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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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Survival (bars) and developmental stage according to [97] until beginning metamorphosis (black lines) of (a) different offspring types and (b) in relation to food treatment. Shown are means ± 1 SE
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Fig5: Survival (bars) and developmental stage according to [97] until beginning metamorphosis (black lines) of (a) different offspring types and (b) in relation to food treatment. Shown are means ± 1 SE

Mentions: Due to the production of unusual and multiple gamete types by some males and females (Fig. 3) the progeny from some crosses was composed of different offspring types. Since larval survival was measured per tub, and tubs corresponded to crosses, potential differences in offspring survival and development were analyzed only for those tubs that contained one single genotype. Tadpole survival and development were both significantly affected by offspring type and food treatment (Table 4a, Fig. 5a). Pairwise comparisons showed that both parental genotypes survived significantly worse than the three hybrid genotypes (all P < 0.001), whereas there were no differences in comparisons between LL and RR and LLR, LR and LRR, respectively (all P = 1.000). Survival increased with the amount of available food (Fig. 5b), being significantly higher in the high food than in the medium and low food treatment (both P < 0.001) and a tendency for better survival under medium than under low food (P = 0.099). Among those tadpoles that did survive, differences in development paralleled those in survival: tadpoles of the three hybrid types developed faster (indicated by higher Gosner stages) than those of the two parental types (Fig. 5a) and those under better food conditions (high and medium) developed faster than those in the low food treatment (Fig. 5b). For both, survival and development, there was no significant interaction between offspring type and food treatment (although for development there was a tendency); and crossing type also had no effect (Table 4a). This indicates that the response to food conditions does not differ between offspring types and is independent of whether the crossed males and females come from the same or from different ponds.Table 4


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 (bars) and developmental stage according to [97] until beginning metamorphosis (black lines) of (a) different offspring types and (b) in relation to food treatment. Shown are means ± 1 SE
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Survival (bars) and developmental stage according to [97] until beginning metamorphosis (black lines) of (a) different offspring types and (b) in relation to food treatment. Shown are means ± 1 SE
Mentions: Due to the production of unusual and multiple gamete types by some males and females (Fig. 3) the progeny from some crosses was composed of different offspring types. Since larval survival was measured per tub, and tubs corresponded to crosses, potential differences in offspring survival and development were analyzed only for those tubs that contained one single genotype. Tadpole survival and development were both significantly affected by offspring type and food treatment (Table 4a, Fig. 5a). Pairwise comparisons showed that both parental genotypes survived significantly worse than the three hybrid genotypes (all P < 0.001), whereas there were no differences in comparisons between LL and RR and LLR, LR and LRR, respectively (all P = 1.000). Survival increased with the amount of available food (Fig. 5b), being significantly higher in the high food than in the medium and low food treatment (both P < 0.001) and a tendency for better survival under medium than under low food (P = 0.099). Among those tadpoles that did survive, differences in development paralleled those in survival: tadpoles of the three hybrid types developed faster (indicated by higher Gosner stages) than those of the two parental types (Fig. 5a) and those under better food conditions (high and medium) developed faster than those in the low food treatment (Fig. 5b). For both, survival and development, there was no significant interaction between offspring type and food treatment (although for development there was a tendency); and crossing type also had no effect (Table 4a). This indicates that the response to food conditions does not differ between offspring types and is independent of whether the crossed males and females come from the same or from different ponds.Table 4

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