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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 second male paternity success (P2) for males from 60 different D. simulans introgressed (IG) lines. For each line we show averages and standard errors. The average P2 score of D. mauritiana is shown as a black circle. The upper bound of the 95% confidence interval of D. mauritiana average P2 is shown as a dotted line.
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Figure 1: Average second male paternity success (P2) for males from 60 different D. simulans introgressed (IG) lines. For each line we show averages and standard errors. The average P2 score of D. mauritiana is shown as a black circle. The upper bound of the 95% confidence interval of D. mauritiana average P2 is shown as a dotted line.

Mentions: A total of 2,635 D. simulans ebony females were set up to doubly mate, first with a male of the same strain then with a male from one of the 60 different IG lines. Females were removed from the final analysis if they failed to mate with either the first or the second male. Under these criteria, 913 females were excluded from the analysis leaving us with a total sample of 1,722 females. The proportion of progeny sired by the second (IG) male (P2) was angular transformed (TP2) to better fit the assumption of a normal distribution required for ANOVA. The second male paternity success scores were positively and significantly correlated with measures of female induced fecundity (Pearson correlation: R= 0.119; P < 0.001) so we tested variation among the average P2 scores of different IG lines using fecundity as a covariate. We found significant variation in P2 scores among IG lines (F59,1599 = 7.11; P < 0.001) with twelve IG lines having P2 scores not significantly higher than D. mauritiana males (t-test IG vs. D. mauritiana with P < 005) (Figure 1). We also found a significant block effect (F8,1599 = 5.71; P < 0.001) suggesting that part of the differences detected between IG males could be due to variation in environmental conditions among block trials. However, we found no significant male line × block interaction (F54,1599 = 1.15; P = 0.219) showing consistent scores of IG lines averages over blocks. The data were reanalyzed using only IG lines for which at least ten males successfully mated and excluding females that produced fewer than twenty offspring [34]. Under these criteria, we found consistent results of significant variation among IG lines (F52,1249 = 9.33; P < 0.001) and a significant block effect (F8,1249 = 4.89; P < 0.001) but a non-significant male line × block interaction (F44,1249 = 1.26; P = 0.125). Under these conditions, eleven IG lines have P2 scores not significantly higher than D. mauritiana males. Ten of them are among the twelve previously identified IG lines, the data restriction led to no data from two lines of the original twelve, and one IG line is added to the previous list as not significantly different from D. mauritiana males (Figure 2).


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 second male paternity success (P2) for males from 60 different D. simulans introgressed (IG) lines. For each line we show averages and standard errors. The average P2 score of D. mauritiana is shown as a black circle. The upper bound of the 95% confidence interval of D. mauritiana average P2 is shown as a dotted line.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Average second male paternity success (P2) for males from 60 different D. simulans introgressed (IG) lines. For each line we show averages and standard errors. The average P2 score of D. mauritiana is shown as a black circle. The upper bound of the 95% confidence interval of D. mauritiana average P2 is shown as a dotted line.
Mentions: A total of 2,635 D. simulans ebony females were set up to doubly mate, first with a male of the same strain then with a male from one of the 60 different IG lines. Females were removed from the final analysis if they failed to mate with either the first or the second male. Under these criteria, 913 females were excluded from the analysis leaving us with a total sample of 1,722 females. The proportion of progeny sired by the second (IG) male (P2) was angular transformed (TP2) to better fit the assumption of a normal distribution required for ANOVA. The second male paternity success scores were positively and significantly correlated with measures of female induced fecundity (Pearson correlation: R= 0.119; P < 0.001) so we tested variation among the average P2 scores of different IG lines using fecundity as a covariate. We found significant variation in P2 scores among IG lines (F59,1599 = 7.11; P < 0.001) with twelve IG lines having P2 scores not significantly higher than D. mauritiana males (t-test IG vs. D. mauritiana with P < 005) (Figure 1). We also found a significant block effect (F8,1599 = 5.71; P < 0.001) suggesting that part of the differences detected between IG males could be due to variation in environmental conditions among block trials. However, we found no significant male line × block interaction (F54,1599 = 1.15; P = 0.219) showing consistent scores of IG lines averages over blocks. The data were reanalyzed using only IG lines for which at least ten males successfully mated and excluding females that produced fewer than twenty offspring [34]. Under these criteria, we found consistent results of significant variation among IG lines (F52,1249 = 9.33; P < 0.001) and a significant block effect (F8,1249 = 4.89; P < 0.001) but a non-significant male line × block interaction (F44,1249 = 1.26; P = 0.125). Under these conditions, eleven IG lines have P2 scores not significantly higher than D. mauritiana males. Ten of them are among the twelve previously identified IG lines, the data restriction led to no data from two lines of the original twelve, and one IG line is added to the previous list as not significantly different from D. mauritiana males (Figure 2).

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