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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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Related in: MedlinePlus

Survival in hybrid (grey) and parental (black) offspring. In (a) the time course of tadpole survival prior to metamorphosis is shown on a weekly basis for medium (circles) and low (triangles) food treatment. Survival under the high food treatment was measured only once after 9 weeks; the corresponding values for hybrid and parental offspring are indicated by grey and black stars, respectively. In (b) only survival of metamorphs emerging from the medium food treatment is shown, because tadpoles from the high and low food treatments were not reared beyond metamorphosis
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Fig6: Survival in hybrid (grey) and parental (black) offspring. In (a) the time course of tadpole survival prior to metamorphosis is shown on a weekly basis for medium (circles) and low (triangles) food treatment. Survival under the high food treatment was measured only once after 9 weeks; the corresponding values for hybrid and parental offspring are indicated by grey and black stars, respectively. In (b) only survival of metamorphs emerging from the medium food treatment is shown, because tadpoles from the high and low food treatments were not reared beyond metamorphosis

Mentions: While the high and low food treatments were terminated at the end of the larval period, tadpoles from the medium food treatment were raised through metamorphosis until July of the following year. During this period, the survival and development patterns found in tadpoles continued through the metamorph and juvenile stages (Fig. 6): at the end of the experiment, parental offspring had survived significantly worse (actually not at all) than hybrid offspring (Table 4b).Fig. 6


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)

Survival in hybrid (grey) and parental (black) offspring. In (a) the time course of tadpole survival prior to metamorphosis is shown on a weekly basis for medium (circles) and low (triangles) food treatment. Survival under the high food treatment was measured only once after 9 weeks; the corresponding values for hybrid and parental offspring are indicated by grey and black stars, respectively. In (b) only survival of metamorphs emerging from the medium food treatment is shown, because tadpoles from the high and low food treatments were not reared beyond metamorphosis
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Survival in hybrid (grey) and parental (black) offspring. In (a) the time course of tadpole survival prior to metamorphosis is shown on a weekly basis for medium (circles) and low (triangles) food treatment. Survival under the high food treatment was measured only once after 9 weeks; the corresponding values for hybrid and parental offspring are indicated by grey and black stars, respectively. In (b) only survival of metamorphs emerging from the medium food treatment is shown, because tadpoles from the high and low food treatments were not reared beyond metamorphosis
Mentions: While the high and low food treatments were terminated at the end of the larval period, tadpoles from the medium food treatment were raised through metamorphosis until July of the following year. During this period, the survival and development patterns found in tadpoles continued through the metamorph and juvenile stages (Fig. 6): at the end of the experiment, parental offspring had survived significantly worse (actually not at all) than hybrid offspring (Table 4b).Fig. 6

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