Population genetics of sporophytic self-incompatibility in Senecio squalidus L. (Asteraceae) II: a spatial autocorrelation approach to determining mating behaviour in the presence of low S allele diversity

Abstract

We recently estimated that as few as six S alleles represent the extent of S locus diversity in a British population of the self-incompatible (SI) coloniser Senecio squalidus (Oxford Ragwort). Despite the predicted constraints to mating imposed by such a low number of S alleles, S. squalidus maintains a strong sporophytic self-incompatibility (SSI) system and there is no evidence for a breakdown of SSI or any obvious negative reproductive consequences for this highly successful coloniser. The present paper assesses mating behaviour in an Oxford S. squalidus population through observations of its effect on spatial patterns of genetic diversity and thus the extent to which it is responsible for ameliorating the potentially detrimental reproductive consequences of low S allele diversity in British S. squalidus. A spatial autocorrelation (SA) treatment of S locus and allozyme polymorphism data for four loci indicates that mating events regularly occur at all the distance classes examined from 60 to 480 m throughout the entire sample population. Less SA is observed for S locus data than for allozyme data in accordance with the hypothesis that SSI and low diversity at the S locus are driving these large-scale mating events. The limited population structure at small distances of 60 m and less observed for SA analysis of the Me-2 locus and by F-statistics for all the allozyme data, is evidence of some local relatedness due to limited seed and pollen dispersal in S. squalidus. However, the overall impression of mating dynamics in this S. squalidus population is that of ample potential mating opportunities with many individuals at large population scales, indicating that reproductive success is not seriously affected by few S alleles available for mating interactions.

Impact of negative frequency-dependent selection on mating pattern and genetic structure: a comparative analysis of the S-locus and nuclear SSR loci in Prunus lannesiana var. speciosa

“…Glémin et al, 2005 compared genetic structure between the S-locus and SSR loci in five populations of Brassica insularis with a sporophytic SI system, and their results were consistent with these predictions. Although Brennan et al, 2003 found no significant spatial genetic structure at either the S-locus or allozyme loci in Senecio aqualidus, Leducq et al (2011) recorded reduced spatial genetic structure at the S-locus than at SSR loci in Arabidopsis halleri. In rosaceous species with a gametophytic SI system, Stoeckel et al (2008) and Holderegger et al (2008) found less genetic differentiation between populations at the S-locus than at SSR loci, although Schueler et al (2006) did not find any differences in the extent of spatial genetic structure between the two locus types.…”

“…In Brassica insularis, Glémin et al (2005) compared the population structure at the S-locus with that indicated by selectively neutral loci, nuclear simple sequence repeats (SSRs or microsatellites); their data supported most of the theoretical predictions. In Senecio squalidus, spatial genetic structure within populations was found to be weak at both the S-locus and at allozyme loci for which variation seemed to be selectively neutral (Brennan et al, 2003), whereas genetic differentiation among populations was smaller at the S-locus than at the allozyme loci (Brennan et al, 2006). In Arabidopsis halleri, the spatial genetic structure within populations was weaker when determined on the basis of the S-locus than when SSR loci were considered (Leducq et al, 2011).…”

Effect of balancing selection on spatial genetic structure within populations: theoretical investigations on the self-incompatibility locus and empirical studies in Arabidopsis halleri

“…Previous empirical studies, together with our own results, showed three contrasted types of situations: (1) no pattern of SGS whatsoever-neither at the S-locus nor at neutral marker loci (Brennan et al, 2003); (2) significant and consistent patterns of SGS at the S-locus and neutral markers (Schueler et al, 2006; population Nivelle in this study); (3) significantly higher extent of SGS at neutral marker loci as compared to the S-locus (populations Auby and Hautes-Fagnes in this study). Situation (1) could be due to the absence of SGS in the case of random dispersal, to recent demographic disturbance or to a lack of resolution of the analysis when sample sizes are small (for example, in the study of Brennan et al, 2003, in S. squalidus only 24 individuals were sampled).…”

“…Two empirical studies investigated SGS within populations for both the S-locus and neutral loci. In a population of Senecio squalidus, Brennan et al (2003) found no significant decrease of genetic similarity between individuals with spatial distance, at neither the S-locus nor allozyme markers. In contrast, in a population of Prunus avium, Schueler et al (2006) found evidence for SGS at both the S-locus and microsatellite markers, with a similar extent of SGS for both types of loci.…”

Unraveling the mysteries of reproduction

“…There is also empirical evidence that the breakdown of SI may have far more complex causes than merely the number of S-alleles, as exemplified by plants that do not behave as they should according to this theory: In the highly successful colonizer Senecio squalidus, the SI system has been maintained despite a very low number of S-alleles (Brennan et al, 2003). Furthermore, other genetic and non-genetic (for example, environmental) factors have been shown to result in a 'leakiness' of SI systems (Reinartz and Les, 1994, and references therein), and even the developmental stage (age of flowers) can make SI a plastic trait (Mena-Alí et al, 2009).…”