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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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Average proportions (± SE) of different genotypes in natural ponds at four developmental stages: E = eggs, T = tadpoles, M = metamorphs, J = 1-year old juveniles A = adults. Grey bars represent the three hybrid types that are surviving and dominate among adults (LLR in a), LR in b) and LRR in c); the black bars show values for the parental species LL (a) and RR (c) that are gradually disappearing. In b) the stippled bars represent LLRR hybrids that are found among adults in low proportions, the hatched bars denote proportions of uncertain genotypes, i.e., those that could not unambiguously be identified in the microsatellite analysis (cf. Methods)
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Fig2: Average proportions (± SE) of different genotypes in natural ponds at four developmental stages: E = eggs, T = tadpoles, M = metamorphs, J = 1-year old juveniles A = adults. Grey bars represent the three hybrid types that are surviving and dominate among adults (LLR in a), LR in b) and LRR in c); the black bars show values for the parental species LL (a) and RR (c) that are gradually disappearing. In b) the stippled bars represent LLRR hybrids that are found among adults in low proportions, the hatched bars denote proportions of uncertain genotypes, i.e., those that could not unambiguously be identified in the microsatellite analysis (cf. Methods)

Mentions: At the fertilized egg stage, we found all offspring types that are to be expected from the gamete type combinations shown in Fig. 1. Only about half of the sample was comprised of the three genotypes that characterize all-hybrid populations (LR, LLR and LRR); the other half was made up by types that exist among adults only very rarely (LLRR hybrids and uncertain genotypes) or not at all, such as the parental forms (LL, LLL, RR and RRR) (Fig. 2). After the egg stage, the parental forms disappear almost completely through the tadpole to the metamorph and juvenile stages (Fig. 2a,c). Among metamorphs we found no LL and only one RR, while among juveniles the reverse was true. This decrease in parental genotypes is paralleled by an increase in the proportion of LR hybrids (Fig. 2b). The changes are reflected by significant effects of stage on proportions of LL, RR and LR (Table 1). Pairwise comparisons show that proportions in the egg stage differ significantly from those in the metamorph and juvenile stage for all three genotypes (all P ≤ 0.028), and for LR and RR also from those in the tadpole stage (both P ≤ 0.024). Proportions did not differ between tadpole, metamorph and juvenile stages for any of the three genotypes. For all other genotypes (LLR, LRR, LLRR and uncertain) proportions were not significantly affected by stage (Table 1); thus, they remained basically constant from eggs to juveniles. Already from the metamorph stage on, the genotype composition was almost identical to that found among juveniles and very similar to the average ratios found among adults in the same 12 study ponds over three consecutive years (2002–2004) (Fig. 2).Fig. 2


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)

Average proportions (± SE) of different genotypes in natural ponds at four developmental stages: E = eggs, T = tadpoles, M = metamorphs, J = 1-year old juveniles A = adults. Grey bars represent the three hybrid types that are surviving and dominate among adults (LLR in a), LR in b) and LRR in c); the black bars show values for the parental species LL (a) and RR (c) that are gradually disappearing. In b) the stippled bars represent LLRR hybrids that are found among adults in low proportions, the hatched bars denote proportions of uncertain genotypes, i.e., those that could not unambiguously be identified in the microsatellite analysis (cf. Methods)
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig2: Average proportions (± SE) of different genotypes in natural ponds at four developmental stages: E = eggs, T = tadpoles, M = metamorphs, J = 1-year old juveniles A = adults. Grey bars represent the three hybrid types that are surviving and dominate among adults (LLR in a), LR in b) and LRR in c); the black bars show values for the parental species LL (a) and RR (c) that are gradually disappearing. In b) the stippled bars represent LLRR hybrids that are found among adults in low proportions, the hatched bars denote proportions of uncertain genotypes, i.e., those that could not unambiguously be identified in the microsatellite analysis (cf. Methods)
Mentions: At the fertilized egg stage, we found all offspring types that are to be expected from the gamete type combinations shown in Fig. 1. Only about half of the sample was comprised of the three genotypes that characterize all-hybrid populations (LR, LLR and LRR); the other half was made up by types that exist among adults only very rarely (LLRR hybrids and uncertain genotypes) or not at all, such as the parental forms (LL, LLL, RR and RRR) (Fig. 2). After the egg stage, the parental forms disappear almost completely through the tadpole to the metamorph and juvenile stages (Fig. 2a,c). Among metamorphs we found no LL and only one RR, while among juveniles the reverse was true. This decrease in parental genotypes is paralleled by an increase in the proportion of LR hybrids (Fig. 2b). The changes are reflected by significant effects of stage on proportions of LL, RR and LR (Table 1). Pairwise comparisons show that proportions in the egg stage differ significantly from those in the metamorph and juvenile stage for all three genotypes (all P ≤ 0.028), and for LR and RR also from those in the tadpole stage (both P ≤ 0.024). Proportions did not differ between tadpole, metamorph and juvenile stages for any of the three genotypes. For all other genotypes (LLR, LRR, LLRR and uncertain) proportions were not significantly affected by stage (Table 1); thus, they remained basically constant from eggs to juveniles. Already from the metamorph stage on, the genotype composition was almost identical to that found among juveniles and very similar to the average ratios found among adults in the same 12 study ponds over three consecutive years (2002–2004) (Fig. 2).Fig. 2

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