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Rogue sperm indicate sexually antagonistic coevolution in nematodes.

Ellis RE, Schärer L - PLoS Biol. (2014)

Bottom Line: These harmful effects are sometimes observed in crosses between animals of the same species but are most easily detected in interspecies crosses, leading to dramatically lowered fitness, presumably because the competitiveness of the sperm and the associated female countermeasures are not precisely matched.This mismatch is most obvious in crosses involving individuals from androdioecious species (which have both hermaphrodites and males), as predicted by the lower levels of sperm competition these species experience.These results suggest a striking example of sexually antagonistic coevolution and dramatically expand the value of nematodes as a laboratory system for studying postcopulatory interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Rowan University SOM, Stratford, New Jersey, United States of America.

ABSTRACT
Intense reproductive competition often continues long after animals finish mating. In many species, sperm from one male compete with those from others to find and fertilize oocytes. Since this competition occurs inside the female reproductive tract, she often influences the outcome through physical or chemical factors, leading to cryptic female choice. Finally, traits that help males compete with each other are sometimes harmful to females, and female countermeasures may thwart the interests of males, which can lead to an arms race between the sexes known as sexually antagonistic coevolution. New studies from Caenorhabditis nematodes suggest that males compete with each other by producing sperm that migrate aggressively and that these sperm may be more likely to win access to oocytes. However, one byproduct of this competition appears to be an increased probability that these sperm will go astray, invading the ovary, prematurely activating oocytes, and sometimes crossing basement membranes and leaving the gonad altogether. These harmful effects are sometimes observed in crosses between animals of the same species but are most easily detected in interspecies crosses, leading to dramatically lowered fitness, presumably because the competitiveness of the sperm and the associated female countermeasures are not precisely matched. This mismatch is most obvious in crosses involving individuals from androdioecious species (which have both hermaphrodites and males), as predicted by the lower levels of sperm competition these species experience. These results suggest a striking example of sexually antagonistic coevolution and dramatically expand the value of nematodes as a laboratory system for studying postcopulatory interactions.

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Sperm vigor and female defenses undergo sexually antagonistic coevolution.(A) In a benign interaction between the sexes, male sperm compete for position in the spermatheca, and a combination of female signals and control of the distal spermathecal valve prevent them from entering the ovary. (B) Because of sperm competition, some males develop more competitive sperm that cannot be excluded from the ovary and thus become invasive; resulting fitness costs will favor additional female countermeasures through sexually antagonistic coevolution.
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pbio-1001916-g004: Sperm vigor and female defenses undergo sexually antagonistic coevolution.(A) In a benign interaction between the sexes, male sperm compete for position in the spermatheca, and a combination of female signals and control of the distal spermathecal valve prevent them from entering the ovary. (B) Because of sperm competition, some males develop more competitive sperm that cannot be excluded from the ovary and thus become invasive; resulting fitness costs will favor additional female countermeasures through sexually antagonistic coevolution.

Mentions: Finally and perhaps most intriguingly, the authors found that male sperm sometimes go astray even in crosses between males and females of the same species. Thus, the interspecies crosses may simply provide a more sensitive way to measure interactions that are going on within individual species in the wild. A simple model that can explain their results is that dioecious males are under intense selection to produce highly migratory sperm, which will have the best chance to find good positions in the spermathecae for fertilizing oocytes (Figure 4A). However, the aggressiveness of these sperm means that females need to develop appropriate countermeasures, such as changes in their chemical signals or the physical strength of the distal spermathecal valve, to keep the sperm contained and prevent them from entering regions of the female gonad where they could cause harm. If the competitiveness of a male's sperm is not in sync with the countermeasures of his mate, some overzealous sperm could go rogue, causing a significant loss in fitness (Figure 4B). Thus, selection on males could favor highly migratory sperm that outcompete those from other males, even if they occasionally lower female fertility. In addition, selection in females should favor protective countermeasures that restore normal fertility but may decrease male fitness. This sexually antagonistic coevolution is expected to cause rapid changes in both sexes, which are revealed when animals from different species are used in experimental crosses.


Rogue sperm indicate sexually antagonistic coevolution in nematodes.

Ellis RE, Schärer L - PLoS Biol. (2014)

Sperm vigor and female defenses undergo sexually antagonistic coevolution.(A) In a benign interaction between the sexes, male sperm compete for position in the spermatheca, and a combination of female signals and control of the distal spermathecal valve prevent them from entering the ovary. (B) Because of sperm competition, some males develop more competitive sperm that cannot be excluded from the ovary and thus become invasive; resulting fitness costs will favor additional female countermeasures through sexually antagonistic coevolution.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4114837&req=5

pbio-1001916-g004: Sperm vigor and female defenses undergo sexually antagonistic coevolution.(A) In a benign interaction between the sexes, male sperm compete for position in the spermatheca, and a combination of female signals and control of the distal spermathecal valve prevent them from entering the ovary. (B) Because of sperm competition, some males develop more competitive sperm that cannot be excluded from the ovary and thus become invasive; resulting fitness costs will favor additional female countermeasures through sexually antagonistic coevolution.
Mentions: Finally and perhaps most intriguingly, the authors found that male sperm sometimes go astray even in crosses between males and females of the same species. Thus, the interspecies crosses may simply provide a more sensitive way to measure interactions that are going on within individual species in the wild. A simple model that can explain their results is that dioecious males are under intense selection to produce highly migratory sperm, which will have the best chance to find good positions in the spermathecae for fertilizing oocytes (Figure 4A). However, the aggressiveness of these sperm means that females need to develop appropriate countermeasures, such as changes in their chemical signals or the physical strength of the distal spermathecal valve, to keep the sperm contained and prevent them from entering regions of the female gonad where they could cause harm. If the competitiveness of a male's sperm is not in sync with the countermeasures of his mate, some overzealous sperm could go rogue, causing a significant loss in fitness (Figure 4B). Thus, selection on males could favor highly migratory sperm that outcompete those from other males, even if they occasionally lower female fertility. In addition, selection in females should favor protective countermeasures that restore normal fertility but may decrease male fitness. This sexually antagonistic coevolution is expected to cause rapid changes in both sexes, which are revealed when animals from different species are used in experimental crosses.

Bottom Line: These harmful effects are sometimes observed in crosses between animals of the same species but are most easily detected in interspecies crosses, leading to dramatically lowered fitness, presumably because the competitiveness of the sperm and the associated female countermeasures are not precisely matched.This mismatch is most obvious in crosses involving individuals from androdioecious species (which have both hermaphrodites and males), as predicted by the lower levels of sperm competition these species experience.These results suggest a striking example of sexually antagonistic coevolution and dramatically expand the value of nematodes as a laboratory system for studying postcopulatory interactions.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Rowan University SOM, Stratford, New Jersey, United States of America.

ABSTRACT
Intense reproductive competition often continues long after animals finish mating. In many species, sperm from one male compete with those from others to find and fertilize oocytes. Since this competition occurs inside the female reproductive tract, she often influences the outcome through physical or chemical factors, leading to cryptic female choice. Finally, traits that help males compete with each other are sometimes harmful to females, and female countermeasures may thwart the interests of males, which can lead to an arms race between the sexes known as sexually antagonistic coevolution. New studies from Caenorhabditis nematodes suggest that males compete with each other by producing sperm that migrate aggressively and that these sperm may be more likely to win access to oocytes. However, one byproduct of this competition appears to be an increased probability that these sperm will go astray, invading the ovary, prematurely activating oocytes, and sometimes crossing basement membranes and leaving the gonad altogether. These harmful effects are sometimes observed in crosses between animals of the same species but are most easily detected in interspecies crosses, leading to dramatically lowered fitness, presumably because the competitiveness of the sperm and the associated female countermeasures are not precisely matched. This mismatch is most obvious in crosses involving individuals from androdioecious species (which have both hermaphrodites and males), as predicted by the lower levels of sperm competition these species experience. These results suggest a striking example of sexually antagonistic coevolution and dramatically expand the value of nematodes as a laboratory system for studying postcopulatory interactions.

Show MeSH