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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 evolved on three independent occasions in CaenorhabditisOnly species with sequenced genomes are shown. Androdioecious species with males and hermaphrodites are marked with a red symbol, and the others are male/female. The species in blue are able to interbreed and produce fertile offspring, and two outgroup species are orange. Modified from Kiontke et al. [18] and Felix et al. [15].
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fig-001: Hermaphrodites evolved on three independent occasions in CaenorhabditisOnly species with sequenced genomes are shown. Androdioecious species with males and hermaphrodites are marked with a red symbol, and the others are male/female. The species in blue are able to interbreed and produce fertile offspring, and two outgroup species are orange. Modified from Kiontke et al. [18] and Felix et al. [15].

Mentions: Here, we review the evolution of self-fertility in Caenorhabditis nematodes. The convergent evolution of hermaphrodites in this genus provides an ideal way to explore both evolutionary change and the use of alternative reproductive strategies (reviewed in [5,6]). Phylogenetic analysis implies that mating systems changed recently, which makes it easier to reconstruct many of the underlying genetic events (Figure 1). Furthermore, technical considerations make this genus ideal for study. C. elegans is one of the leading models for studying sex-determination, and decades of research provide the background information needed to characterize its relatives. This task is simplified by the genome sequences of C. elegans [7] and C. briggsae [8], and the partial sequences of seven related species (Figure 1). Finally, orthologous genes can be characterized by powerful reverse genetic techniques, including RNA interference and gene-editing with transcription activator-like effector nucleases (TALENs) or clustered regularly interspaced short palindromic repeats (CRISPRs) [9-13], which allow the control of mating systems to be dissected in all species.


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

Ellis RE, Lin SY - F1000Prime Rep (2014)

Hermaphrodites evolved on three independent occasions in CaenorhabditisOnly species with sequenced genomes are shown. Androdioecious species with males and hermaphrodites are marked with a red symbol, and the others are male/female. The species in blue are able to interbreed and produce fertile offspring, and two outgroup species are orange. Modified from Kiontke et al. [18] and Felix et al. [15].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig-001: Hermaphrodites evolved on three independent occasions in CaenorhabditisOnly species with sequenced genomes are shown. Androdioecious species with males and hermaphrodites are marked with a red symbol, and the others are male/female. The species in blue are able to interbreed and produce fertile offspring, and two outgroup species are orange. Modified from Kiontke et al. [18] and Felix et al. [15].
Mentions: Here, we review the evolution of self-fertility in Caenorhabditis nematodes. The convergent evolution of hermaphrodites in this genus provides an ideal way to explore both evolutionary change and the use of alternative reproductive strategies (reviewed in [5,6]). Phylogenetic analysis implies that mating systems changed recently, which makes it easier to reconstruct many of the underlying genetic events (Figure 1). Furthermore, technical considerations make this genus ideal for study. C. elegans is one of the leading models for studying sex-determination, and decades of research provide the background information needed to characterize its relatives. This task is simplified by the genome sequences of C. elegans [7] and C. briggsae [8], and the partial sequences of seven related species (Figure 1). Finally, orthologous genes can be characterized by powerful reverse genetic techniques, including RNA interference and gene-editing with transcription activator-like effector nucleases (TALENs) or clustered regularly interspaced short palindromic repeats (CRISPRs) [9-13], which allow the control of mating systems to be dissected in all species.

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