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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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Typical gamete production in female and male genotypes from all hybrid P. esculentus populations and offspring types arising from the nine potential mating combinations. Female LR can produce both diploid eggs and haploid eggs. Genotypes in grey boxes do not occur among the adults in the population although they are initially produced
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Fig1: Typical gamete production in female and male genotypes from all hybrid P. esculentus populations and offspring types arising from the nine potential mating combinations. Female LR can produce both diploid eggs and haploid eggs. Genotypes in grey boxes do not occur among the adults in the population although they are initially produced

Mentions: A third population type (EE-system) is represented by all-hybrid populations of P. esculentus. They dominate in the northern part of the distribution area, including our study area in southern Sweden; but they are also found in some areas of Central and Eastern Europe (reviewed by [35, 36]). These populations consist of diploid hybrids (genotype LR), plus one or two triploid forms (LLR and/or LRR); tetraploid LLRR hybrids are very rare exceptions that amounted to only 0.3 % of all sampled frogs [37]. While the formation of diploid and triploid hybrids is well understood [38–41], the absence of parental genotypes from these all-hybrid systems remains a puzzle. Based on the typical gamete production patterns in these populations, both LL and RR offspring are to be expected (Fig. 1); but despite of extensive sampling of 3165 frogs we have not found adults with these genotypes.Fig. 1


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)

Typical gamete production in female and male genotypes from all hybrid P. esculentus populations and offspring types arising from the nine potential mating combinations. Female LR can produce both diploid eggs and haploid eggs. Genotypes in grey boxes do not occur among the adults in the population although they are initially produced
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Typical gamete production in female and male genotypes from all hybrid P. esculentus populations and offspring types arising from the nine potential mating combinations. Female LR can produce both diploid eggs and haploid eggs. Genotypes in grey boxes do not occur among the adults in the population although they are initially produced
Mentions: A third population type (EE-system) is represented by all-hybrid populations of P. esculentus. They dominate in the northern part of the distribution area, including our study area in southern Sweden; but they are also found in some areas of Central and Eastern Europe (reviewed by [35, 36]). These populations consist of diploid hybrids (genotype LR), plus one or two triploid forms (LLR and/or LRR); tetraploid LLRR hybrids are very rare exceptions that amounted to only 0.3 % of all sampled frogs [37]. While the formation of diploid and triploid hybrids is well understood [38–41], the absence of parental genotypes from these all-hybrid systems remains a puzzle. Based on the typical gamete production patterns in these populations, both LL and RR offspring are to be expected (Fig. 1); but despite of extensive sampling of 3165 frogs we have not found adults with these genotypes.Fig. 1

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