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Higher rate of tissue regeneration in polyploid asexual versus diploid sexual freshwater snails.

ABSTRACT: Characterizing phenotypic differences between sexual and asexual organisms is a critical step towards understanding why sexual reproduction is so common. Because asexuals are often polyploid, understanding how ploidy influences phenotype is directly relevant to the study of sex and will provide key insights into the evolution of ploidy-level variation. The well-established association between genome size and cell cycle duration, evidence for a link between genome size and tissue regeneration rate and the growing body of research showing that ploidy influences growth rate and gene expression led us to hypothesize that healing and tissue regeneration might be affected by ploidy-level variation. We evaluated this hypothesis by measuring the rate of regeneration of antenna tissue of Potamopyrgus antipodarum, a New Zealand snail characterized by frequent coexistence between diploid sexuals and polyploid asexuals. Antennae of triploid and presumptive tetraploid asexuals regenerated more rapidly than the antennae of diploid sexuals, but regeneration rate did not differ between triploids and tetraploids. These results suggest either that ploidy elevation has nonlinear positive effects on tissue regeneration and/or that factors associated directly with reproductive mode affect regeneration rate more than ploidy level. The results of this study also indicate that the lower ploidy of sexual P. antipodarum is unlikely to confer advantages associated with more rapid regeneration.

SUBMITTER: Krois NR

PROVIDER: S-EPMC3730654 | biostudies-literature | 2013 Aug

REPOSITORIES: biostudies-literature

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Higher rate of tissue regeneration in polyploid asexual versus diploid sexual freshwater snails.

Krois Nicole R NR Cherukuri Anvesh A Puttagunta Nikhil N Neiman Maurine M

Biology letters 20130710 4

Characterizing phenotypic differences between sexual and asexual organisms is a critical step towards understanding why sexual reproduction is so common. Because asexuals are often polyploid, understanding how ploidy influences phenotype is directly relevant to the study of sex and will provide key insights into the evolution of ploidy-level variation. The well-established association between genome size and cell cycle duration, evidence for a link between genome size and tissue regeneration rat ...[more]

PMID: 23843218

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Project description:Background and Aims:In Central Europe Hypericum perforatum and Hypericum maculatum show significant hybridization and introgression as a consequence of Pleistocene range fluctuations, and their gene pools are merging on higher ploidy levels. This paper discusses whether polyploid hybrid gene pools are trapped in the ecological climatic niche space of their diploid ancestors, and tests the idea of geographical parthenogenesis. Methods:DNA sequence information of nuclear ribosomal DNA and plastid loci, ploidy level estimates and ecological niche modelling are used to characterize the various diploid and polyploid gene pools and unravel spatio-temporal patterns of gene flow among them. Key Results:On the diploid level, the three gene pools are clearly distinct between and within species of H. perforatum (two gene pools) and H. maculatum, and their divergence dates back to the first half of the Pleistocene. All polyploids in Central Europe show high levels of past and contemporary gene flow between all three gene pools. The correlation of genetic and geographical distances breaks down if the latter is larger than 250 km, indicating recent and ongoing gene flow. The two species are ecologically differentiated, but in particular hybrids among all three gene pools do not show significant niche differences compared to their parental gene pools, except for some combinations with H. maculatum. Conclusions:Inter- and intraspecific gene flow between inter- and intra-species gene pools is limited on the diploid level, and the geographical distribution of the diploids largely reflects Pleistocene evolutionary history. Secondary contact promoted hybridization and introgression on the polyploid level, enabling offspring to escape the diploid gene pools. However, the hybrid polyploids do not show significant niche differences compared to their diploid progenitors. It is concluded that the observed absence of niche divergence has precluded further differentiation and geographical partitioning of new polyploid lineages being effectively separated from the parental lines. The predominantly apomictic reproducing polyploids are trapped in the polyploid gene pool and the ecological climatic niche space of their diploid ancestors.

Project description:Asexual reproduction, including parthenogenesis in which embryos develop within a female without fertilization, is assumed to confer advantages over sexual reproduction, which includes a "cost of males." Sexual reproduction largely predominates in animals, however, indicating that this cost is outweighed by the genetic and/or ecological benefits of sexuality, including the acquisition of advantageous mutations occurring in different individuals and the elimination of deleterious mutations. But the evolution of sexual reproduction remains unclear, because we have limited examples that demonstrate the relative success of sexual lineages in the face of competition from asexual lineages in the same environment. Here we investigated a sympatric occurrence of sexual and asexual reproduction in the pineapple mealybug, Dysmicoccus brevipes. This pest invaded southwestern Japan, including Okinawa and Ishigaki Islands, in the 1930s in association with imported pineapple plants. Our recent censuses demonstrated that on Okinawa sexually reproducing individuals can coexist with and even dominate asexual individuals in the presence of habitat and resource competition, which is considered to be severe for this nearly immobile insect. Molecular phylogeny based on partial DNA sequences in the mitochondrial and nuclear genomes, as well as the endosymbiotic bacterial genome, revealed that the asexual lineage diverged from a common sexual ancestor in the relatively recent past. In contrast, only the asexual lineage exhibiting obligate apomictic thelytoky was discovered on Ishigaki. Co-existence of the two lineages cannot be explained by the results of laboratory experiments, which showed that the intrinsic rate of increase in the sexual lineage was not obviously superior to that of the asexual lineage. Differences in biotic and/or abiotic selective forces operating on the two islands might be the cause of this discrepancy. This biological system offers a unique opportunity to assess the relative success of sexual versus asexual lineages with an unusual morphology and life cycle.

Dataset Information

Higher rate of tissue regeneration in polyploid asexual versus diploid sexual freshwater snails.

Publications

Higher rate of tissue regeneration in polyploid asexual versus diploid sexual freshwater snails.

Similar Datasets

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