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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.

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Mechanisms of sterilization by heterospecific males.(A) Shortly after mating, the smaller C. elegans male sperm (red) are displaced from the spermatheca by larger C. nigoni sperm (green) in C. elegans fog-2 “females” doubly mated to vitally dyed males. sth, spermatheca; u, uterus, v, vulva. This panel is a mosaic assembled from multiple overlapping images. (B) C. briggsae adult hermaphrodite after overnight mating with conspecific males. Abundant embryos (e) are restricted to the uterus and reliably laid through the vulva (v). Diakinesis stage oocytes (do) are seen distal to the uterus, but not beyond the bend in the reflexed gonad (asterisk). (C) When mated overnight with C. nigoni males, few embryos are produced despite abundant sperm (sp). Proximal oocytes are abnormal (ao), and diakinesis oocytes are pushed distal to the gonad bend. p, copulatory plug. (D) In hermaphrodites recently inseminated by heterospecific males, the germ line is generally well organized, but ectopic embryos (ece) can be observed distal to the oviduct (od), which is often distended by sperm that have breached it from the spermatheca (sth). Embryos are also seen in the normal uterine position, explaining how some cross progeny are laid [39]. (E) Hoechst DNA staining of conspecifically mated C. briggsae reveals abundant punctate sperm nuclei (sp) that are always restricted to the uterus and spermatheca and multiple diakinesis-stage meiotic nuclei (do). (F) DNA staining of C. briggsae hermaphrodites mated overnight with C. nigoni (similar to B) reveal a zone of endomitotic oocytes (emo) in the proximal region of the ovary abutting a large mass of sperm (sp). (G) In some cases, embryos localized to the uterus (emb) are viable (as judged by their advanced state of development) but not laid through the vulva (v).
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pbio-1001915-g003: Mechanisms of sterilization by heterospecific males.(A) Shortly after mating, the smaller C. elegans male sperm (red) are displaced from the spermatheca by larger C. nigoni sperm (green) in C. elegans fog-2 “females” doubly mated to vitally dyed males. sth, spermatheca; u, uterus, v, vulva. This panel is a mosaic assembled from multiple overlapping images. (B) C. briggsae adult hermaphrodite after overnight mating with conspecific males. Abundant embryos (e) are restricted to the uterus and reliably laid through the vulva (v). Diakinesis stage oocytes (do) are seen distal to the uterus, but not beyond the bend in the reflexed gonad (asterisk). (C) When mated overnight with C. nigoni males, few embryos are produced despite abundant sperm (sp). Proximal oocytes are abnormal (ao), and diakinesis oocytes are pushed distal to the gonad bend. p, copulatory plug. (D) In hermaphrodites recently inseminated by heterospecific males, the germ line is generally well organized, but ectopic embryos (ece) can be observed distal to the oviduct (od), which is often distended by sperm that have breached it from the spermatheca (sth). Embryos are also seen in the normal uterine position, explaining how some cross progeny are laid [39]. (E) Hoechst DNA staining of conspecifically mated C. briggsae reveals abundant punctate sperm nuclei (sp) that are always restricted to the uterus and spermatheca and multiple diakinesis-stage meiotic nuclei (do). (F) DNA staining of C. briggsae hermaphrodites mated overnight with C. nigoni (similar to B) reveal a zone of endomitotic oocytes (emo) in the proximal region of the ovary abutting a large mass of sperm (sp). (G) In some cases, embryos localized to the uterus (emb) are viable (as judged by their advanced state of development) but not laid through the vulva (v).

Mentions: One possible mechanism of reduced female fitness is competitive displacement of conspecific sperm by heterospecific sperm. Hermaphrodite Caenorhabditis make relatively small sperm that compete poorly with even conspecific male sperm, and their conspecific males make sperm that are smaller than those of dioecious species' males [31],[48],[49],[51]. Thus, the sterilization of hermaphrodites could result from the displacement of self-sperm by larger, yet ineffectual, heterospecific sperm [41]. To address this issue, we labeled C. elegans and C. nigoni males with vital dyes, mated them to phenotypically female C. elegans fog-2 animals, and observed the transferred sperm from each male in live animals. Indeed, within a few hours of mating, we observed strong displacement of the smaller C. elegans male sperm from the spermathecae by the larger C. nigoni sperm (Figures 3A and S6C). However, sperm displacement does not explain the adverse effects of heterospecific mating on survivorship nor does it account for the seeming irreversibility of sterility induced by males upon their mating partners.


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)

Mechanisms of sterilization by heterospecific males.(A) Shortly after mating, the smaller C. elegans male sperm (red) are displaced from the spermatheca by larger C. nigoni sperm (green) in C. elegans fog-2 “females” doubly mated to vitally dyed males. sth, spermatheca; u, uterus, v, vulva. This panel is a mosaic assembled from multiple overlapping images. (B) C. briggsae adult hermaphrodite after overnight mating with conspecific males. Abundant embryos (e) are restricted to the uterus and reliably laid through the vulva (v). Diakinesis stage oocytes (do) are seen distal to the uterus, but not beyond the bend in the reflexed gonad (asterisk). (C) When mated overnight with C. nigoni males, few embryos are produced despite abundant sperm (sp). Proximal oocytes are abnormal (ao), and diakinesis oocytes are pushed distal to the gonad bend. p, copulatory plug. (D) In hermaphrodites recently inseminated by heterospecific males, the germ line is generally well organized, but ectopic embryos (ece) can be observed distal to the oviduct (od), which is often distended by sperm that have breached it from the spermatheca (sth). Embryos are also seen in the normal uterine position, explaining how some cross progeny are laid [39]. (E) Hoechst DNA staining of conspecifically mated C. briggsae reveals abundant punctate sperm nuclei (sp) that are always restricted to the uterus and spermatheca and multiple diakinesis-stage meiotic nuclei (do). (F) DNA staining of C. briggsae hermaphrodites mated overnight with C. nigoni (similar to B) reveal a zone of endomitotic oocytes (emo) in the proximal region of the ovary abutting a large mass of sperm (sp). (G) In some cases, embryos localized to the uterus (emb) are viable (as judged by their advanced state of development) but not laid through the vulva (v).
© Copyright Policy
Related In: Results  -  Collection

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

pbio-1001915-g003: Mechanisms of sterilization by heterospecific males.(A) Shortly after mating, the smaller C. elegans male sperm (red) are displaced from the spermatheca by larger C. nigoni sperm (green) in C. elegans fog-2 “females” doubly mated to vitally dyed males. sth, spermatheca; u, uterus, v, vulva. This panel is a mosaic assembled from multiple overlapping images. (B) C. briggsae adult hermaphrodite after overnight mating with conspecific males. Abundant embryos (e) are restricted to the uterus and reliably laid through the vulva (v). Diakinesis stage oocytes (do) are seen distal to the uterus, but not beyond the bend in the reflexed gonad (asterisk). (C) When mated overnight with C. nigoni males, few embryos are produced despite abundant sperm (sp). Proximal oocytes are abnormal (ao), and diakinesis oocytes are pushed distal to the gonad bend. p, copulatory plug. (D) In hermaphrodites recently inseminated by heterospecific males, the germ line is generally well organized, but ectopic embryos (ece) can be observed distal to the oviduct (od), which is often distended by sperm that have breached it from the spermatheca (sth). Embryos are also seen in the normal uterine position, explaining how some cross progeny are laid [39]. (E) Hoechst DNA staining of conspecifically mated C. briggsae reveals abundant punctate sperm nuclei (sp) that are always restricted to the uterus and spermatheca and multiple diakinesis-stage meiotic nuclei (do). (F) DNA staining of C. briggsae hermaphrodites mated overnight with C. nigoni (similar to B) reveal a zone of endomitotic oocytes (emo) in the proximal region of the ovary abutting a large mass of sperm (sp). (G) In some cases, embryos localized to the uterus (emb) are viable (as judged by their advanced state of development) but not laid through the vulva (v).
Mentions: One possible mechanism of reduced female fitness is competitive displacement of conspecific sperm by heterospecific sperm. Hermaphrodite Caenorhabditis make relatively small sperm that compete poorly with even conspecific male sperm, and their conspecific males make sperm that are smaller than those of dioecious species' males [31],[48],[49],[51]. Thus, the sterilization of hermaphrodites could result from the displacement of self-sperm by larger, yet ineffectual, heterospecific sperm [41]. To address this issue, we labeled C. elegans and C. nigoni males with vital dyes, mated them to phenotypically female C. elegans fog-2 animals, and observed the transferred sperm from each male in live animals. Indeed, within a few hours of mating, we observed strong displacement of the smaller C. elegans male sperm from the spermathecae by the larger C. nigoni sperm (Figures 3A and S6C). However, sperm displacement does not explain the adverse effects of heterospecific mating on survivorship nor does it account for the seeming irreversibility of sterility induced by males upon their mating partners.

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