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Difference in reproductive mode rather than ploidy explains niche differentiation in sympatric sexual and apomictic populations of Potentilla puberula.

ABSTRACT: Apomicts tend to have larger geographical distributional ranges and to occur in ecologically more extreme environments than their sexual progenitors. However, the expression of apomixis is typically linked to polyploidy. Thus, it is a priori not clear whether intrinsic effects related to the change in the reproductive mode or rather in the ploidy drive ecological differentiation. We used sympatric sexual and apomictic populations of Potentilla puberula to test for ecological differentiation. To distinguish the effects of reproductive mode and ploidy on the ecology of cytotypes, we compared the niches (a) of sexuals (tetraploids) and autopolyploid apomicts (penta-, hepta-, and octoploids) and (b) of the three apomictic cytotypes. We based comparisons on a ploidy screen of 238 populations along a latitudinal transect through the Eastern European Alps and associated bioclimatic, and soil and topographic data. Sexual tetraploids preferred primary habitats at drier, steeper, more south-oriented slopes, while apomicts mostly occurred in human-made habitats with higher water availability. Contrariwise, we found no or only marginal ecological differentiation among the apomictic higher ploids. Based on the pronounced ecological differences found between sexuals and apomicts, in addition to the lack of niche differentiation among cytotypes of the same reproductive mode, we conclude that reproductive mode rather than ploidy is the main driver of the observed differences. Moreover, we compared our system with others from the literature, to stress the importance of identifying alternative confounding effects (such as hybrid origin). Finally, we underline the relevance of studying ecological parthenogenesis in sympatry, to minimize the effects of differential migration abilities.

SUBMITTER: Alonso-Marcos H

PROVIDER: S-EPMC6434561 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Difference in reproductive mode rather than ploidy explains niche differentiation in sympatric sexual and apomictic populations of <i>Potentilla puberula</i>.

Alonso-Marcos Henar H Nardi Flavia Domizia FD Scheffknecht Susanne S Tribsch Andreas A Hülber Karl K Dobeš Christoph C

Ecology and evolution 20190305 6

Apomicts tend to have larger geographical distributional ranges and to occur in ecologically more extreme environments than their sexual progenitors. However, the expression of apomixis is typically linked to polyploidy. Thus, it is a priori not clear whether intrinsic effects related to the change in the reproductive mode or rather in the ploidy drive ecological differentiation. We used sympatric sexual and apomictic populations of <i>Potentilla puberula</i> to test for ecological differentiati ...[more]

PMID: 30988899

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Project description:Apomixis evolves from a sexual background and usually is linked to polyploidization. Pseudogamous gametophytic apomicts, which require a fertilization to initiate seed development, of various ploidy levels frequently co-occur with their lower-ploid sexual ancestors, but the stability of such mixed populations is affected by reproductive interferences mediated by cross-pollination. Thereby, reproductive success of crosses depends on the difference in ploidy levels of mating partners, that is, on tolerance of deviation from the balanced ratio of maternal versus paternal genomes. Quality of pollen can further affect reproductive success in intercytotype pollinations. Cross-fertilization, however, can be avoided by selfing which may be induced upon pollination with mixtures of self- and cross-pollen (i.e., mentor effects). We tested for reproductive compatibility of naturally co-occurring tetraploid sexuals and penta- to octoploid apomicts in the rosaceous species Potentilla puberula by means of controlled crosses. We estimated the role of selfing as a crossing barrier and effects of self- and cross-pollen quality as well as maternal: paternal genomic ratios in the endosperm on reproductive success. Cross-fertilization of sexuals by apomicts was not blocked by selfing, and seed set was reduced in hetero- compared to homoploid crosses. Thereby, seed set was negatively related to deviations from balanced parental genomic ratios in the endosperm. In contrast, seed set in the apomictic cytotypes was not reduced in hetero- compared to homoploid crosses. Thus, apomictic cytotypes either avoided intercytotype cross-fertilization through selfing, tolerated intercytotype cross-fertilizations without negative effects on reproductive success, or even benefitted from higher pollen quality in intercytotype pollinations. Our experiment provides evidence for asymmetric reproductive interference, in favor of the apomicts, with significantly reduced seed set of sexuals in cytologically mixed populations, whereas seed set in apomicts was not affected. Incompleteness of crossing barriers further indicated at least partial losses of a parental genomic endosperm balance requirement.

Project description:Apomixis - asexual reproduction via seeds - might arise de novo following polyploidisation events, or via reproductive transfer of apomixis. Both processes can be obtained within species or via hybridisation. We aimed to determine the origin of apomictic genotypes in Potentilla puberula, a rosaceous species showing reproductive differentiation with ploidy: sexual tetraploids and apomictic penta- to octoploids, which regularly co-occur in sympatry. The study is based on 726 individuals, comprising all cytotypes, collected from 138 populations in the Eastern European Alps. We established relationships of cytotypes based on AFLP fingerprinting and cpDNA sequencing to test (1) whether the apomicts are of recurrent allopolyploid origin or originated from within the species via autopolyploidy, and (2) whether there are indications for reproductive transfer versus de novo origin of apomixis. Three principal pathways were identified which explain the origin of new apomictic genotypes, all involving at least one apomictic parent and thus compatible with the idea of reproductive transfer of the apomictic trait to the progeny: (1) self-fertilisation of unreduced egg cells in apomicts; (2) cross-fertilisation among apomicts; and (3) occasionally, heteroploid crosses among sexuals and apomicts. Autopolyploids derived from tetraploid sexuals were repeatedly observed, but did not express apomixis. Finally, our results suggest no role of other species in the origin of extant apomictic genotypes of P. puberula, although local hybrids with P. crantzii were identified. In conclusion, our results show that the formation of new apomictic genotypes required a genetic contribution from at least one apomictic parent. This finding is in accordance with the idea that apomixis is inheritable in P. puberula. On the contrary, lack of apomixis in penta- and hexaploids derived from sexual backgrounds did not support the hypothesis of a de novo origin of apomixis. Relatively high frequency of remnant sexuality in the apomicts involving different cytological pathways of seed formation can explain their high cytological and genotypic diversity. Finally, lack of global introgression from a third taxon is in support of P. puberula as a concise, although highly diverse, species.

Dataset Information

Difference in reproductive mode rather than ploidy explains niche differentiation in sympatric sexual and apomictic populations of Potentilla puberula.

Publications

Difference in reproductive mode rather than ploidy explains niche differentiation in sympatric sexual and apomictic populations of <i>Potentilla puberula</i>.

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