Limits...
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.

Show MeSH

Related in: MedlinePlus

Expression of fgfr1 and msxC during caudal fin regeneration. fgfr1 is expressed in the regenerating caudal fin blastema. In situ hybridisation on longitudinal sections at 4 days post amputation (dpa) reveal fgfr1 expression in the basal layer of the epidermis and in scleroblasts (A). msxC expression overlaps with thatof fgfr1 in scleroblasts (B) and shows additional expression in the distal blastema (B, G, H). There is no overall clearly visible difference in expression of fgfr1 (C-F) and msxC (G, H) between sword and non-sword regenerates until 7 dpa. At 11 dpa fgfr1 (I) and msxC (J) show higher levels of expression in regenerating sword rays than in non-sword rays, though this difference is more obvious for msxC. White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. bl = basal epidermal layer; db = distal blastema; e = epidermis; l = lepidotrichia; m = mesenchyme (4 dpa fgfr1: n = 8; 7 dpa fgfr1: n = 5; 7 dpa msxC: n = 5; 11 dpa fgfr1: n = 5; 11 dpa msxC: n = 4; scale bars: A and B: 100 μm, C-J: 200 μm).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2577654&req=5

Figure 5: Expression of fgfr1 and msxC during caudal fin regeneration. fgfr1 is expressed in the regenerating caudal fin blastema. In situ hybridisation on longitudinal sections at 4 days post amputation (dpa) reveal fgfr1 expression in the basal layer of the epidermis and in scleroblasts (A). msxC expression overlaps with thatof fgfr1 in scleroblasts (B) and shows additional expression in the distal blastema (B, G, H). There is no overall clearly visible difference in expression of fgfr1 (C-F) and msxC (G, H) between sword and non-sword regenerates until 7 dpa. At 11 dpa fgfr1 (I) and msxC (J) show higher levels of expression in regenerating sword rays than in non-sword rays, though this difference is more obvious for msxC. White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. bl = basal epidermal layer; db = distal blastema; e = epidermis; l = lepidotrichia; m = mesenchyme (4 dpa fgfr1: n = 8; 7 dpa fgfr1: n = 5; 7 dpa msxC: n = 5; 11 dpa fgfr1: n = 5; 11 dpa msxC: n = 4; scale bars: A and B: 100 μm, C-J: 200 μm).

Mentions: High levels of msxC transcription are also associated with regenerating sword rays after amputation [23]. It is assumed that the general mechanisms of growth control that act during early development are re-established during regeneration [36,37]. To test whether fgfr1 is similarly regulated in regenerating and in developing sword rays, we assayed gene expression in caudal fin blastemata. The regeneration kinetics of X. helleri roughly equals that of zebrafish at 25°C, where the regenerative outgrowth starts at ~4 dpa [38]. fgfr1 is expressed in the basal layer of the epidermis and in a proximal region, which are likely to be scleroblasts (Figure 5A). msxC and fgfr1 expression overlap in these cells. Furthermore, msxC is not expressed in the basal epidermal layer, but transcription is high in the distal blastema (Figure 5B). Sword rays and non-sword rays show similar levels of fgfr1 and msxC at different stages of regenerative outgrowth (Figures 5C–F and Figures 5G, H). Both genes stay highly up-regulated in growing blastemata until 7 dpa (Figures 5E–H).


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 during caudal fin regeneration. fgfr1 is expressed in the regenerating caudal fin blastema. In situ hybridisation on longitudinal sections at 4 days post amputation (dpa) reveal fgfr1 expression in the basal layer of the epidermis and in scleroblasts (A). msxC expression overlaps with thatof fgfr1 in scleroblasts (B) and shows additional expression in the distal blastema (B, G, H). There is no overall clearly visible difference in expression of fgfr1 (C-F) and msxC (G, H) between sword and non-sword regenerates until 7 dpa. At 11 dpa fgfr1 (I) and msxC (J) show higher levels of expression in regenerating sword rays than in non-sword rays, though this difference is more obvious for msxC. White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. bl = basal epidermal layer; db = distal blastema; e = epidermis; l = lepidotrichia; m = mesenchyme (4 dpa fgfr1: n = 8; 7 dpa fgfr1: n = 5; 7 dpa msxC: n = 5; 11 dpa fgfr1: n = 5; 11 dpa msxC: n = 4; scale bars: A and B: 100 μm, C-J: 200 μm).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Expression of fgfr1 and msxC during caudal fin regeneration. fgfr1 is expressed in the regenerating caudal fin blastema. In situ hybridisation on longitudinal sections at 4 days post amputation (dpa) reveal fgfr1 expression in the basal layer of the epidermis and in scleroblasts (A). msxC expression overlaps with thatof fgfr1 in scleroblasts (B) and shows additional expression in the distal blastema (B, G, H). There is no overall clearly visible difference in expression of fgfr1 (C-F) and msxC (G, H) between sword and non-sword regenerates until 7 dpa. At 11 dpa fgfr1 (I) and msxC (J) show higher levels of expression in regenerating sword rays than in non-sword rays, though this difference is more obvious for msxC. White arrowheads indicate expression in scleroblasts, black arrowheads the msxC expression domain in the distal blastema and white arrows the plain of amputation. bl = basal epidermal layer; db = distal blastema; e = epidermis; l = lepidotrichia; m = mesenchyme (4 dpa fgfr1: n = 8; 7 dpa fgfr1: n = 5; 7 dpa msxC: n = 5; 11 dpa fgfr1: n = 5; 11 dpa msxC: n = 4; scale bars: A and B: 100 μm, C-J: 200 μm).
Mentions: High levels of msxC transcription are also associated with regenerating sword rays after amputation [23]. It is assumed that the general mechanisms of growth control that act during early development are re-established during regeneration [36,37]. To test whether fgfr1 is similarly regulated in regenerating and in developing sword rays, we assayed gene expression in caudal fin blastemata. The regeneration kinetics of X. helleri roughly equals that of zebrafish at 25°C, where the regenerative outgrowth starts at ~4 dpa [38]. fgfr1 is expressed in the basal layer of the epidermis and in a proximal region, which are likely to be scleroblasts (Figure 5A). msxC and fgfr1 expression overlap in these cells. Furthermore, msxC is not expressed in the basal epidermal layer, but transcription is high in the distal blastema (Figure 5B). Sword rays and non-sword rays show similar levels of fgfr1 and msxC at different stages of regenerative outgrowth (Figures 5C–F and Figures 5G, H). Both genes stay highly up-regulated in growing blastemata until 7 dpa (Figures 5E–H).

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