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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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Means in fertilization success and hatching rate for the different genotypes of females and males listed per pond. Error bars represent ±1 SE
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Fig4: Means in fertilization success and hatching rate for the different genotypes of females and males listed per pond. Error bars represent ±1 SE

Mentions: Female genotypes did not significantly differ in either fertilization success or hatching rate (Table 3, Fig. 4). On average, 66 % of all eggs were fertilized and 40 % of those developed into hatchlings. Male reproductive success, however, showed clear differences between genotypes and pond of origin. Triploid males of both types (LLR and LRR) had fairly high average fertilization success and hatching rates of their offspring, whereas for diploid LR males the values were significantly lower, with marked differences between the three ponds of origin (Fig. 4). The very low fertilization rate by sperm of LR males from pond 001 (8 %) and the poor hatching rate of their offspring (19 %) translated into only very few surviving tadpoles from crossings involving these males. The interaction between male and female genotype and the crossing type had no significant influence on fertilization success and hatching rate, indicating that initial reproductive success did not depend on which parental genotypes were crossed and whether mothers and fathers came from the same or from different ponds. Since the effect of differing pond origin might be most severe in the homotypic offspring genotypes LL or RR where deleterious mutations in homozygous (same clone) or heterozygous states (different clones) are not countered by the influence of another genome, we also tested for only these two genotypes if crossing type is influencing reproductive success in early life stages; but there were no significant differences in fertilization or hatching rate (tfertilization = 0.04, P = 0.966; thatching = 0.33, P = 0.741).Table 3


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)

Means in fertilization success and hatching rate for the different genotypes of females and males listed per pond. Error bars represent ±1 SE
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Means in fertilization success and hatching rate for the different genotypes of females and males listed per pond. Error bars represent ±1 SE
Mentions: Female genotypes did not significantly differ in either fertilization success or hatching rate (Table 3, Fig. 4). On average, 66 % of all eggs were fertilized and 40 % of those developed into hatchlings. Male reproductive success, however, showed clear differences between genotypes and pond of origin. Triploid males of both types (LLR and LRR) had fairly high average fertilization success and hatching rates of their offspring, whereas for diploid LR males the values were significantly lower, with marked differences between the three ponds of origin (Fig. 4). The very low fertilization rate by sperm of LR males from pond 001 (8 %) and the poor hatching rate of their offspring (19 %) translated into only very few surviving tadpoles from crossings involving these males. The interaction between male and female genotype and the crossing type had no significant influence on fertilization success and hatching rate, indicating that initial reproductive success did not depend on which parental genotypes were crossed and whether mothers and fathers came from the same or from different ponds. Since the effect of differing pond origin might be most severe in the homotypic offspring genotypes LL or RR where deleterious mutations in homozygous (same clone) or heterozygous states (different clones) are not countered by the influence of another genome, we also tested for only these two genotypes if crossing type is influencing reproductive success in early life stages; but there were no significant differences in fertilization or hatching rate (tfertilization = 0.04, P = 0.966; thatching = 0.33, P = 0.741).Table 3

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