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Genetic variation and genetic structure within metapopulations of two closely related selfing and outcrossing Zingiber species (Zingiberaceae).

ABSTRACT: Habitat fragmentation strongly affects the genetic diversity of plant populations, and this has always attracted much research interest. Although numerous studies have investigated the effects of habitat fragmentation on the genetic diversity of plant populations, fewer studies have compared species with contrasting breeding systems while accounting for phylogenetic distance. Here, we compare the levels of genetic diversity and differentiation within and among subpopulations in metapopulations (at fine-scale level) of two closely related Zingiber species, selfing Zingiber corallinum and outcrossing Zingiber nudicarpum. Comparisons of the genetic structure of species from unrelated taxa may be confounded by the effects of correlated ecological traits or/and phylogeny. Thus, we possibly reveal the differences in genetic diversity and spatial distribution of genetic variation within metapopulations that relate to mating systems. Compared to outcrossing Z. nudicarpum, the subpopulation genetic diversity in selfing Z. corallinum was significantly lower, but the metapopulation genetic diversity was not different. Most genetic variation resided among subpopulations in selfing Z. corallinum metapopulations, while a significant portion of variation resided either within or among subpopulations in outcrossing Z. nudicarpum, depending on whether the degree of subpopulation isolation surpasses the dispersal ability of pollen and seed. A stronger spatial genetic structure appeared within subpopulations of selfing Z. corallinum potentially due to restricted pollen flow and seed dispersal. In contrast, a weaker genetic structure was apparent in subpopulations of outcrossing Z. nudicarpum most likely caused by extensive pollen movement. Our study shows that high genetic variation can be maintained within metapopulations of selfing Zingiber species, due to increased genetic differentiation intensified primarily by the stochastic force of genetic drift among subpopulations. Therefore, maintenance of natural variability among subpopulations in fragmented areas is key to conserve the full range of genetic diversity of selfing Zingiber species. For outcrossing Zingiber species, maintenance of large populations is an important factor to enhance genetic diversity. Compared to outcrossing Z. nudicarpum, the subpopulation genetic diversity in selfing Z. corallinum was significantly lower, but the metapopulation genetic diversity did not differ. Most genetic variation resided among subpopulations in selfing Z. corallinum metapopulations, while a significant portion of variation resided either within or among subpopulations in outcrossing Z. nudicarpum, depending on whether the degree of subpopulation isolation surpasses the dispersal ability of pollen and seed. Our study shows that selfing Z. corallinum could maintain high genetic diversity through differentiation intensified primarily by the stochastic force of genetic drift among subpopulations at fine-scale level, but not local adaptation.

SUBMITTER: Huang R

PROVIDER: S-EPMC7788390 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThere has always been controversy over whether clonal plants have lower genetic diversity than plants that reproduce sexually. These conflicts could be attributed to the fact that few studies have taken into account the mating system of sexually reproducing plants and their phylogenetic distance. Moreover, most clonal plants in these previous studies regularly produce sexual progeny. Here, we describe a study examining the levels of genetic diversity and differentiation within and between local populations of fully clonal Zingiber zerumbet at a microgeographical scale and compare the results with data for the closely related selfing Z. corallinum and outcrossing Z. nudicarpum. Such studies could disentangle the phylogenetic and sexually reproducing effect on genetic variation of clonal plants, and thus contribute to an improved understanding in the clonally reproducing effects on genetic diversity and population structure.ResultsThe results revealed that the level of local population genetic diversity of clonal Z. zerumbet was comparable to that of outcrossing Z. nudicarpum and significantly higher than that of selfing Z. corallinum. However, the level of microgeographic genetic diversity of clonal Z. zerumbet is comparable to that of selfing Z. corallinum and even slightly higher than that of outcrossing Z. nudicarpum. The genetic differentiation among local populations of clonal Z. zerumbet was significantly lower than that of selfing Z. corallinum, but higher than that of outcrossing Z. nudicarpum. A stronger spatial genetic structure appeared within local populations of Z. zerumbet compared with selfing Z. corallinum and outcrossing Z. nudicarpum.ConclusionsOur study shows that fully clonal plants are able not only to maintain a high level of within-population genetic diversity like outcrossing plants, but can also maintain a high level of microgeographic genetic diversity like selfing plant species, probably due to the accumulation of somatic mutations and absence of a capacity for sexual reproduction. We suggest that conservation strategies for the genetic diversity of clonal and selfing plant species should be focused on the protection of all habitat types, especially fragments within ecosystems, while maintenance of large populations is a key to enhance the genetic diversity of outcrossing species.

Project description:Empirical studies on natural populations of Medicago truncatula revealed selfing rates higher than 80%, but never up to 100%. Similarly, several studies of predominantly selfing species show variability in the level of residual outcrossing between populations and also between temporal samples of the same population. However, these studies measure global selfing rates at the scale of the population and we do not know whether there is intra-population variation and how outcrossing events are distributed, between genotypes, plants, flowers, or seeds. Theoretical studies predict the maintenance of residual outcrossing in highly selfing species due to environmental (e.g., pollen biology) and/or genetic determinants and decompositions of the variation in outcrossing rate using experimental data can be very informative to test these hypotheses. Here, we focus on one natural population of M. truncatula in order to describe precisely its mating system. In particular, we investigated the determinants of the selfing rate by testing for seasonal variations (environmental determinism) and variations between genotypes (genetic determinism). We measured selfing rates in maternal progenies from plants collected widely across a natural population. For each plant, we collected pods from flowers produced at the beginning and at the end of the flowering season to test for a seasonal variation in the outcrossing rate. For each collected offspring, we also estimated the likelihood that it was issued from a self-fertilization event and assessed the genetic component of variation of this mating system measure. We found a significant, albeit small, increase in outcrossing rate in progenies collected at the end [t m = 0.137 (SD = 0.025)] compared to those collected at the beginning [t m = 0.083 (0.016)] of the flowering season. A significant between genotypes variation in selfing rate was also detected, resulting in a heritability of 9% for the rate of residual outcrossing. Altogether, our work shows that despite a predominantly selfing reproductive mode, M. truncatula displays variation in residual outcrossing rate, and that this trait is likely under a complex determinism combining environmental and genetic factors. We discuss the evolutionary implications of our results for the population.

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Genetic variation and genetic structure within metapopulations of two closely related selfing and outcrossing Zingiber species (Zingiberaceae).

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