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Exposure to endosulfan influences sperm competition in Drosophila melanogaster.

Misra S, Kumar A, Ratnasekhar Ch, Sharma V, Mudiam MK, Ravi Ram K - Sci Rep (2014)

Bottom Line: These assays, in part, are biased towards monogamy.Females soliciting multiple male partners (polyandry) is the norm in many species.Endosulfan (2 μg/ml) had no significant effect on progeny production and on the expression of certain genes associated with reproduction.

View Article: PubMed Central - PubMed

Affiliation: 1] Embryotoxicology, CSIR-Indian Institute of Toxicology Research, M.G. Marg, Lucknow 226001, Uttar Pradesh, India [2] Academy of Scientific and Innovative Research (AcSIR), CSIR-IITR campus, Lucknow 226001, UP, India.

ABSTRACT
Dwindling male fertility due to xenobiotics is of global concern. Accordingly, male reproductive toxicity assessment of xenobiotics through semen quality analysis in exposed males, and examining progeny production of their mates is critical. These assays, in part, are biased towards monogamy. Females soliciting multiple male partners (polyandry) is the norm in many species. Polyandry incites sperm competition and allows females to bias sperm use. However, consequences of xenobiotic exposure to the sperm in the light of sperm competition remain to be understood. Therefore, we exposed Drosophila melanogaster males to endosulfan, and evaluated their progeny production as well as the ability of their sperm to counter rival control sperm in the storage organs of females sequentially mated to control/exposed males. Endosulfan (2 μg/ml) had no significant effect on progeny production and on the expression of certain genes associated with reproduction. However, exposed males performed worse in sperm competition, both as 1(st) and 2(nd) male competitors. These findings indicate that simple non-competitive measures of reproductive ability may fail to demonstrate the harmful effects of low-level exposure to xenobiotics on reproduction and advocate consideration of sperm competition, as a parameter, in the reproductive toxicity assessment of xenobiotics to mimic situations prevailing in the nature.

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Assessment of the ability of sperm from males exposed to endosulfan (EGFP) to displace the rival control sperm.GFP (green) and dsRed (red) sperm observed at 2 h ASSM in the seminal receptacle of w1118 females first mated to control Prot B-dsRed males and remated to control Prot B-EGFP males (Panel A) or Prot B-EGFP males exposed to 2 μg/ml endosulfan (Panel B) are represented. Panel C represents the proportion of second male sperm (S2) in different sperm storage organs, seminal receptacle (SR), spermathecae (SP) and among the total sperm in storage (**p < 0.01; N = 10–15). Panel D represents the proportion of red eyed progeny sired by Prot B- EGFP (control/exposed) when they were second to mate (P2) with females first mated to w1118 males, out of the total (red + white eyed) progeny/female/10 days ASSM (*p = 0.0245; N = 25–30).
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f2: Assessment of the ability of sperm from males exposed to endosulfan (EGFP) to displace the rival control sperm.GFP (green) and dsRed (red) sperm observed at 2 h ASSM in the seminal receptacle of w1118 females first mated to control Prot B-dsRed males and remated to control Prot B-EGFP males (Panel A) or Prot B-EGFP males exposed to 2 μg/ml endosulfan (Panel B) are represented. Panel C represents the proportion of second male sperm (S2) in different sperm storage organs, seminal receptacle (SR), spermathecae (SP) and among the total sperm in storage (**p < 0.01; N = 10–15). Panel D represents the proportion of red eyed progeny sired by Prot B- EGFP (control/exposed) when they were second to mate (P2) with females first mated to w1118 males, out of the total (red + white eyed) progeny/female/10 days ASSM (*p = 0.0245; N = 25–30).

Mentions: To determine the efficiency of the sperm from males exposed to endosulfan to rival the control sperm from the first mate, we presented control dsRed males to the w1118 virgin females, as their first mates, and control/exposed EGFP males, as their second mates. Subsequently, we determined the proportion of second male's sperm (S2) by counting EGFP and dsRed sperm in the storage organs of these females. Under control conditions, S2 in the seminal receptacles was 0.9302 ± 0.014 (Figs. 2A & 2C). However, we observed a significant reduction in the S2 (0.7906 ± 0.0278; p = 0.0012; Figs. 2B & 2C) in seminal receptacles of females mated to exposed EGFP males, as their second mates, in comparison to those in controls (see above). On the contrary, similar to our observations in defensive sperm competition, S2 in the spermathecae of females mated to control EGFP males (0.7110 ± 0.03814; Fig. 2C) did not differ from that of females to exposed EGFP males, (0.6278 ± 0.04926; p = 0.2343; Fig. 2C). Nevertheless, the difference in the S2 levels among total sperm stored by females mated to exposed males (0.7410 ± 0.02408; p = 0.0012; Fig. 2C) was significantly different from that in their controls (0.8868 ± 0.01605; Fig. 2C). In addition, the ratio of EGFP to dsRed in seminal receptacle (p = 0.0054; Fig. S2), spermathecae (p = 0.3922; Fig. S2) and total sperm (p = 0.0015; Fig. S2) is concordant with the observed S2 levels. The altered offense capability was also reflected at the organismal level in the proportion of progeny sired by the second male (P2) of endosulfan exposure group. When the EGFP males were the second to mate, the proportions of red eyed progeny sired by them under exposed conditions were significantly lower (p = 0.0245; Fig. 2D) when compared to those under control conditions.


Exposure to endosulfan influences sperm competition in Drosophila melanogaster.

Misra S, Kumar A, Ratnasekhar Ch, Sharma V, Mudiam MK, Ravi Ram K - Sci Rep (2014)

Assessment of the ability of sperm from males exposed to endosulfan (EGFP) to displace the rival control sperm.GFP (green) and dsRed (red) sperm observed at 2 h ASSM in the seminal receptacle of w1118 females first mated to control Prot B-dsRed males and remated to control Prot B-EGFP males (Panel A) or Prot B-EGFP males exposed to 2 μg/ml endosulfan (Panel B) are represented. Panel C represents the proportion of second male sperm (S2) in different sperm storage organs, seminal receptacle (SR), spermathecae (SP) and among the total sperm in storage (**p < 0.01; N = 10–15). Panel D represents the proportion of red eyed progeny sired by Prot B- EGFP (control/exposed) when they were second to mate (P2) with females first mated to w1118 males, out of the total (red + white eyed) progeny/female/10 days ASSM (*p = 0.0245; N = 25–30).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4262826&req=5

f2: Assessment of the ability of sperm from males exposed to endosulfan (EGFP) to displace the rival control sperm.GFP (green) and dsRed (red) sperm observed at 2 h ASSM in the seminal receptacle of w1118 females first mated to control Prot B-dsRed males and remated to control Prot B-EGFP males (Panel A) or Prot B-EGFP males exposed to 2 μg/ml endosulfan (Panel B) are represented. Panel C represents the proportion of second male sperm (S2) in different sperm storage organs, seminal receptacle (SR), spermathecae (SP) and among the total sperm in storage (**p < 0.01; N = 10–15). Panel D represents the proportion of red eyed progeny sired by Prot B- EGFP (control/exposed) when they were second to mate (P2) with females first mated to w1118 males, out of the total (red + white eyed) progeny/female/10 days ASSM (*p = 0.0245; N = 25–30).
Mentions: To determine the efficiency of the sperm from males exposed to endosulfan to rival the control sperm from the first mate, we presented control dsRed males to the w1118 virgin females, as their first mates, and control/exposed EGFP males, as their second mates. Subsequently, we determined the proportion of second male's sperm (S2) by counting EGFP and dsRed sperm in the storage organs of these females. Under control conditions, S2 in the seminal receptacles was 0.9302 ± 0.014 (Figs. 2A & 2C). However, we observed a significant reduction in the S2 (0.7906 ± 0.0278; p = 0.0012; Figs. 2B & 2C) in seminal receptacles of females mated to exposed EGFP males, as their second mates, in comparison to those in controls (see above). On the contrary, similar to our observations in defensive sperm competition, S2 in the spermathecae of females mated to control EGFP males (0.7110 ± 0.03814; Fig. 2C) did not differ from that of females to exposed EGFP males, (0.6278 ± 0.04926; p = 0.2343; Fig. 2C). Nevertheless, the difference in the S2 levels among total sperm stored by females mated to exposed males (0.7410 ± 0.02408; p = 0.0012; Fig. 2C) was significantly different from that in their controls (0.8868 ± 0.01605; Fig. 2C). In addition, the ratio of EGFP to dsRed in seminal receptacle (p = 0.0054; Fig. S2), spermathecae (p = 0.3922; Fig. S2) and total sperm (p = 0.0015; Fig. S2) is concordant with the observed S2 levels. The altered offense capability was also reflected at the organismal level in the proportion of progeny sired by the second male (P2) of endosulfan exposure group. When the EGFP males were the second to mate, the proportions of red eyed progeny sired by them under exposed conditions were significantly lower (p = 0.0245; Fig. 2D) when compared to those under control conditions.

Bottom Line: These assays, in part, are biased towards monogamy.Females soliciting multiple male partners (polyandry) is the norm in many species.Endosulfan (2 μg/ml) had no significant effect on progeny production and on the expression of certain genes associated with reproduction.

View Article: PubMed Central - PubMed

Affiliation: 1] Embryotoxicology, CSIR-Indian Institute of Toxicology Research, M.G. Marg, Lucknow 226001, Uttar Pradesh, India [2] Academy of Scientific and Innovative Research (AcSIR), CSIR-IITR campus, Lucknow 226001, UP, India.

ABSTRACT
Dwindling male fertility due to xenobiotics is of global concern. Accordingly, male reproductive toxicity assessment of xenobiotics through semen quality analysis in exposed males, and examining progeny production of their mates is critical. These assays, in part, are biased towards monogamy. Females soliciting multiple male partners (polyandry) is the norm in many species. Polyandry incites sperm competition and allows females to bias sperm use. However, consequences of xenobiotic exposure to the sperm in the light of sperm competition remain to be understood. Therefore, we exposed Drosophila melanogaster males to endosulfan, and evaluated their progeny production as well as the ability of their sperm to counter rival control sperm in the storage organs of females sequentially mated to control/exposed males. Endosulfan (2 μg/ml) had no significant effect on progeny production and on the expression of certain genes associated with reproduction. However, exposed males performed worse in sperm competition, both as 1(st) and 2(nd) male competitors. These findings indicate that simple non-competitive measures of reproductive ability may fail to demonstrate the harmful effects of low-level exposure to xenobiotics on reproduction and advocate consideration of sperm competition, as a parameter, in the reproductive toxicity assessment of xenobiotics to mimic situations prevailing in the nature.

Show MeSH
Related in: MedlinePlus