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Experimental insight into the proximate causes of male persistence variation among two strains of the androdioecious Caenorhabditis elegans (Nematoda).

Wegewitz V, Schulenburg H, Streit A - BMC Ecol. (2008)

Bottom Line: This is not the case in some other wild type isolates of C. elegans, among them the Hawaiian strain CB4856.We determined the kinetics of the loss of males over time for multiple population sizes and wild isolates and found significant differences.In particular, CB4856 males obtained a higher number of successful copulations than N2 males and sired correspondingly more cross-progeny.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany. viktoria.wegewitz@tuebingen.mpg.de

ABSTRACT

Background: In the androdioecious nematode Caenorhabditis elegans virtually all progeny produced by hermaphrodite self-fertilization is hermaphrodite while 50% of the progeny that results from cross-fertilization by a male is male. In the standard laboratory wild type strain N2 males disappear rapidly from populations. This is not the case in some other wild type isolates of C. elegans, among them the Hawaiian strain CB4856.

Results: We determined the kinetics of the loss of males over time for multiple population sizes and wild isolates and found significant differences. We performed systematic inter- and intra-strain crosses with N2 and CB4856 and show that the males and the hermaphrodites contribute to the difference in male maintenance between these two strains. In particular, CB4856 males obtained a higher number of successful copulations than N2 males and sired correspondingly more cross-progeny. On the other hand, N2 hermaphrodites produced a higher number of self-progeny, both when singly mated and when not mated.

Conclusion: These two differences have the potential to explain the observed variation in male persistence, since they should lead to a predominance of self-progeny (and thus hermaphrodites) in N2 and, at the same time, a high proportion of cross-progeny (and thus the presence of males as well as hermaphrodites) in CB4856.

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Offspring production by repeatedly mated hermaphrodites. A) Repeated mating of an individual hermaphrodite with a single virgin male every day. The hermaphrodite strain is indicated first and the male strain second. The number of cross-progeny (dark colors) and self-progeny (light colors) were determined. Each value is the average of five replicates. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 7]. Repeated mating of individual hermaphrodites with different numbers of virgin males added every day. The figure shows total progeny. Note that the proportion of self-progeny was low (see A) and did not differ significantly between treatments; thus, the observed variation is mainly determined by cross-progeny. Each value is the average of five hermaphrodites. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 8].
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Figure 4: Offspring production by repeatedly mated hermaphrodites. A) Repeated mating of an individual hermaphrodite with a single virgin male every day. The hermaphrodite strain is indicated first and the male strain second. The number of cross-progeny (dark colors) and self-progeny (light colors) were determined. Each value is the average of five replicates. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 7]. Repeated mating of individual hermaphrodites with different numbers of virgin males added every day. The figure shows total progeny. Note that the proportion of self-progeny was low (see A) and did not differ significantly between treatments; thus, the observed variation is mainly determined by cross-progeny. Each value is the average of five hermaphrodites. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 8].

Mentions: CB4856 males had significantly more successful copulations (Figure 2A and Table 1) and significantly more offspring than N2 males (Figure 2B and Table 1). These two traits were not significantly affected by the hermaphrodite strain used. Therefore, the difference in progeny production by males is most likely a consequence of the differences in mating rates. It does not seem to be caused by variations in the fertilization rates males achieve per successful mating event: The number of cross-progeny per mated hermaphrodite was not significantly affected by any factor of the model or the overall model as a whole (P > 0.05; Figure 2C and Table 1). At the same time, it is interesting to note that N2 males appear to produce more cross-progeny with N2 rather than CB4856 hermaphrodites (Fig. 2C; see also similar results obtained after repeated mating of hermaphrodites in Fig. 4A). This effect may account for the trend of a difference produced by the factor male strain in this context (Table 1). It is responsible for the significant interaction term, which was inferred for the data from the first two days (Table 2). One possible explanation for this result is a certain degree of genetic incompatibility, which only becomes visible in one type of cross between the two strains (male N2 and hermaphrodite CB4856) and which may be related to the recent report of genetic incompatibilities among different natural C. elegans isolates [33].


Experimental insight into the proximate causes of male persistence variation among two strains of the androdioecious Caenorhabditis elegans (Nematoda).

Wegewitz V, Schulenburg H, Streit A - BMC Ecol. (2008)

Offspring production by repeatedly mated hermaphrodites. A) Repeated mating of an individual hermaphrodite with a single virgin male every day. The hermaphrodite strain is indicated first and the male strain second. The number of cross-progeny (dark colors) and self-progeny (light colors) were determined. Each value is the average of five replicates. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 7]. Repeated mating of individual hermaphrodites with different numbers of virgin males added every day. The figure shows total progeny. Note that the proportion of self-progeny was low (see A) and did not differ significantly between treatments; thus, the observed variation is mainly determined by cross-progeny. Each value is the average of five hermaphrodites. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 8].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2483263&req=5

Figure 4: Offspring production by repeatedly mated hermaphrodites. A) Repeated mating of an individual hermaphrodite with a single virgin male every day. The hermaphrodite strain is indicated first and the male strain second. The number of cross-progeny (dark colors) and self-progeny (light colors) were determined. Each value is the average of five replicates. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 7]. Repeated mating of individual hermaphrodites with different numbers of virgin males added every day. The figure shows total progeny. Note that the proportion of self-progeny was low (see A) and did not differ significantly between treatments; thus, the observed variation is mainly determined by cross-progeny. Each value is the average of five hermaphrodites. The error bars represent standard errors. For exact numbers and statistical analysis [see additional file 8].
Mentions: CB4856 males had significantly more successful copulations (Figure 2A and Table 1) and significantly more offspring than N2 males (Figure 2B and Table 1). These two traits were not significantly affected by the hermaphrodite strain used. Therefore, the difference in progeny production by males is most likely a consequence of the differences in mating rates. It does not seem to be caused by variations in the fertilization rates males achieve per successful mating event: The number of cross-progeny per mated hermaphrodite was not significantly affected by any factor of the model or the overall model as a whole (P > 0.05; Figure 2C and Table 1). At the same time, it is interesting to note that N2 males appear to produce more cross-progeny with N2 rather than CB4856 hermaphrodites (Fig. 2C; see also similar results obtained after repeated mating of hermaphrodites in Fig. 4A). This effect may account for the trend of a difference produced by the factor male strain in this context (Table 1). It is responsible for the significant interaction term, which was inferred for the data from the first two days (Table 2). One possible explanation for this result is a certain degree of genetic incompatibility, which only becomes visible in one type of cross between the two strains (male N2 and hermaphrodite CB4856) and which may be related to the recent report of genetic incompatibilities among different natural C. elegans isolates [33].

Bottom Line: This is not the case in some other wild type isolates of C. elegans, among them the Hawaiian strain CB4856.We determined the kinetics of the loss of males over time for multiple population sizes and wild isolates and found significant differences.In particular, CB4856 males obtained a higher number of successful copulations than N2 males and sired correspondingly more cross-progeny.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany. viktoria.wegewitz@tuebingen.mpg.de

ABSTRACT

Background: In the androdioecious nematode Caenorhabditis elegans virtually all progeny produced by hermaphrodite self-fertilization is hermaphrodite while 50% of the progeny that results from cross-fertilization by a male is male. In the standard laboratory wild type strain N2 males disappear rapidly from populations. This is not the case in some other wild type isolates of C. elegans, among them the Hawaiian strain CB4856.

Results: We determined the kinetics of the loss of males over time for multiple population sizes and wild isolates and found significant differences. We performed systematic inter- and intra-strain crosses with N2 and CB4856 and show that the males and the hermaphrodites contribute to the difference in male maintenance between these two strains. In particular, CB4856 males obtained a higher number of successful copulations than N2 males and sired correspondingly more cross-progeny. On the other hand, N2 hermaphrodites produced a higher number of self-progeny, both when singly mated and when not mated.

Conclusion: These two differences have the potential to explain the observed variation in male persistence, since they should lead to a predominance of self-progeny (and thus hermaphrodites) in N2 and, at the same time, a high proportion of cross-progeny (and thus the presence of males as well as hermaphrodites) in CB4856.

Show MeSH
Related in: MedlinePlus