Limits...
Intense sperm-mediated sexual conflict promotes reproductive isolation in Caenorhabditis nematodes.

Ting JJ, Woodruff GC, Leung G, Shin NR, Cutter AD, Haag ES - PLoS Biol. (2014)

Bottom Line: This sperm-mediated harm is pervasive across species, but idiosyncrasies in its magnitude implicate both independent histories of sexually antagonistic coevolution within species and differences in reproductive mode (self-fertilizing hermaphrodites versus females) in determining its severity.Consistent with this conclusion, in androdioecious species the hermaphrodites are more vulnerable, the males more benign, or both.Patterns of assortative mating and a low incidence of invasive sperm occurring with conspecific mating are indicative of ongoing intra-specific sexual conflict that results in inter-species reproductive incompatibility.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada.

ABSTRACT
Conflict between the sexes over reproductive interests can drive rapid evolution of reproductive traits and promote speciation. Here we show that inter-species mating between Caenorhabditis nematodes sterilizes maternal individuals. The principal effectors of male-induced harm are sperm cells, which induce sterility and shorten lifespan by displacing conspecific sperm, invading the ovary, and sometimes breaching the gonad to infiltrate other tissues. This sperm-mediated harm is pervasive across species, but idiosyncrasies in its magnitude implicate both independent histories of sexually antagonistic coevolution within species and differences in reproductive mode (self-fertilizing hermaphrodites versus females) in determining its severity. Consistent with this conclusion, in androdioecious species the hermaphrodites are more vulnerable, the males more benign, or both. Patterns of assortative mating and a low incidence of invasive sperm occurring with conspecific mating are indicative of ongoing intra-specific sexual conflict that results in inter-species reproductive incompatibility.

Show MeSH

Related in: MedlinePlus

Impacts of inter-species matings on females.Females from dioecious species (A: C. nigoni, B: C. remanei) were initially mated overnight to conspecific males, followed by overnight mating of treatment females (white) to heterospecific males from either dioecious (C. nigoni, C. remanei, C. brenneri) or androdioecious (C. briggsae, C. elegans) species; control females (red) did not receive a second mating. Reproductive output was then quantified as the number of progeny produced two days post mating treatment. (A, B) Females often became sterilized upon a subsequent mating with heterospecific males from dioecious species compared to controls: (A) C. nigoni females (C. remanei males U = 385.5, p = 0.001; C. brenneri males U = 206.5, p≤0.001), (B) C. remanei females (C. nigoni males U = 239.5, p≤0.001; C. brenneri males U = 259.5, p≤0.001). However, females were resistant to harm induced by males of androdioecious species: (A) C. nigoni (C. briggsae males U = 409.5, p = 0.020; C. elegans males U = 577.0, p = 0.291), (B) C. remanei (C. briggsae males U = 887.0, p = 0.886; C. elegans males U = 863.0, p = 0.731). (C) C. nigoni females mated to heterospecific C. briggsae males (solid red line) did not incur a statistically significant survival cost relative to conspecific mating (dashed black line; Kaplan-Meier log-rank test: χ2 = 0.203, df = 1, p = 0.652; ns not significant). Asterisks in (A and B) indicate significant difference from controls (Bonferroni correction for multiple tests were applied; corrected α = 0.0125). Boxplot whiskers in (A and B) indicate 1.5× (interquartile range) and dotted horizontal lines indicate median of viable progeny produced by the controls (females mated with conspecifics); sample sizes are shown in parentheses.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4114750&req=5

pbio-1001915-g002: Impacts of inter-species matings on females.Females from dioecious species (A: C. nigoni, B: C. remanei) were initially mated overnight to conspecific males, followed by overnight mating of treatment females (white) to heterospecific males from either dioecious (C. nigoni, C. remanei, C. brenneri) or androdioecious (C. briggsae, C. elegans) species; control females (red) did not receive a second mating. Reproductive output was then quantified as the number of progeny produced two days post mating treatment. (A, B) Females often became sterilized upon a subsequent mating with heterospecific males from dioecious species compared to controls: (A) C. nigoni females (C. remanei males U = 385.5, p = 0.001; C. brenneri males U = 206.5, p≤0.001), (B) C. remanei females (C. nigoni males U = 239.5, p≤0.001; C. brenneri males U = 259.5, p≤0.001). However, females were resistant to harm induced by males of androdioecious species: (A) C. nigoni (C. briggsae males U = 409.5, p = 0.020; C. elegans males U = 577.0, p = 0.291), (B) C. remanei (C. briggsae males U = 887.0, p = 0.886; C. elegans males U = 863.0, p = 0.731). (C) C. nigoni females mated to heterospecific C. briggsae males (solid red line) did not incur a statistically significant survival cost relative to conspecific mating (dashed black line; Kaplan-Meier log-rank test: χ2 = 0.203, df = 1, p = 0.652; ns not significant). Asterisks in (A and B) indicate significant difference from controls (Bonferroni correction for multiple tests were applied; corrected α = 0.0125). Boxplot whiskers in (A and B) indicate 1.5× (interquartile range) and dotted horizontal lines indicate median of viable progeny produced by the controls (females mated with conspecifics); sample sizes are shown in parentheses.

Mentions: To assess the generality of heterospecific sterilization, we also examined male effects on females of dioecious species (Figure 2). Despite their similar sperm sizes [48],[49], heterospecific mating of dioecious males from C. remanei, C. nigoni, and C. brenneri reduced the reproductive output of females of C. remanei and C. nigoni (Figure 2A and 2B). However, males from highly selfing species lacked the capacity to compromise the fecundity of heterospecific females (Figure 2A and 2B).


Intense sperm-mediated sexual conflict promotes reproductive isolation in Caenorhabditis nematodes.

Ting JJ, Woodruff GC, Leung G, Shin NR, Cutter AD, Haag ES - PLoS Biol. (2014)

Impacts of inter-species matings on females.Females from dioecious species (A: C. nigoni, B: C. remanei) were initially mated overnight to conspecific males, followed by overnight mating of treatment females (white) to heterospecific males from either dioecious (C. nigoni, C. remanei, C. brenneri) or androdioecious (C. briggsae, C. elegans) species; control females (red) did not receive a second mating. Reproductive output was then quantified as the number of progeny produced two days post mating treatment. (A, B) Females often became sterilized upon a subsequent mating with heterospecific males from dioecious species compared to controls: (A) C. nigoni females (C. remanei males U = 385.5, p = 0.001; C. brenneri males U = 206.5, p≤0.001), (B) C. remanei females (C. nigoni males U = 239.5, p≤0.001; C. brenneri males U = 259.5, p≤0.001). However, females were resistant to harm induced by males of androdioecious species: (A) C. nigoni (C. briggsae males U = 409.5, p = 0.020; C. elegans males U = 577.0, p = 0.291), (B) C. remanei (C. briggsae males U = 887.0, p = 0.886; C. elegans males U = 863.0, p = 0.731). (C) C. nigoni females mated to heterospecific C. briggsae males (solid red line) did not incur a statistically significant survival cost relative to conspecific mating (dashed black line; Kaplan-Meier log-rank test: χ2 = 0.203, df = 1, p = 0.652; ns not significant). Asterisks in (A and B) indicate significant difference from controls (Bonferroni correction for multiple tests were applied; corrected α = 0.0125). Boxplot whiskers in (A and B) indicate 1.5× (interquartile range) and dotted horizontal lines indicate median of viable progeny produced by the controls (females mated with conspecifics); sample sizes are shown in parentheses.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4114750&req=5

pbio-1001915-g002: Impacts of inter-species matings on females.Females from dioecious species (A: C. nigoni, B: C. remanei) were initially mated overnight to conspecific males, followed by overnight mating of treatment females (white) to heterospecific males from either dioecious (C. nigoni, C. remanei, C. brenneri) or androdioecious (C. briggsae, C. elegans) species; control females (red) did not receive a second mating. Reproductive output was then quantified as the number of progeny produced two days post mating treatment. (A, B) Females often became sterilized upon a subsequent mating with heterospecific males from dioecious species compared to controls: (A) C. nigoni females (C. remanei males U = 385.5, p = 0.001; C. brenneri males U = 206.5, p≤0.001), (B) C. remanei females (C. nigoni males U = 239.5, p≤0.001; C. brenneri males U = 259.5, p≤0.001). However, females were resistant to harm induced by males of androdioecious species: (A) C. nigoni (C. briggsae males U = 409.5, p = 0.020; C. elegans males U = 577.0, p = 0.291), (B) C. remanei (C. briggsae males U = 887.0, p = 0.886; C. elegans males U = 863.0, p = 0.731). (C) C. nigoni females mated to heterospecific C. briggsae males (solid red line) did not incur a statistically significant survival cost relative to conspecific mating (dashed black line; Kaplan-Meier log-rank test: χ2 = 0.203, df = 1, p = 0.652; ns not significant). Asterisks in (A and B) indicate significant difference from controls (Bonferroni correction for multiple tests were applied; corrected α = 0.0125). Boxplot whiskers in (A and B) indicate 1.5× (interquartile range) and dotted horizontal lines indicate median of viable progeny produced by the controls (females mated with conspecifics); sample sizes are shown in parentheses.
Mentions: To assess the generality of heterospecific sterilization, we also examined male effects on females of dioecious species (Figure 2). Despite their similar sperm sizes [48],[49], heterospecific mating of dioecious males from C. remanei, C. nigoni, and C. brenneri reduced the reproductive output of females of C. remanei and C. nigoni (Figure 2A and 2B). However, males from highly selfing species lacked the capacity to compromise the fecundity of heterospecific females (Figure 2A and 2B).

Bottom Line: This sperm-mediated harm is pervasive across species, but idiosyncrasies in its magnitude implicate both independent histories of sexually antagonistic coevolution within species and differences in reproductive mode (self-fertilizing hermaphrodites versus females) in determining its severity.Consistent with this conclusion, in androdioecious species the hermaphrodites are more vulnerable, the males more benign, or both.Patterns of assortative mating and a low incidence of invasive sperm occurring with conspecific mating are indicative of ongoing intra-specific sexual conflict that results in inter-species reproductive incompatibility.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada.

ABSTRACT
Conflict between the sexes over reproductive interests can drive rapid evolution of reproductive traits and promote speciation. Here we show that inter-species mating between Caenorhabditis nematodes sterilizes maternal individuals. The principal effectors of male-induced harm are sperm cells, which induce sterility and shorten lifespan by displacing conspecific sperm, invading the ovary, and sometimes breaching the gonad to infiltrate other tissues. This sperm-mediated harm is pervasive across species, but idiosyncrasies in its magnitude implicate both independent histories of sexually antagonistic coevolution within species and differences in reproductive mode (self-fertilizing hermaphrodites versus females) in determining its severity. Consistent with this conclusion, in androdioecious species the hermaphrodites are more vulnerable, the males more benign, or both. Patterns of assortative mating and a low incidence of invasive sperm occurring with conspecific mating are indicative of ongoing intra-specific sexual conflict that results in inter-species reproductive incompatibility.

Show MeSH
Related in: MedlinePlus