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Mutations of the Drosophila myosin regulatory light chain affect courtship song and reduce reproductive success.

Chakravorty S, Vu H, Foelber V, Vigoreaux JO - PLoS ONE (2014)

Bottom Line: All three mutant males produce a less vigorous pulse song and exhibit impaired mating behavior compared to Control males.These results open the possibility that DMLC2, and perhaps contractile protein genes in general, are partly under sexual selection.That mutations in DMLC2 manifest differently in song and flight suggest that this protein fulfills different roles in song and flight and that stretch activation plays a smaller role in song production than in flight.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, The University of Vermont, Burlington, Vermont, United States of America.

ABSTRACT
The Drosophila indirect flight muscles (IFM) rely on an enhanced stretch-activation response to generate high power output for flight. The IFM is neurally activated during the male courtship song, but its role, if any, in generating the small amplitude wing vibrations that produce the song is not known. Here, we examined the courtship song properties and mating behavior of three mutant strains of the myosin regulatory light chain (DMLC2) that are known to affect IFM contractile properties and impair flight: (i) Dmlc2(Δ2-46) (Ext), an N-terminal extension truncation; (ii) Dmlc2(S66A,S67A) (Phos), a disruption of two MLC kinase phosphorylation sites; and (iii) Dmlc2(Δ2-46;S66A,S67A) (Dual), expressing both mutations. Our results show that the Dmlc2 gene is pleiotropic and that mutations that have a profound effect on flight mechanics (Phos and Dual) have minimal effects on courtship song. None of the mutations affect interpulse interval (IPI), a determinant of species-specific song, and intrapulse frequency (IPF) compared to Control (Dmlc2 (+) rescued strain). However, abnormalities in the sine song (increased frequency) and the pulse song (increased cycles per pulse and pulse length) evident in Ext males are not apparent in Dual males suggesting that Ext and Phos interact differently in song and flight mechanics, given their known additive effect on the latter. All three mutant males produce a less vigorous pulse song and exhibit impaired mating behavior compared to Control males. As a result, females are less receptive to Ext, Phos, and Dual males when a Control male is present. These results open the possibility that DMLC2, and perhaps contractile protein genes in general, are partly under sexual selection. That mutations in DMLC2 manifest differently in song and flight suggest that this protein fulfills different roles in song and flight and that stretch activation plays a smaller role in song production than in flight.

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Dmlc2 mutations affect male courtship vigor and female preference.(A) Female preference index (FPI) is the relative advantage of a male of specific genotype over a male of a different genotype, i.e., the excess number of copulations with a male of specific genotype divided by the total number of copulations [62]. Negative FPI indicate the Ext (red), Phos (green) and Dual (yellow) mutant males were out-competed by the Control male for female preference. Positive FPI indicate the Phos (green) and Dual (yellow) mutant males individually out-competed the Ext mutant males. There is no female preference for Phos or Dual males (FPI = 0). (B–C) Male courtship vigor in competitive mating situation was calculated via. courtship index (CI) and wing extension index (WEI). Ext and Dual mutants had significantly reduced CI and WEI but Phos mutant had only significantly reduced WEI compared to Control. In competition between mutants, Phos and Dual mutants have significantly higher CI and WEI compared to the Ext mutant. There is no difference between Phos and Dual. n = 20–30 for each mating competition group. *(p<0.05) indicate significant difference from Control. § (p<0.05) indicate significant differences from Ext mutant. No error bars in (A), (B–C) error bars indicate SEM.
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pone-0090077-g005: Dmlc2 mutations affect male courtship vigor and female preference.(A) Female preference index (FPI) is the relative advantage of a male of specific genotype over a male of a different genotype, i.e., the excess number of copulations with a male of specific genotype divided by the total number of copulations [62]. Negative FPI indicate the Ext (red), Phos (green) and Dual (yellow) mutant males were out-competed by the Control male for female preference. Positive FPI indicate the Phos (green) and Dual (yellow) mutant males individually out-competed the Ext mutant males. There is no female preference for Phos or Dual males (FPI = 0). (B–C) Male courtship vigor in competitive mating situation was calculated via. courtship index (CI) and wing extension index (WEI). Ext and Dual mutants had significantly reduced CI and WEI but Phos mutant had only significantly reduced WEI compared to Control. In competition between mutants, Phos and Dual mutants have significantly higher CI and WEI compared to the Ext mutant. There is no difference between Phos and Dual. n = 20–30 for each mating competition group. *(p<0.05) indicate significant difference from Control. § (p<0.05) indicate significant differences from Ext mutant. No error bars in (A), (B–C) error bars indicate SEM.

Mentions: To understand if the mutations’ effects on song and courtship affect their reproductive success, we conducted pairwise mating competitions of each mutant strain with a Control male for an OR wild-type female. All the mutant males were outcompeted by Control males as determined by female preference index (FPI) (Videos S1, S2, S3, Figure 5A). In the case of Ext and Dual, female choice was nearly 100% for Control male, whereas female preference was 60% higher for Control males than for Phos males. All mutant males exhibited lower courtship performance in the presence of a Control male, indicated by a lower CI and WEI (Ext and Dual) or lower WEI (Phos) (Figure 5B, C). Ext males are outcompeted by Phos and Dual males (Videos S4 and S5, Figure 5A) and show significantly reduced CI and WEI (Figure 5B, C). Dual males, which showed the least song aberrations compared to other mutants based on the number of parameters affected (Figure 3F,G), were able to outcompete Ext males (Video S5, Figure 5A) most likely due to their higher CI and WEI (Figure 5B, C). There is no female preference between Dual and Phos males when presented with the choice (Figure 5A). These mutant males exhibited similar CI and WEI when competing for an OR female (Figure 5B, C).


Mutations of the Drosophila myosin regulatory light chain affect courtship song and reduce reproductive success.

Chakravorty S, Vu H, Foelber V, Vigoreaux JO - PLoS ONE (2014)

Dmlc2 mutations affect male courtship vigor and female preference.(A) Female preference index (FPI) is the relative advantage of a male of specific genotype over a male of a different genotype, i.e., the excess number of copulations with a male of specific genotype divided by the total number of copulations [62]. Negative FPI indicate the Ext (red), Phos (green) and Dual (yellow) mutant males were out-competed by the Control male for female preference. Positive FPI indicate the Phos (green) and Dual (yellow) mutant males individually out-competed the Ext mutant males. There is no female preference for Phos or Dual males (FPI = 0). (B–C) Male courtship vigor in competitive mating situation was calculated via. courtship index (CI) and wing extension index (WEI). Ext and Dual mutants had significantly reduced CI and WEI but Phos mutant had only significantly reduced WEI compared to Control. In competition between mutants, Phos and Dual mutants have significantly higher CI and WEI compared to the Ext mutant. There is no difference between Phos and Dual. n = 20–30 for each mating competition group. *(p<0.05) indicate significant difference from Control. § (p<0.05) indicate significant differences from Ext mutant. No error bars in (A), (B–C) error bars indicate SEM.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3935995&req=5

pone-0090077-g005: Dmlc2 mutations affect male courtship vigor and female preference.(A) Female preference index (FPI) is the relative advantage of a male of specific genotype over a male of a different genotype, i.e., the excess number of copulations with a male of specific genotype divided by the total number of copulations [62]. Negative FPI indicate the Ext (red), Phos (green) and Dual (yellow) mutant males were out-competed by the Control male for female preference. Positive FPI indicate the Phos (green) and Dual (yellow) mutant males individually out-competed the Ext mutant males. There is no female preference for Phos or Dual males (FPI = 0). (B–C) Male courtship vigor in competitive mating situation was calculated via. courtship index (CI) and wing extension index (WEI). Ext and Dual mutants had significantly reduced CI and WEI but Phos mutant had only significantly reduced WEI compared to Control. In competition between mutants, Phos and Dual mutants have significantly higher CI and WEI compared to the Ext mutant. There is no difference between Phos and Dual. n = 20–30 for each mating competition group. *(p<0.05) indicate significant difference from Control. § (p<0.05) indicate significant differences from Ext mutant. No error bars in (A), (B–C) error bars indicate SEM.
Mentions: To understand if the mutations’ effects on song and courtship affect their reproductive success, we conducted pairwise mating competitions of each mutant strain with a Control male for an OR wild-type female. All the mutant males were outcompeted by Control males as determined by female preference index (FPI) (Videos S1, S2, S3, Figure 5A). In the case of Ext and Dual, female choice was nearly 100% for Control male, whereas female preference was 60% higher for Control males than for Phos males. All mutant males exhibited lower courtship performance in the presence of a Control male, indicated by a lower CI and WEI (Ext and Dual) or lower WEI (Phos) (Figure 5B, C). Ext males are outcompeted by Phos and Dual males (Videos S4 and S5, Figure 5A) and show significantly reduced CI and WEI (Figure 5B, C). Dual males, which showed the least song aberrations compared to other mutants based on the number of parameters affected (Figure 3F,G), were able to outcompete Ext males (Video S5, Figure 5A) most likely due to their higher CI and WEI (Figure 5B, C). There is no female preference between Dual and Phos males when presented with the choice (Figure 5A). These mutant males exhibited similar CI and WEI when competing for an OR female (Figure 5B, C).

Bottom Line: All three mutant males produce a less vigorous pulse song and exhibit impaired mating behavior compared to Control males.These results open the possibility that DMLC2, and perhaps contractile protein genes in general, are partly under sexual selection.That mutations in DMLC2 manifest differently in song and flight suggest that this protein fulfills different roles in song and flight and that stretch activation plays a smaller role in song production than in flight.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, The University of Vermont, Burlington, Vermont, United States of America.

ABSTRACT
The Drosophila indirect flight muscles (IFM) rely on an enhanced stretch-activation response to generate high power output for flight. The IFM is neurally activated during the male courtship song, but its role, if any, in generating the small amplitude wing vibrations that produce the song is not known. Here, we examined the courtship song properties and mating behavior of three mutant strains of the myosin regulatory light chain (DMLC2) that are known to affect IFM contractile properties and impair flight: (i) Dmlc2(Δ2-46) (Ext), an N-terminal extension truncation; (ii) Dmlc2(S66A,S67A) (Phos), a disruption of two MLC kinase phosphorylation sites; and (iii) Dmlc2(Δ2-46;S66A,S67A) (Dual), expressing both mutations. Our results show that the Dmlc2 gene is pleiotropic and that mutations that have a profound effect on flight mechanics (Phos and Dual) have minimal effects on courtship song. None of the mutations affect interpulse interval (IPI), a determinant of species-specific song, and intrapulse frequency (IPF) compared to Control (Dmlc2 (+) rescued strain). However, abnormalities in the sine song (increased frequency) and the pulse song (increased cycles per pulse and pulse length) evident in Ext males are not apparent in Dual males suggesting that Ext and Phos interact differently in song and flight mechanics, given their known additive effect on the latter. All three mutant males produce a less vigorous pulse song and exhibit impaired mating behavior compared to Control males. As a result, females are less receptive to Ext, Phos, and Dual males when a Control male is present. These results open the possibility that DMLC2, and perhaps contractile protein genes in general, are partly under sexual selection. That mutations in DMLC2 manifest differently in song and flight suggest that this protein fulfills different roles in song and flight and that stretch activation plays a smaller role in song production than in flight.

Show MeSH
Related in: MedlinePlus