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Third chromosome candidate genes for conspecific sperm precedence between D. simulans and D. mauritiana.

Levesque L, Brouwers B, Sundararajan V, Civetta A - BMC Genet. (2010)

Bottom Line: Our results show a complex genetic basis for conspecific sperm precedence, with evidence of gene interactions between at least two third chromosome loci.Pleiotropy is also evident from correlation between conspecific sperm precedence and female induced fecundity and the identification of candidate genes that might exert an effect through genetic conflict and immunity.A third of candidate genes within these two loci are located in the 89B cytogenetic position, highlighting a possible major role for this chromosome position during the evolution of species specific adaptations to postmating prezygotic reproductive challenges.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of Winnipeg, Winnipeg, Manitoba, R3B 2E9, Canada.

ABSTRACT

Background: Male - female incompatibilities can be critical in keeping species as separate and discrete units. Premating incompatibilities and postzygotic hybrid sterility/inviability have been widely studied as isolating barriers between species. In recent years, a number of studies have brought attention to postmating prezygotic barriers arising from male - male competition and male - female interactions. Yet little is known about the genetic basis of postmating prezygotic isolation barriers between species.

Results: Using D. simulans lines with mapped introgressions of D. mauritiana into their third chromosome, we find at least two D. mauritiana introgressions causing male breakdown in competitive paternity success. Eighty one genes within the mapped introgressed regions were identified as broad-sense candidates on the basis of male reproductive tract expression and male-related function. The list of candidates was narrowed down to five genes based on differences in male reproductive tract expression between D. simulans and D. mauritiana. Another ten genes were confirmed as candidates using evidence of adaptive gene coding sequence diversification in the D. simulans and/or D. mauritiana lineage. Our results show a complex genetic basis for conspecific sperm precedence, with evidence of gene interactions between at least two third chromosome loci. Pleiotropy is also evident from correlation between conspecific sperm precedence and female induced fecundity and the identification of candidate genes that might exert an effect through genetic conflict and immunity.

Conclusions: We identified at least two loci responsible for conspecific sperm precedence. A third of candidate genes within these two loci are located in the 89B cytogenetic position, highlighting a possible major role for this chromosome position during the evolution of species specific adaptations to postmating prezygotic reproductive challenges.

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Average fold difference in expression from male reproductive tract RNA extractions for 81 candidate genes between D. simulans and D. mauritiana. The differences in gene expression are shown as D. mauritiana relative to D. simulans (ma/si). The data is plotted with the X axis representing the cytogenetic map position. Experiment-wise statistical threshold at P < 0.05 and P < 0.1 are shown by solid and dotted lines respectively. Notice that 3 out of 5 genes showing significant differences in gene expression (P < 0.05) are located in map position 89B (CG14891, CG10317 and Mst89B).
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Figure 3: Average fold difference in expression from male reproductive tract RNA extractions for 81 candidate genes between D. simulans and D. mauritiana. The differences in gene expression are shown as D. mauritiana relative to D. simulans (ma/si). The data is plotted with the X axis representing the cytogenetic map position. Experiment-wise statistical threshold at P < 0.05 and P < 0.1 are shown by solid and dotted lines respectively. Notice that 3 out of 5 genes showing significant differences in gene expression (P < 0.05) are located in map position 89B (CG14891, CG10317 and Mst89B).

Mentions: We used 60 IG lines to map loci causing CSP, but we are ultimately interested in gene differences at mapped positions between pure species rather than IG lines. Therefore, differences in gene expression for all 81 broad-sense candidate genes were tested between D. simulans and D. mauritiana. We obtained RNA samples from the male reproductive tract of both D. mauritiana and D. simulans and performed quantitative real-time PCR (qRT-PCR) from reverse transcribed products corresponding to our 81 broad-sense candidate genes. We identified between five (CG10317, CG14891, Mst89B, CG6040 and CG4836) and eight (same as before plus CG3610, CG17387 and CG31287) candidate genes with significant differences in gene expression between the two species using either a five or ten percent threshold level respectively (Figure 3). This result is not qualitatively different when using two-fold average differences in gene expression and its 95% confidence interval as threshold (data not shown). Only one (CG17387) of the eight genes is located in the 77B to 84B. Three of the five differentially regulated genes (CG10397, CG14891 and Mst89B) as well as CG31287 are located in the 89B position suggesting that the evolution of species specific coregulation patterns of this gene cluster could be critical during species diversification and the evolution of CSP.


Third chromosome candidate genes for conspecific sperm precedence between D. simulans and D. mauritiana.

Levesque L, Brouwers B, Sundararajan V, Civetta A - BMC Genet. (2010)

Average fold difference in expression from male reproductive tract RNA extractions for 81 candidate genes between D. simulans and D. mauritiana. The differences in gene expression are shown as D. mauritiana relative to D. simulans (ma/si). The data is plotted with the X axis representing the cytogenetic map position. Experiment-wise statistical threshold at P < 0.05 and P < 0.1 are shown by solid and dotted lines respectively. Notice that 3 out of 5 genes showing significant differences in gene expression (P < 0.05) are located in map position 89B (CG14891, CG10317 and Mst89B).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2864193&req=5

Figure 3: Average fold difference in expression from male reproductive tract RNA extractions for 81 candidate genes between D. simulans and D. mauritiana. The differences in gene expression are shown as D. mauritiana relative to D. simulans (ma/si). The data is plotted with the X axis representing the cytogenetic map position. Experiment-wise statistical threshold at P < 0.05 and P < 0.1 are shown by solid and dotted lines respectively. Notice that 3 out of 5 genes showing significant differences in gene expression (P < 0.05) are located in map position 89B (CG14891, CG10317 and Mst89B).
Mentions: We used 60 IG lines to map loci causing CSP, but we are ultimately interested in gene differences at mapped positions between pure species rather than IG lines. Therefore, differences in gene expression for all 81 broad-sense candidate genes were tested between D. simulans and D. mauritiana. We obtained RNA samples from the male reproductive tract of both D. mauritiana and D. simulans and performed quantitative real-time PCR (qRT-PCR) from reverse transcribed products corresponding to our 81 broad-sense candidate genes. We identified between five (CG10317, CG14891, Mst89B, CG6040 and CG4836) and eight (same as before plus CG3610, CG17387 and CG31287) candidate genes with significant differences in gene expression between the two species using either a five or ten percent threshold level respectively (Figure 3). This result is not qualitatively different when using two-fold average differences in gene expression and its 95% confidence interval as threshold (data not shown). Only one (CG17387) of the eight genes is located in the 77B to 84B. Three of the five differentially regulated genes (CG10397, CG14891 and Mst89B) as well as CG31287 are located in the 89B position suggesting that the evolution of species specific coregulation patterns of this gene cluster could be critical during species diversification and the evolution of CSP.

Bottom Line: Our results show a complex genetic basis for conspecific sperm precedence, with evidence of gene interactions between at least two third chromosome loci.Pleiotropy is also evident from correlation between conspecific sperm precedence and female induced fecundity and the identification of candidate genes that might exert an effect through genetic conflict and immunity.A third of candidate genes within these two loci are located in the 89B cytogenetic position, highlighting a possible major role for this chromosome position during the evolution of species specific adaptations to postmating prezygotic reproductive challenges.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of Winnipeg, Winnipeg, Manitoba, R3B 2E9, Canada.

ABSTRACT

Background: Male - female incompatibilities can be critical in keeping species as separate and discrete units. Premating incompatibilities and postzygotic hybrid sterility/inviability have been widely studied as isolating barriers between species. In recent years, a number of studies have brought attention to postmating prezygotic barriers arising from male - male competition and male - female interactions. Yet little is known about the genetic basis of postmating prezygotic isolation barriers between species.

Results: Using D. simulans lines with mapped introgressions of D. mauritiana into their third chromosome, we find at least two D. mauritiana introgressions causing male breakdown in competitive paternity success. Eighty one genes within the mapped introgressed regions were identified as broad-sense candidates on the basis of male reproductive tract expression and male-related function. The list of candidates was narrowed down to five genes based on differences in male reproductive tract expression between D. simulans and D. mauritiana. Another ten genes were confirmed as candidates using evidence of adaptive gene coding sequence diversification in the D. simulans and/or D. mauritiana lineage. Our results show a complex genetic basis for conspecific sperm precedence, with evidence of gene interactions between at least two third chromosome loci. Pleiotropy is also evident from correlation between conspecific sperm precedence and female induced fecundity and the identification of candidate genes that might exert an effect through genetic conflict and immunity.

Conclusions: We identified at least two loci responsible for conspecific sperm precedence. A third of candidate genes within these two loci are located in the 89B cytogenetic position, highlighting a possible major role for this chromosome position during the evolution of species specific adaptations to postmating prezygotic reproductive challenges.

Show MeSH
Related in: MedlinePlus