5; scale bars: 200 μm).
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Figure 6: Expression of X. helleri fgf24 during fin regeneration. fgf24 is expressed in the wound epidermis at 3 dpa (A, B). Expression diminishes after 3 dpa and is almost absent by 4 dpa (C, D). fgf24 is not differentially expressed in sword rays (B) compared to non-sword rays (A). White arrowheads indicate the expression in wound epidermis and white arrows the level of amputation. (3 dpa fgf24: n = 6; 4 dpa fgf24: n = 5; scale bars: 200 μm).

Mentions: To further analyse the regulation of sword development and regeneration upstream of fgfr1, we cloned two putative ligands of Fgfr1, fgf24 and fgf20a, which are known to be involved in fin regeneration and development [27,28,39]. To this end we examined the expression patterns of both genes in developing and regenerating swords. We detected strong expression of fgf24 and fgf20a in caudal fin regenerates up to 3 dpa and ~1 dpa, respectively, before the transcription rate of both genes decreased (Figures 6A–D and data not shown). Therefore both genes are unlikely to play a role in the regulation of Fgf-signalling or msxC in later stages of sword regeneration, when gene regulation becomes different between sword and non-sword rays. In addition, as neither fgf24 nor fgf20a were expressed in developing swords or gonopodia (data not shown), it is unlikely that they act as ligands for Fgfr1 during these processes.


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 X. helleri fgf24 during fin regeneration. fgf24 is expressed in the wound epidermis at 3 dpa (A, B). Expression diminishes after 3 dpa and is almost absent by 4 dpa (C, D). fgf24 is not differentially expressed in sword rays (B) compared to non-sword rays (A). White arrowheads indicate the expression in wound epidermis and white arrows the level of amputation. (3 dpa fgf24: n = 6; 4 dpa fgf24: n = 5; scale bars: 200 μm).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2577654&req=5

Figure 6: Expression of X. helleri fgf24 during fin regeneration. fgf24 is expressed in the wound epidermis at 3 dpa (A, B). Expression diminishes after 3 dpa and is almost absent by 4 dpa (C, D). fgf24 is not differentially expressed in sword rays (B) compared to non-sword rays (A). White arrowheads indicate the expression in wound epidermis and white arrows the level of amputation. (3 dpa fgf24: n = 6; 4 dpa fgf24: n = 5; scale bars: 200 μm).
Mentions: To further analyse the regulation of sword development and regeneration upstream of fgfr1, we cloned two putative ligands of Fgfr1, fgf24 and fgf20a, which are known to be involved in fin regeneration and development [27,28,39]. To this end we examined the expression patterns of both genes in developing and regenerating swords. We detected strong expression of fgf24 and fgf20a in caudal fin regenerates up to 3 dpa and ~1 dpa, respectively, before the transcription rate of both genes decreased (Figures 6A–D and data not shown). Therefore both genes are unlikely to play a role in the regulation of Fgf-signalling or msxC in later stages of sword regeneration, when gene regulation becomes different between sword and non-sword rays. In addition, as neither fgf24 nor fgf20a were expressed in developing swords or gonopodia (data not shown), it is unlikely that they act as ligands for Fgfr1 during these processes.

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