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Post-zygotic selection against parental genotypes during larval development maintains all-hybrid populations of the frog Pelophylax esculentus.

Reyer HU, Arioli-Jakob C, Arioli M - BMC Evol. Biol. (2015)

Bottom Line: In both parts of the study, we found numerous LL and RR offspring during the egg and early larval stages; but the frequency of these parental genotypes decreased drastically during later stages.From the combined results we conclude that the absence of parental genotypes in all-hybrid populations is due to post-zygotic selection against them, rather than to pre-zygotic mechanisms that might prevent their formation in the first place.For this post-zygotic selection, genetic mechanisms resulting from low genetic diversity and fixation of deleterious mutations seem to be a more likely explanation than ecological factors.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland. uli.reyer@ieu.uzh.ch.

ABSTRACT

Background: Hybridization between two species usually leads to inviable or infertile offspring, due to endogenous or exogenous selection pressures. Yet, hybrid taxa are found in several plant and animal genera, and some of these hybrid taxa are ecologically and evolutionarily very successful. One example of such a successful hybrid is the water frog, Pelophylax esculentus which originated from matings between the two species P. ridibundus (genotype RR) and P. lessonae (LL). At the northern border of the distribution all-hybrid populations consisting of diploid (LR) and one or two triploid (LLR, LRR) frog types have been established. Here, the hybrid has achieved reproductive independence from its sexual ancestors and forms a self-sustaining evolutionary unit. Based on the gamete production of these hybrids, certain mating combinations should lead to LL and RR offspring, but these parental forms are absent among the adults.

Results: In order to investigate the mechanisms that maintain such an all-hybrid system, we performed a field study and a crossing experiment. In the field we sampled several ponds for water frog larvae at different developmental stages. Genotype compositions were then analysed and life-history differences between the genotypes examined. In the experiment we crossed diploid and triploid males and females from different ponds and determined fertilization success as well as development speed and survival rates of the offspring under high, medium and low food availability. In both parts of the study, we found numerous LL and RR offspring during the egg and early larval stages; but the frequency of these parental genotypes decreased drastically during later stages. In natural ponds almost all of them had disappeared already before metamorphosis; under the more benign experimental conditions the last ones died as juveniles during the following year.

Conclusions: From the combined results we conclude that the absence of parental genotypes in all-hybrid populations is due to post-zygotic selection against them, rather than to pre-zygotic mechanisms that might prevent their formation in the first place. For this post-zygotic selection, genetic mechanisms resulting from low genetic diversity and fixation of deleterious mutations seem to be a more likely explanation than ecological factors.

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Mating combinations resulting from the experimental crossing design with frogs from three ponds. We included three different individuals per genotype and cross in the experiment with the exception of pond 011, where only one LLR female was caught and one LR individual was initially falsely categorized as a LLR. A total of 120 crossings was carried out. Shaded areas are crosses done within a pond, white areas are crosses done between ponds
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Fig7: Mating combinations resulting from the experimental crossing design with frogs from three ponds. We included three different individuals per genotype and cross in the experiment with the exception of pond 011, where only one LLR female was caught and one LR individual was initially falsely categorized as a LLR. A total of 120 crossings was carried out. Shaded areas are crosses done within a pond, white areas are crosses done between ponds

Mentions: Crosses were performed using the artificial fertilization procedure described in detail by [101]. From each of the three ponds we used three males and three females of each available genotype, with the exceptions of pond 011. Here one of the two originally supposed LLR females turned out to be an LR after final genotype analyses, leaving us with only one LLR but four LR females from this pond (Fig. 7). We used only females that were obviously carrying eggs, which was determined according to [102]. Each individual of one sex was crossed with each possible genotype of the other sex within and between ponds. This yielded 120 crossings in the 42 different mating combinations shown in Fig. 7. All crossings were done on the same day. Freshly fertilized eggs were kept in petri dishes filled with filtered pond water. Fertilization success per cross was determined as the proportion of eggs per petri dish that had rotated their black animal hemisphere to the top [101, 103].Fig. 7


Post-zygotic selection against parental genotypes during larval development maintains all-hybrid populations of the frog Pelophylax esculentus.

Reyer HU, Arioli-Jakob C, Arioli M - BMC Evol. Biol. (2015)

Mating combinations resulting from the experimental crossing design with frogs from three ponds. We included three different individuals per genotype and cross in the experiment with the exception of pond 011, where only one LLR female was caught and one LR individual was initially falsely categorized as a LLR. A total of 120 crossings was carried out. Shaded areas are crosses done within a pond, white areas are crosses done between ponds
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4491251&req=5

Fig7: Mating combinations resulting from the experimental crossing design with frogs from three ponds. We included three different individuals per genotype and cross in the experiment with the exception of pond 011, where only one LLR female was caught and one LR individual was initially falsely categorized as a LLR. A total of 120 crossings was carried out. Shaded areas are crosses done within a pond, white areas are crosses done between ponds
Mentions: Crosses were performed using the artificial fertilization procedure described in detail by [101]. From each of the three ponds we used three males and three females of each available genotype, with the exceptions of pond 011. Here one of the two originally supposed LLR females turned out to be an LR after final genotype analyses, leaving us with only one LLR but four LR females from this pond (Fig. 7). We used only females that were obviously carrying eggs, which was determined according to [102]. Each individual of one sex was crossed with each possible genotype of the other sex within and between ponds. This yielded 120 crossings in the 42 different mating combinations shown in Fig. 7. All crossings were done on the same day. Freshly fertilized eggs were kept in petri dishes filled with filtered pond water. Fertilization success per cross was determined as the proportion of eggs per petri dish that had rotated their black animal hemisphere to the top [101, 103].Fig. 7

Bottom Line: In both parts of the study, we found numerous LL and RR offspring during the egg and early larval stages; but the frequency of these parental genotypes decreased drastically during later stages.From the combined results we conclude that the absence of parental genotypes in all-hybrid populations is due to post-zygotic selection against them, rather than to pre-zygotic mechanisms that might prevent their formation in the first place.For this post-zygotic selection, genetic mechanisms resulting from low genetic diversity and fixation of deleterious mutations seem to be a more likely explanation than ecological factors.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland. uli.reyer@ieu.uzh.ch.

ABSTRACT

Background: Hybridization between two species usually leads to inviable or infertile offspring, due to endogenous or exogenous selection pressures. Yet, hybrid taxa are found in several plant and animal genera, and some of these hybrid taxa are ecologically and evolutionarily very successful. One example of such a successful hybrid is the water frog, Pelophylax esculentus which originated from matings between the two species P. ridibundus (genotype RR) and P. lessonae (LL). At the northern border of the distribution all-hybrid populations consisting of diploid (LR) and one or two triploid (LLR, LRR) frog types have been established. Here, the hybrid has achieved reproductive independence from its sexual ancestors and forms a self-sustaining evolutionary unit. Based on the gamete production of these hybrids, certain mating combinations should lead to LL and RR offspring, but these parental forms are absent among the adults.

Results: In order to investigate the mechanisms that maintain such an all-hybrid system, we performed a field study and a crossing experiment. In the field we sampled several ponds for water frog larvae at different developmental stages. Genotype compositions were then analysed and life-history differences between the genotypes examined. In the experiment we crossed diploid and triploid males and females from different ponds and determined fertilization success as well as development speed and survival rates of the offspring under high, medium and low food availability. In both parts of the study, we found numerous LL and RR offspring during the egg and early larval stages; but the frequency of these parental genotypes decreased drastically during later stages. In natural ponds almost all of them had disappeared already before metamorphosis; under the more benign experimental conditions the last ones died as juveniles during the following year.

Conclusions: From the combined results we conclude that the absence of parental genotypes in all-hybrid populations is due to post-zygotic selection against them, rather than to pre-zygotic mechanisms that might prevent their formation in the first place. For this post-zygotic selection, genetic mechanisms resulting from low genetic diversity and fixation of deleterious mutations seem to be a more likely explanation than ecological factors.

Show MeSH
Related in: MedlinePlus