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Coexistence of diploid and triploid hybrid water frogs: population differences persist in the apparent absence of differential survival.

Christiansen DG, Jakob C, Arioli M, Roethlisberger S, Reyer HU - BMC Ecol. (2010)

Bottom Line: As the relative survival and proportion of LLR, LR and LRR did not correlate within ponds, this study provided no evidence for the selection hypothesis in adults.The result was a weak preference for the gamete pattern hypothesis.Moreover, the study provided valuable data on genotype-specific body lengths, adult survival and sex ratios.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, Zurich, Switzerland. ditte.christiansen@ieu.uzh.ch

ABSTRACT

Unlabelled: The role of differential selection in determining the geographic distribution of genotypes in hybrid systems has long been discussed, but not settled. The present study aims to asses the importance of selection in structuring all-hybrid Pelophylax esculentus populations. These populations, in which the parental species (P. lessonae with genotype LL and P. ridibundus with genotype RR) are absent, have pond-specific proportions of diploid (LR) and triploid (LLR and LRR) genotypes.

Results: With data from 12 Swedish ponds, we first show that in spite of significant changes in genotype proportions over time, the most extreme ponds retained their differences over a six year study period. The uneven distribution of genotypes among ponds could be a consequence of differential selection varying among ponds (selection hypothesis), or, alternatively, of different gamete production patterns among ponds (gamete pattern hypothesis). The selection hypothesis was tested in adults by a six year mark-recapture study in all 12 ponds. As the relative survival and proportion of LLR, LR and LRR did not correlate within ponds, this study provided no evidence for the selection hypothesis in adults. Then, both hypotheses were tested simultaneously in juvenile stages (eggs, tadpoles, metamorphs and one year old froglets) in three of the ponds. A gradual approach to adult genotype proportions through successive stages would support the selection hypotheses, whereas the presence of adult genotype proportions already at the egg stage would support the gamete pattern hypothesis. The result was a weak preference for the gamete pattern hypothesis.

Conclusions: These results thus suggest that selection is of little importance for shaping genotype distributions of all-hybrid populations of P. esculentus, but further studies are needed for confirmation. Moreover, the study provided valuable data on genotype-specific body lengths, adult survival and sex ratios.

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Simplified illustration of gamete production and population maintenance of all-hybrid P. esculentus populations. Note that the frogs mostly produce offspring with genotypes different from their own. LL and RR die before sexual maturity; LRR males (and LLRR frogs) are formed rarely, because LR sperm (as opposed to LR eggs) is rare.
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Figure 1: Simplified illustration of gamete production and population maintenance of all-hybrid P. esculentus populations. Note that the frogs mostly produce offspring with genotypes different from their own. LL and RR die before sexual maturity; LRR males (and LLRR frogs) are formed rarely, because LR sperm (as opposed to LR eggs) is rare.

Mentions: The hybrids reproduce by hybridogenesis, which implies that genetic recombination does normally not take place between L and R genomes in hybrids. Instead, gametes contain one or the other genome, or both, but not a mixture. Hybrids are thus formed anew every generation by the fusion of two gametes with different genomic contents. In the all-hybrid populations of Southern Sweden that were investigated in this study, LLR frogs of both sexes make mostly L gametes (LLR females also make low proportions of LL eggs), LRR of both sexes make R gametes, LR females make LR and some R eggs while LR males make R and rarely also LR or L sperm (Figure 1, [7,8,14]). When two L or two R gametes combine, offspring with parental species genotypes (LL and RR) arise, but under natural conditions they die before sexual maturity [8,10]. Sex determination is an XX-XY system with a male-determining Y factor located in one L genome in males [14]. As a consequence, LRR males are rare, except in ponds with high frequencies of LR sperm [14]. Tetraploids are also rare [7]. The remaining five hybrid genotypes, LLR and LR males, LLR, LR and LRR females, are frequent in almost all ponds [7].


Coexistence of diploid and triploid hybrid water frogs: population differences persist in the apparent absence of differential survival.

Christiansen DG, Jakob C, Arioli M, Roethlisberger S, Reyer HU - BMC Ecol. (2010)

Simplified illustration of gamete production and population maintenance of all-hybrid P. esculentus populations. Note that the frogs mostly produce offspring with genotypes different from their own. LL and RR die before sexual maturity; LRR males (and LLRR frogs) are formed rarely, because LR sperm (as opposed to LR eggs) is rare.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2902419&req=5

Figure 1: Simplified illustration of gamete production and population maintenance of all-hybrid P. esculentus populations. Note that the frogs mostly produce offspring with genotypes different from their own. LL and RR die before sexual maturity; LRR males (and LLRR frogs) are formed rarely, because LR sperm (as opposed to LR eggs) is rare.
Mentions: The hybrids reproduce by hybridogenesis, which implies that genetic recombination does normally not take place between L and R genomes in hybrids. Instead, gametes contain one or the other genome, or both, but not a mixture. Hybrids are thus formed anew every generation by the fusion of two gametes with different genomic contents. In the all-hybrid populations of Southern Sweden that were investigated in this study, LLR frogs of both sexes make mostly L gametes (LLR females also make low proportions of LL eggs), LRR of both sexes make R gametes, LR females make LR and some R eggs while LR males make R and rarely also LR or L sperm (Figure 1, [7,8,14]). When two L or two R gametes combine, offspring with parental species genotypes (LL and RR) arise, but under natural conditions they die before sexual maturity [8,10]. Sex determination is an XX-XY system with a male-determining Y factor located in one L genome in males [14]. As a consequence, LRR males are rare, except in ponds with high frequencies of LR sperm [14]. Tetraploids are also rare [7]. The remaining five hybrid genotypes, LLR and LR males, LLR, LR and LRR females, are frequent in almost all ponds [7].

Bottom Line: As the relative survival and proportion of LLR, LR and LRR did not correlate within ponds, this study provided no evidence for the selection hypothesis in adults.The result was a weak preference for the gamete pattern hypothesis.Moreover, the study provided valuable data on genotype-specific body lengths, adult survival and sex ratios.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, Zurich, Switzerland. ditte.christiansen@ieu.uzh.ch

ABSTRACT

Unlabelled: The role of differential selection in determining the geographic distribution of genotypes in hybrid systems has long been discussed, but not settled. The present study aims to asses the importance of selection in structuring all-hybrid Pelophylax esculentus populations. These populations, in which the parental species (P. lessonae with genotype LL and P. ridibundus with genotype RR) are absent, have pond-specific proportions of diploid (LR) and triploid (LLR and LRR) genotypes.

Results: With data from 12 Swedish ponds, we first show that in spite of significant changes in genotype proportions over time, the most extreme ponds retained their differences over a six year study period. The uneven distribution of genotypes among ponds could be a consequence of differential selection varying among ponds (selection hypothesis), or, alternatively, of different gamete production patterns among ponds (gamete pattern hypothesis). The selection hypothesis was tested in adults by a six year mark-recapture study in all 12 ponds. As the relative survival and proportion of LLR, LR and LRR did not correlate within ponds, this study provided no evidence for the selection hypothesis in adults. Then, both hypotheses were tested simultaneously in juvenile stages (eggs, tadpoles, metamorphs and one year old froglets) in three of the ponds. A gradual approach to adult genotype proportions through successive stages would support the selection hypotheses, whereas the presence of adult genotype proportions already at the egg stage would support the gamete pattern hypothesis. The result was a weak preference for the gamete pattern hypothesis.

Conclusions: These results thus suggest that selection is of little importance for shaping genotype distributions of all-hybrid populations of P. esculentus, but further studies are needed for confirmation. Moreover, the study provided valuable data on genotype-specific body lengths, adult survival and sex ratios.

Show MeSH