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Relative strength of fine-scale spatial genetic structure in paternally vs biparentally inherited DNA in a dioecious plant depends on both sex proportions and pollen-to-seed dispersal ratio.

ABSTRACT: In plants, the spatial genetic structure (SGS) is shaped mainly by gene dispersal and effective population density. Among additional factors, the mode of DNA inheritance and dioecy influence SGS. However, their joint impact on SGS remains unclear, especially in the case of paternally inherited DNA. Using theoretical approximations and computer simulations, here we showed that the relative intensity of SGS measured in paternally and biparentally inherited DNA in a dioecious plant population depends on both the proportion of males and the pollen-to-seed dispersal ratio. As long as males do not prevail in a population, SGS is more intense in paternally than biparentally inherited DNA. When males prevail, the intensity of SGS in paternally vs biparentally inherited DNA depends on the compound effect of sex proportions and the pollen-to-seed dispersal ratio. To empirically validate our predictions, we used the case of Taxus baccata, a dioecious European tree. First, we showed that mitochondrial DNA (mtDNA) in T. baccata is predominantly (98%) paternally inherited. Subsequently, using nuclear DNA (nuDNA) and mitochondrial microsatellite data, we compared the fine-scale SGS intensity at both marker types in two natural populations. The population with equal sex proportions showed stronger SGS in mtDNA than in nuDNA. On the other hand, we found lower SGS intensity in mtDNA than in nuDNA in the population with 67% males. Thus, the empirical results provided good support for the theoretical predictions, suggesting that knowledge about SGS in paternally vs biparentally inherited DNA may provide insight into effective sex proportions within dioecious populations.

SUBMITTER: Chybicki IJ

PROVIDER: S-EPMC5117843 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Relative strength of fine-scale spatial genetic structure in paternally vs biparentally inherited DNA in a dioecious plant depends on both sex proportions and pollen-to-seed dispersal ratio.

Chybicki I J IJ Dering M M Iszkuło G G Meyza K K Suszka J J

Heredity 20160831 6

In plants, the spatial genetic structure (SGS) is shaped mainly by gene dispersal and effective population density. Among additional factors, the mode of DNA inheritance and dioecy influence SGS. However, their joint impact on SGS remains unclear, especially in the case of paternally inherited DNA. Using theoretical approximations and computer simulations, here we showed that the relative intensity of SGS measured in paternally and biparentally inherited DNA in a dioecious plant population depen ...[more]

PMID: 27577692

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Project description:Background and Aims:Dispersal is crucial due to its direct impact on dynamics of a species' distribution as well as having a role in shaping adaptive potential through gene flow. In plants forming scarce and small populations, knowledge about the dispersal process is required to assess the potential for colonizing new habitats and connectivity of present and future populations. This study aimed to assess dispersal potential in Taxus baccata, a dioecious gymnosperm tree with a wide but highly fragmented distribution. Methods:Seed and pollen dispersal kernels were estimated directly in the framework of the spatially explicit mating model, where genealogies of naturally established seedlings were reconstructed with the help of microsatellite markers. In this way, six differently shaped dispersal functions were compared. Key Results:Seed dispersal followed a leptokurtic distribution, with the Exponential-Power, the Power-law and Weibull being almost equally best-fitting models. The pollen dispersal kernel appeared to be more fat-tailed than the seed dispersal kernel, and the Lognormal and the Exponential-Power function showed the best fit. The rate of seed immigration from the background sources was not significantly different from the rate of pollen immigration (13.1 % vs. 19.7 %) and immigration rates were in agreement with or below maximum predictions based on the estimated dispersal kernels. Based on the multimodel approach, 95 % of seeds travel <109 m, while 95 % of pollen travels <704 m from the source. Conclusions:The results showed that, at a local spatial scale, yew seeds travel shorter distances than pollen, facilitating a rapid development of a kinship structure. At the landscape level, however, although yew exhibits some potential to colonize new habitats through seed dispersal, genetic connectivity between different yew remnants is strongly limited. Taking into account strong population fragmentation, the study suggests that gene dispersal may be a limiting factor of the adaptability of the species.

Project description:The high prevalence of dioecy in marine angiosperms or seagrasses (>50% of all species) is thought to enforce cross-fertilization. However, seagrasses are clonal plants, and they may still be subject to sibling-mating or bi-parental inbreeding if the genetic neighborhood is smaller than the size of the genets. We tested this by determining the genetic neighborhoods of the dioecious seagrass Thalassia testudinum at two sites (Back-Reef and Mid-Lagoon) in Puerto Morelos Reef Lagoon, Mexico, by measuring dispersal of pollen and seeds in situ, and by fine-scale spatial autocorrelation analysis with eight polymorphic microsatellite DNA markers. Prevalence of inbreeding was verified by estimating pairwise kinship coefficients; and by analysing the genotypes of seedlings grown from seeds in mesocosms. Average dispersal of pollen was 0.3-1.6 m (max. 4.8 m) and of seeds was 0.3-0.4 m (max. 1.8 m), resulting in a neighborhood area of 7.4 m2 (range 3.4-11.4 m2) at Back-Reef and 1.9 (range 1.87-1.92 m2) at Mid-Lagoon. Neighborhood area (Na) derived from spatial autocorrelation was 0.1-20.5 m2 at Back-Reef and 0.1-16.9 m2 at Mid-Lagoon. Maximal extensions of the genets, in 19 × 30 m plots, were 19.2 m (median 7.5 m) and 10.8 m (median 4.8 m) at Back-Reef and Mid-Lagoon. There was no indication of deficit or excess of heterozygotes nor were coefficients of inbreeding (FIS) significant. The seedlings did not show statistically significant deficit of heterozygotes (except for 1 locus at Back-Reef). Contrary to our expectations, we did not find evidence of bi-parental inbreeding in this dioecious seagrass with large genets but small genetic neighborhoods. Proposed mechanisms to avoid bi-parental inbreeding are possible selection against homozygotes during fecundation or ovule development. Additionally, the genets grew highly dispersed (aggregation index Ac was 0.09 and 0.10 for Back-Reef and Mid-Lagoon, respectively); such highly dispersed guerrilla-like clonal growth form likely increases the probability of crossing between different potentially unrelated genets.

Dataset Information

Relative strength of fine-scale spatial genetic structure in paternally vs biparentally inherited DNA in a dioecious plant depends on both sex proportions and pollen-to-seed dispersal ratio.

Publications

Relative strength of fine-scale spatial genetic structure in paternally vs biparentally inherited DNA in a dioecious plant depends on both sex proportions and pollen-to-seed dispersal ratio.

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