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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

Modifications to the sex-determination pathway allow XX larvae to make spermProteins promoting spermatogenesis are blue, and those promoting oogenesis are pink. Positive interactions are shown as solid lines with arrowheads, negative ones as lines with bars, and nuclear import by dashed lines. Line thickness and font size represent the strength of each interaction. The TRA-2 receptor can be cleaved by the calpain protease TRA-3 to form the intracellular form TRA-2ic [111,112]. The target of the Caenorhabditis briggsae puf-1.2, puf-2, gld-1 and puf-8 pathway is not yet known, but it is likely that PUF-8 represses a gene needed for oogenesis [49,52]. Likewise, the secondary role that the three fem genes play downstream of tra-1 in C. elegans [56] and possibly in C. briggsae [113] is not shown because their targets remain unclear. Finally, additional genetic interactions are needed for adult hermaphrodites to switch back to oogenesis, which are reviewed elsewhere [20]. For other details, see the text.
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fig-003: Modifications to the sex-determination pathway allow XX larvae to make spermProteins promoting spermatogenesis are blue, and those promoting oogenesis are pink. Positive interactions are shown as solid lines with arrowheads, negative ones as lines with bars, and nuclear import by dashed lines. Line thickness and font size represent the strength of each interaction. The TRA-2 receptor can be cleaved by the calpain protease TRA-3 to form the intracellular form TRA-2ic [111,112]. The target of the Caenorhabditis briggsae puf-1.2, puf-2, gld-1 and puf-8 pathway is not yet known, but it is likely that PUF-8 represses a gene needed for oogenesis [49,52]. Likewise, the secondary role that the three fem genes play downstream of tra-1 in C. elegans [56] and possibly in C. briggsae [113] is not shown because their targets remain unclear. Finally, additional genetic interactions are needed for adult hermaphrodites to switch back to oogenesis, which are reviewed elsewhere [20]. For other details, see the text.

Mentions: Decades of research with C. elegans have defined a signal transduction pathway that regulates sexual development in both the somatic tissues and the germ line (Figure 3; reviewed in [19,20]). In signaling cells, the ratio of X chromosomes to autosomes controls xol-1, a gene that specifies male development. Next, XOL-1 acts through the syndecan (SDC) proteins to control the production of a hormone, HER-1 (human epidermal growth factor receptor-1), that causes cells throughout the body to adopt male fates. The ultimate target of this pathway is TRA-1, a transcription factor related to the Gli proteins [21].


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

Ellis RE, Lin SY - F1000Prime Rep (2014)

Modifications to the sex-determination pathway allow XX larvae to make spermProteins promoting spermatogenesis are blue, and those promoting oogenesis are pink. Positive interactions are shown as solid lines with arrowheads, negative ones as lines with bars, and nuclear import by dashed lines. Line thickness and font size represent the strength of each interaction. The TRA-2 receptor can be cleaved by the calpain protease TRA-3 to form the intracellular form TRA-2ic [111,112]. The target of the Caenorhabditis briggsae puf-1.2, puf-2, gld-1 and puf-8 pathway is not yet known, but it is likely that PUF-8 represses a gene needed for oogenesis [49,52]. Likewise, the secondary role that the three fem genes play downstream of tra-1 in C. elegans [56] and possibly in C. briggsae [113] is not shown because their targets remain unclear. Finally, additional genetic interactions are needed for adult hermaphrodites to switch back to oogenesis, which are reviewed elsewhere [20]. For other details, see the text.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-003: Modifications to the sex-determination pathway allow XX larvae to make spermProteins promoting spermatogenesis are blue, and those promoting oogenesis are pink. Positive interactions are shown as solid lines with arrowheads, negative ones as lines with bars, and nuclear import by dashed lines. Line thickness and font size represent the strength of each interaction. The TRA-2 receptor can be cleaved by the calpain protease TRA-3 to form the intracellular form TRA-2ic [111,112]. The target of the Caenorhabditis briggsae puf-1.2, puf-2, gld-1 and puf-8 pathway is not yet known, but it is likely that PUF-8 represses a gene needed for oogenesis [49,52]. Likewise, the secondary role that the three fem genes play downstream of tra-1 in C. elegans [56] and possibly in C. briggsae [113] is not shown because their targets remain unclear. Finally, additional genetic interactions are needed for adult hermaphrodites to switch back to oogenesis, which are reviewed elsewhere [20]. For other details, see the text.
Mentions: Decades of research with C. elegans have defined a signal transduction pathway that regulates sexual development in both the somatic tissues and the germ line (Figure 3; reviewed in [19,20]). In signaling cells, the ratio of X chromosomes to autosomes controls xol-1, a gene that specifies male development. Next, XOL-1 acts through the syndecan (SDC) proteins to control the production of a hormone, HER-1 (human epidermal growth factor receptor-1), that causes cells throughout the body to adopt male fates. The ultimate target of this pathway is TRA-1, a transcription factor related to the Gli proteins [21].

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