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The evolutionary origins and consequences of self-fertility in nematodes.

Ellis RE, Lin SY - F1000Prime Rep (2014)

Bottom Line: Self-fertile hermaphrodites have evolved from male/female ancestors in many nematode species, and this transition occurred on three independent occasions in the genus Caenorhabditis.Finally, the adoption of a hermaphroditic lifestyle had profound effects on ecological and sexual interactions and genomic organization.Thus, nematode mating systems are ideal for elucidating the origin of novel traits, and studying the influence of developmental processes on evolutionary change.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Rowan University SOM, B303 Science Center 2 Medical Center Drive, Stratford, NJ 08084 USA.

ABSTRACT
Self-fertile hermaphrodites have evolved from male/female ancestors in many nematode species, and this transition occurred on three independent occasions in the genus Caenorhabditis. Genetic analyses in Caenorhabditis show that the origin of hermaphrodites required two types of changes: alterations to the sex-determination pathway that allowed otherwise female animals to make sperm during larval development, and the production of signals from the gonad that caused these sperm to activate and fertilize oocytes. Comparisons of C. elegans and C. briggsae hermaphrodites show that the ancestral sex-determination pathway has been altered in multiple unique ways. Some of these changes must have precipitated the production of sperm in XX animals, and others were modifying mutations that increased the efficiency of hermaphroditic reproduction. Reverse genetic experiments show that XX animals acquired the ability to activate sperm by co-opting one of the two redundant pathways that normally work in males. Finally, the adoption of a hermaphroditic lifestyle had profound effects on ecological and sexual interactions and genomic organization. Thus, nematode mating systems are ideal for elucidating the origin of novel traits, and studying the influence of developmental processes on evolutionary change.

No MeSH data available.


Related in: MedlinePlus

Hermaphrodites have co-opted one of two redundant sperm activation pathwaysA. Studies of Caenorhabditis elegans and C. briggsae males show that two redundant pathways control sperm activation. One pathway uses the SPE-8 group of sperm proteins to respond to an unknown signal (denoted “S8 signal”). The other pathway uses an unknown receptor (denoted “?”) to respond to the TRY-5 protease. Males defective for both pathways are sterile.B. C. briggsae and C. elegans hermaphrodites rely on the SPE-8 pathway to activate sperm, whereas C. tropicalis hermaphrodites rely on the TRY-5 pathway. For details, see the text (Wei et al., unpublished data).
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fig-004: Hermaphrodites have co-opted one of two redundant sperm activation pathwaysA. Studies of Caenorhabditis elegans and C. briggsae males show that two redundant pathways control sperm activation. One pathway uses the SPE-8 group of sperm proteins to respond to an unknown signal (denoted “S8 signal”). The other pathway uses an unknown receptor (denoted “?”) to respond to the TRY-5 protease. Males defective for both pathways are sterile.B. C. briggsae and C. elegans hermaphrodites rely on the SPE-8 pathway to activate sperm, whereas C. tropicalis hermaphrodites rely on the TRY-5 pathway. For details, see the text (Wei et al., unpublished data).

Mentions: How is sperm activation controlled? C. elegans males use two redundant pathways, one dependent on SPE-8 and the other dependent on TRY-5, whereas hermaphrodites use only the SPE-8 pathway (Figure 4, reviewed in [61]). The five genes of the spe-8 group encode sperm proteins [62-66] that appear to respond to labile zinc [67]. By contrast, TRY-5 is a protease that activates sperm by cleaving unknown targets [68]. Prior to ejaculation, TRY-5 activity is kept in check by the inhibitor SWM-1 (Figure 4A) [69]. Because C. elegans hermaphrodites normally use the spe-8 pathway to activate sperm, mutants in these genes are not self-fertile. However, their spermatids can be activated by exposure to male seminal fluid in a process called trans-activation [70]. This is done experimentally by mating sterile spe-8 hermaphrodites with males, resulting in the activation of some hermaphrodite sperm and the production of self-progeny. Transactivation implies that TRY-5 targets remain functional in hermaphrodite sperm, even if they are not normally used.


The evolutionary origins and consequences of self-fertility in nematodes.

Ellis RE, Lin SY - F1000Prime Rep (2014)

Hermaphrodites have co-opted one of two redundant sperm activation pathwaysA. Studies of Caenorhabditis elegans and C. briggsae males show that two redundant pathways control sperm activation. One pathway uses the SPE-8 group of sperm proteins to respond to an unknown signal (denoted “S8 signal”). The other pathway uses an unknown receptor (denoted “?”) to respond to the TRY-5 protease. Males defective for both pathways are sterile.B. C. briggsae and C. elegans hermaphrodites rely on the SPE-8 pathway to activate sperm, whereas C. tropicalis hermaphrodites rely on the TRY-5 pathway. For details, see the text (Wei et al., unpublished data).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4126538&req=5

fig-004: Hermaphrodites have co-opted one of two redundant sperm activation pathwaysA. Studies of Caenorhabditis elegans and C. briggsae males show that two redundant pathways control sperm activation. One pathway uses the SPE-8 group of sperm proteins to respond to an unknown signal (denoted “S8 signal”). The other pathway uses an unknown receptor (denoted “?”) to respond to the TRY-5 protease. Males defective for both pathways are sterile.B. C. briggsae and C. elegans hermaphrodites rely on the SPE-8 pathway to activate sperm, whereas C. tropicalis hermaphrodites rely on the TRY-5 pathway. For details, see the text (Wei et al., unpublished data).
Mentions: How is sperm activation controlled? C. elegans males use two redundant pathways, one dependent on SPE-8 and the other dependent on TRY-5, whereas hermaphrodites use only the SPE-8 pathway (Figure 4, reviewed in [61]). The five genes of the spe-8 group encode sperm proteins [62-66] that appear to respond to labile zinc [67]. By contrast, TRY-5 is a protease that activates sperm by cleaving unknown targets [68]. Prior to ejaculation, TRY-5 activity is kept in check by the inhibitor SWM-1 (Figure 4A) [69]. Because C. elegans hermaphrodites normally use the spe-8 pathway to activate sperm, mutants in these genes are not self-fertile. However, their spermatids can be activated by exposure to male seminal fluid in a process called trans-activation [70]. This is done experimentally by mating sterile spe-8 hermaphrodites with males, resulting in the activation of some hermaphrodite sperm and the production of self-progeny. Transactivation implies that TRY-5 targets remain functional in hermaphrodite sperm, even if they are not normally used.

Bottom Line: Self-fertile hermaphrodites have evolved from male/female ancestors in many nematode species, and this transition occurred on three independent occasions in the genus Caenorhabditis.Finally, the adoption of a hermaphroditic lifestyle had profound effects on ecological and sexual interactions and genomic organization.Thus, nematode mating systems are ideal for elucidating the origin of novel traits, and studying the influence of developmental processes on evolutionary change.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Rowan University SOM, B303 Science Center 2 Medical Center Drive, Stratford, NJ 08084 USA.

ABSTRACT
Self-fertile hermaphrodites have evolved from male/female ancestors in many nematode species, and this transition occurred on three independent occasions in the genus Caenorhabditis. Genetic analyses in Caenorhabditis show that the origin of hermaphrodites required two types of changes: alterations to the sex-determination pathway that allowed otherwise female animals to make sperm during larval development, and the production of signals from the gonad that caused these sperm to activate and fertilize oocytes. Comparisons of C. elegans and C. briggsae hermaphrodites show that the ancestral sex-determination pathway has been altered in multiple unique ways. Some of these changes must have precipitated the production of sperm in XX animals, and others were modifying mutations that increased the efficiency of hermaphroditic reproduction. Reverse genetic experiments show that XX animals acquired the ability to activate sperm by co-opting one of the two redundant pathways that normally work in males. Finally, the adoption of a hermaphroditic lifestyle had profound effects on ecological and sexual interactions and genomic organization. Thus, nematode mating systems are ideal for elucidating the origin of novel traits, and studying the influence of developmental processes on evolutionary change.

No MeSH data available.


Related in: MedlinePlus