Geographical parthenogenesis and population genetic structure in the alpine species Ranunculus kuepferi (Ranunculaceae)

Abstract

Geographical parthenogenesis describes the enigmatic phenomenon that asexual organisms have larger distribution areas than their sexual relatives, especially in previously glaciated areas. Classical models suggest temporary advantages to asexuality in colonization scenarios because of uniparental reproduction and clonality. We analyzed population genetic structure and self-fertility of the plant species Ranunculus kuepferi on 59 populations from the whole distribution area (European Alps, Apennines and Corsica). Amplified fragment length polymorphisms (AFLPs) and five microsatellite loci revealed individual genotypes for all populations and mostly insignificant differences between diploid sexuals and tetraploid apomicts in all measures of genetic diversity. Low frequencies of private AFLP fragments/simple sequence repeat alleles, and character incompatibility analyses suggest that facultative recombination explains best the unexpectedly high genotypic diversity of apomicts. STRUCTURE analyses using AFLPs revealed a higher number of partitions and a stronger geographical subdivision for diploids than for tetraploids, which contradicts expectations of standard gene flow models, but indicates a reduction of genetic structure in asexuals. Apomictic populations exhibited high admixture near the sexual area, but appeared rather uniform in remote areas. Bagging experiments and analyses of pollen tube growth confirmed self-fertility for pollen-dependent apomicts, but self-sterility for diploid sexuals. Facultative apomixis combines advantages of both modes of reproduction: uniparental reproduction allows for rapid colonization of remote areas, whereas facultative sexuality and polyploidy maintains genetic diversity within apomictic populations. The density dependence of outcrossing limits range expansions of sexual populations.

Figure 1

Map of the distribution area of R. kuepferi; black squares, tetraploid populations; white squares, diploid populations; numbers beside the squares correspond to population numbers in Table 1. Colors represent the respective partitions identified by the STRUCTURE analysis. Individual posterior assignment probabilities (thin vertical lines) show the affiliation to the particular partitions. (a) STRUCTURE analysis with diploids and tetraploids analyzed separately and shown with different color schemes (see Materials and methods); (b) STRUCTURE analysis with all populations treated as diploids and shown with one color scheme.

Figure 2

Boxplots of the variation of percentages of well-developed achenes per collective fruit for diploid sexuals and tetraploid apomicts. The box shows the 25th and 75th percentile range and the median value, and maximum and minimum values within the normal range (capped bars); circles are outliers, asterisks (*) represent extreme values. N, number of flowers (collective fruits).

Figure 3

Pollen tube growth in diploids and tetraploids after manual crossing and manual selfing. Values are percentages of carpels with respective pollen tube length; white, pollen tube missing; dotted, pollen tube growth stops at the stigma surface; cross-hatched, pollen tube growth stops within the stigma; gray, pollen tube growth stops in the style, and black, pollen tubes reach the base of the style and enter the ovary.