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Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations.

ABSTRACT: BACKGROUND:Models of the maintenance of sex predict that one reproductive strategy, sexual or parthenogenetic, should outcompete the other. Distribution patterns may reflect the outcome of this competition as well as the effect of chance and historical events. We review the distribution data of sexual and parthenogenetic biotypes of the planarian Schmidtea polychroa. RESULTS:S. polychroa lives in allopatry or sympatry across Europe except for Central and North-Western Europe, where sexual individuals have never been reported. A phylogenetic relationship between 36 populations based on a 385 bp fragment of the mitochondrial cytochrome oxidase I gene revealed that haplotypes were often similar over large geographic distances. In North Italian lakes, however, diversity was extreme, with sequence differences of up to 5% within the same lake in both sexuals and parthenogens. Mixed populations showed "endemic" parthenogenetic lineages that presumably originated from coexisting sexuals, and distantly related ones that probably result from colonization by parthenogens independent from sexuals. CONCLUSIONS:Parthenogens originated repeatedly from sexuals, mainly in Italy, but the same may apply to other Mediterranean regions (Spain, Greece). The degree of divergence between populations suggests that S. polychroa survived the ice ages in separate ice-free areas in Central, Eastern and Southern Europe and re-colonised Europe after the retreat of the major glaciers. Combining these results with those based on nuclear markers, the data suggest that repeated hybridisation between sexuals and parthenogenetic lineages in mixed populations maintains high levels of genetic diversity in parthenogens. This can explain why parthenogens persist in populations that were originally sexual. Exclusive parthenogenesis in central and western populations suggests better colonisation capacity, possibly because of inbreeding costs as well as hybridisation of sexuals with parthenogens.

SUBMITTER: Pongratz N

PROVIDER: S-EPMC280671 | biostudies-literature | 2003 Nov

REPOSITORIES: biostudies-literature

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Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations.

Pongratz Norbert N Storhas Martin M Carranza Salvador S Michiels Nicolaas K NK

BMC evolutionary biology 20031117

<h4>Background</h4>Models of the maintenance of sex predict that one reproductive strategy, sexual or parthenogenetic, should outcompete the other. Distribution patterns may reflect the outcome of this competition as well as the effect of chance and historical events. We review the distribution data of sexual and parthenogenetic biotypes of the planarian Schmidtea polychroa.<h4>Results</h4>S. polychroa lives in allopatry or sympatry across Europe except for Central and North-Western Europe, wher ...[more]

PMID: 14622447

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Project description:BACKGROUND: Multiple loci and population genetic methods were employed to study the phylogeographic history of the Patagonian freshwater crab Aegla neuquensis (Aeglidae: Decopoda). This taxon occurs in two large river systems in the Patagonian Steppe, from the foothills of the Andes Mountains east to the Atlantic Ocean. METHODOLOGY/PRINCIPAL FINDINGS: A nuclear phylogeny and multilocus nested clade phylogeographic analysis detected a fragmentation event between the Negro and Chico-Chubut river systems. This event occurred approximately 137 thousand years ago. An isolation-with-migration analysis and maximum-likelihood estimates of gene flow showed asymmetrical exchange of genetic material between these two river systems exclusively in their headwaters. We used information theory to determine the best-fit demographic history between these two river systems under an isolation-with-migration model. The best-fit model suggests that the Negro and the ancestral populations have the same effective population sizes; whereas the Chico-Chubut population is smaller and shows that gene flow from the Chico-Chubut into the Negro is four times higher than in the reverse direction. Much of the Chico-Chubut system appears to have only been recently colonized while the Negro populations appear to have been in place for most of the evolutionary history of this taxon. CONCLUSIONS/SIGNIFICANCE: Due to mitochondrial introgression, three nuclear loci provided different phylogeographic resolution than the three mitochondrial genes for an ancient fragmentation event observed in the nuclear phylogeny. However, the mitochondrial locus provided greater resolution on more recent evolutionary events. Our study, therefore, demonstrates the need to include both nuclear and mitochondrial loci for a more complete understanding of evolutionary histories and associated phylogeographic events. Our results suggest that gene flow between these systems, before and after fragmentation was through periodic paleolakes that formed in the headwaters region. Fragmentation between the Negro and Chico-Chubut systems was driven by the disappearance of these paleolakes during the Patagonian Glaciation.

Project description:The dominance of sex in Metazoa is enigmatic. Sexual species allocate resources to the production of males, while potentially facing negative effects such as the loss of well-adapted genotypes due to recombination, and exposure to diseases and predators during mating. Two major hypotheses have been put forward to explain the advantages of parthenogenetic versus sexual reproduction in animals, that is, the Red Queen hypothesis and the Tangled Bank/Structured Resource Theory of Sex. The Red Queen hypothesis assumes that antagonistic predator-prey/ parasite-host interactions favor sex. The Structured Resource Theory of Sex predicts sexual reproduction to be favored if resources are in short supply and aggregated in space. In soil, a remarkable number of invertebrates reproduce by parthenogenesis, and this pattern is most pronounced in oribatid mites (Oribatida, Acari). Oribatid mites are abundant in virtually any soil across very different habitats, and include many sexual and parthenogenetic (thelytokous) species. Thereby, they represent an ideal model group to investigate the role of sexual versus parthenogenetic reproduction across different ecosystems and habitats. Here, we compiled data on oribatid mite communities from different ecosystems and habitats across biomes, including tropical rainforests, temperate forests, grasslands, arable fields, salt marshes, bogs, caves, and deadwood. Based on the compiled dataset, we analyzed if the percentage of parthenogenetic species and the percentage of individuals of parthenogenetic species are related to total oribatid mite density, species number, and other potential driving factors of the reproductive mode including altitude and latitude. We then interpret the results in support of either the Red Queen hypothesis or the Structured Resource Theory of Sex. Overall, the data showed that low density of oribatid mites due to harsh environmental conditions is associated with high frequency of parthenogenesis supporting predictions of the Structured Resource Theory of Sex rather than the Red Queen hypothesis.

Dataset Information

Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations.

Publications

Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: patterns and explanations.

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