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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 of gamete types produced by the crossed male and female hybrids
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Fig3: Average proportions of gamete types produced by the crossed male and female hybrids

Mentions: The gamete types produced by the crossed adults basically confirmed the pattern found in previous studies of all-hybrid populations (Fig. 3): triploid individuals produced haploid gametes with the genome that they carried in two copies (i.e., L in LLR and R in LRR). In males, this was 100 % true for all six LLR and all three LRR and in females for one of four LLR and four of six LRR. The other three LLR females produced a few diploid LL eggs (2.6 – 10.7 %), while one of the six LRR females produced a few diploid RR eggs (4.3 %) and the other one a few LR eggs (3.6 %). In diploid individuals gamete production was more variable (Fig. 3). Four out of 10 females and five out of nine males produced exclusively the gamete types that according to a previous investigation were known to be most frequent in LR hybrids from our study area [40], i.e., LR eggs and R sperm, respectively. The other six LR females produced also haploid R eggs in a frequency ranging from 2.8 to 48.8 %, while the other four LR males showed very diverse gamete ratios. In three of them the expected haploid R sperm amounted to 28.0–89.3 % and the additionally produced diploid LR sperm to 10.7–48.0 %. Two of these males also produced gametes of a third type, namely 10.0–24.0 % haploid L sperm. The fourth unusual LR male had an extremely low fertilization success resulting in only two larvae (one sired by an L and the other by an R sperm), which does not allow a reliable conclusion about the gamete production of this male. Interestingly, all three LR males that produced both haploid L and R sperm came from the same pond (001). As a result of this production of unusual gametes in some males and females, some crosses not only produced the five common and expected offspring types (LR, LLR, LRR, LL and RR); we also found a few rare ones, namely 13 tetraploid LLRR, two LLL and one tadpole each with the genotypes RRR, LLLR and LRRR.Fig. 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)

Average proportions of gamete types produced by the crossed male and female hybrids
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig3: Average proportions of gamete types produced by the crossed male and female hybrids
Mentions: The gamete types produced by the crossed adults basically confirmed the pattern found in previous studies of all-hybrid populations (Fig. 3): triploid individuals produced haploid gametes with the genome that they carried in two copies (i.e., L in LLR and R in LRR). In males, this was 100 % true for all six LLR and all three LRR and in females for one of four LLR and four of six LRR. The other three LLR females produced a few diploid LL eggs (2.6 – 10.7 %), while one of the six LRR females produced a few diploid RR eggs (4.3 %) and the other one a few LR eggs (3.6 %). In diploid individuals gamete production was more variable (Fig. 3). Four out of 10 females and five out of nine males produced exclusively the gamete types that according to a previous investigation were known to be most frequent in LR hybrids from our study area [40], i.e., LR eggs and R sperm, respectively. The other six LR females produced also haploid R eggs in a frequency ranging from 2.8 to 48.8 %, while the other four LR males showed very diverse gamete ratios. In three of them the expected haploid R sperm amounted to 28.0–89.3 % and the additionally produced diploid LR sperm to 10.7–48.0 %. Two of these males also produced gametes of a third type, namely 10.0–24.0 % haploid L sperm. The fourth unusual LR male had an extremely low fertilization success resulting in only two larvae (one sired by an L and the other by an R sperm), which does not allow a reliable conclusion about the gamete production of this male. Interestingly, all three LR males that produced both haploid L and R sperm came from the same pond (001). As a result of this production of unusual gametes in some males and females, some crosses not only produced the five common and expected offspring types (LR, LLR, LRR, LL and RR); we also found a few rare ones, namely 13 tetraploid LLRR, two LLL and one tadpole each with the genotypes RRR, LLLR and LRRR.Fig. 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