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Diploid males and their triploid offspring in the paper wasp Polistes dominulus.

ABSTRACT: Although the hymenopteran sex-determining mechanism generally results in haploid males and diploid females, diploid males can be produced via homozygosity at the sex-determining locus. Diploid males have low fitness because they are effectively sterile or produce presumably sterile triploid offspring. Previously, triploid females were observed in three species of North American Polistes paper wasps, and this was interpreted as indirect evidence of diploid males. Here we report what is, to our knowledge, the first direct evidence: four of five early male-producing Polistes dominulus nests from three populations contained diploid males. Because haploid males were also found, however, the adaptive value of early males cannot be ignored. Using genetic and morphological data from triploid females, we also present evidence that both diploid males and triploid females remain undetected throughout the colony cycle. Consequently, diploid male production may result in a delayed fitness cost for two generations. This phenomenon is particularly relevant for introduced populations with few alleles at the sex-determining locus, but cannot be ignored in native populations without supporting genetic data. Future research using paper wasp populations to test theories of social evolution should explicitly consider the potential impacts of diploid males.

SUBMITTER: Liebert AE

PROVIDER: S-EPMC1626210 | biostudies-literature | 2005 Jun

REPOSITORIES: biostudies-literature

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Diploid males and their triploid offspring in the paper wasp Polistes dominulus.

Liebert Aviva E AE Sumana Annagiri A Starks Philip T PT

Biology letters 20050601 2

Although the hymenopteran sex-determining mechanism generally results in haploid males and diploid females, diploid males can be produced via homozygosity at the sex-determining locus. Diploid males have low fitness because they are effectively sterile or produce presumably sterile triploid offspring. Previously, triploid females were observed in three species of North American Polistes paper wasps, and this was interpreted as indirect evidence of diploid males. Here we report what is, to our kn ...[more]

PMID: 17148166

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Project description:BACKGROUND:Polyploidy is widespread in animals and especially in plants. Different kinds of ploidies exist, for example, hexaploidy in wheat, octaploidy in strawberries, and diploidy, triploidy, tetraploidy, and pseudo-tetraploidy (partly tetraploid) in fish. Triploid offspring from diploid parents occur frequently in the wild in Atlantic salmon (Salmo salar) and, as with triploidy in general, the triploid individuals are sterile. Induced triploidy in Atlantic salmon is common practice to produce sterile fish. In Norwegian aquaculture, production of sterile triploid fish is an attempt by government and industry to limit genetic introgression between wild and farmed fish. However, triploid fish may have traits and properties that differ from those of diploids. Investigating the genetics behind traits in triploids has proved challenging because genotype calling of genetic markers in triploids is not supported by standard software. Our aim was to develop a method that can be used for genotype calling of genetic markers in triploid individuals. RESULTS:Allele signals were produced for 381 triploid Atlantic salmon offspring using a 56 K Thermo Fisher GeneTitan genotyping platform. Genotypes were successfully called by applying finite normal mixture models to the (transformed) allele signals. Subsets of markers were filtered by quality control statistics for use with downstream analyses. The quality of the called genotypes was sufficient to allow for assignment of diploid parents to the triploid offspring and to discriminate between maternal and paternal parents from autosomal inheritance patterns. In addition, as the maternal inheritance in triploid offspring is identical to gynogenetic inheritance, the maternal recombination pattern for each chromosome could be mapped by using a similar approach as that used in gene-centromere mapping. CONCLUSIONS:We show that calling of dense marker genotypes for triploid individuals is feasible. The resulting genotypes can be used in parentage assignment of triploid offspring to diploid parents, to discriminate between maternal and paternal parents using autosomal inheritance patterns, and to map the maternal recombination pattern using an approach similar to gene-centromere mapping. Genotyping of triploid individuals is important both for selective breeding programs and unravelling the underlying genetics of phenotypes recorded in triploids. In principle, the developed method can be used for genotype calling of other polyploid organisms.

Project description:In cooperative breeders, subordinates that have alternative reproductive options are expected to stay and help dominant breeders only as long as they contribute to group productivity, if their fitness is linked with colony success. Female Polistes dominula paper wasps live as cooperative breeders in small groups of typically fewer than 10 females. Subordinates tend to have high-quality outside options, and so could choose alternative breeding tactics if their work efforts increased productivity negligibly. In the founding stage before workers emerge, we tested the effect of various predictors on nest growth, as a proxy for group productivity, and explored the shape of the relationship between group size and nest growth. We found group size to be the only significant predictor of nest growth: variation among body sizes within the group showed no effect, suggesting a lack of size-dependent task specialization in this species. Average body size and average genetic relatedness between group members similarly showed no effects on nest growth. Group size had a non-linear effect so that per-capita benefits to nest growth decreased in larger groups, and groups of 10 or more would benefit negligibly from additional group members. Hence, females might be better off pursuing other options than joining a large group. This finding helps to explain why P. dominula groups are usually relatively small in our study population. Further studies may illuminate the mechanisms behind the smaller per-capita nest growth that we found in larger groups.Identifying which factors influence the productivity of animal groups is key to understanding why different species breed cooperatively in groups of varying sizes. In the paper wasp Polistes dominula, we investigated the growth rate of nests as a measure of group productivity. We found that average body size, the variation in body sizes within the group, and average genetic relatedness between group members did not affect nest growth, while group size had a strong, positive effect: nests grew faster with more group members, but the per-capita benefit decreased in larger groups. The addition of extra group members in groups of 10 or more had negligible effects on nest growth. Hence, wasps may be better off pursuing other options than joining large groups. This finding helps to explain why groups normally consist of fewer than 10 wasps in this population.

Dataset Information

Diploid males and their triploid offspring in the paper wasp Polistes dominulus.

Publications

Diploid males and their triploid offspring in the paper wasp Polistes dominulus.

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