Breeding system of diploid sexuals within theRanunculus auricomuscomplex and its role in a geographical parthenogenesis scenario

Abstract

The larger distribution area of asexuals compared with their sexual relatives in geographical parthenogenesis (GP) scenarios has been widely attributed to the advantages of uniparental reproduction and polyploidy. However, potential disadvantages of sexuals due to their breeding system have received little attention so far. Here, we study the breeding system of five narrowly distributed sexual lineages of Ranunculus notabilis s.l. ( R. auricomus complex) and its effects on outcrossing, inbreeding, female fitness, and heterozygosity. We performed selfing and intra‐ and interlineage crossings by bagging 481 flowers (59 garden individuals) followed by germination experiments. We compared seed set and germination rates, and related them to genetic distance and genome‐wide heterozygosity (thousands of RADseq loci). Selfings (2.5%) unveiled a significantly lower seed set compared with intra‐ (69.0%) and interlineage crossings (69.5%). Seed set of intra‐ (65%) compared to interpopulation crossings (78%) was significantly lower. In contrast, all treatments showed comparable germination rates (32%–43%). Generalized linear regressions between seed set and genetic distance revealed positive relationships in general and between lineages, and a negative one within lineages. Seed set was the main decisive factor for female fitness. Germination rates were not related to genetic distance at any level, but were positively associated with heterozygosity in interlineage crossings. Experiments confirmed full crossability and predominant outcrossing among sexual R. notabilis s.l. lineages. However, up to 5% (outliers 15%–31%) of seeds were formed by selfing, probably due to semi‐self‐compatibility in a multi‐locus gametophytic SI system. Less seed set in intrapopulation crossings, and higher seed set and germination rates from crossings of genetically more distant and heterozygous lineages (interlineage) indicate negative inbreeding and positive outbreeding effects. In GP scenarios, sexual species with small and/or isolated populations can suffer from decreased female fitness due to their breeding system. This factor, among others, probably limits range expansion of sexuals.

Moving beyond assumptions: Polyploidy and environmental effects explain a geographical parthenogenesis scenario in European plants

“…To investigate genetic structure, we carried out sNMF analyses provided by the R package lea version 3.0.0 (Frichot et al, 2014, Frichot & François, 2015, 2020) and based on the min30 alignment (see Karbstein, Rahmsdorf, et al, 2020 for calculations of genetic distance and heterozygosity, and comparability). We used the *.ugeno output file (1 SNP/locus; 33,165 loci) as input and set the number of genetic clusters (K) from 1 to 80, ploidy to four, and repetitions to seven.…”

“…Phylogenetic relationships and genome evolution among described apomictic polyploid taxa of the R. auricomus complex are still unknown. Sexual species are predominantly self-incompatible, whereas pseudogamous apomicts are self-fertile (Hörandl, 2008(Hörandl, , 2010Karbstein, Tomasello, Hodač, Dunkel, et al, 2020, Karbstein, Rahmsdorf, et al, 2020. Apomicts often exhibit no or a variable number of petals (petaloid nectary leaves) whereas sexuals usually possess five of them.…”

Greater reproductive assurance of asexual plant compared with sexual relative in a low‐density sympatric population: Experimental evidence for pollen limitation

“…Although the underlying mechanisms of larger geographical ranges of asexuals are still not well‐understood (Hörandl, 2006), our study suggests that in obligately asexual organisms with fully autonomous apomixis like in Hieracium s.str., the uniparental reproduction strategy could be the most important factor for the establishment success when compared to sexuals. This advantage of asexuals could be further reinforced by lowered fitness of sexuals due to inbreeding depression in small founder populations (Haag & Ebert, 2004; Karbstein et al., 2020; Pinc et al., 2020).…”

Unraveling Phylogenetic Relationships, Reticulate Evolution, and Genome Composition of Polyploid Plant Complexes by Rad-Seq and Hyb-Seq

“…Historically, polyploids were thus often avoided or dropped in phylogenetic studies (Freyman et al 2020;Rothfels 2021). Already the sexual progenitors of polyploid complexes are often characterized by low genetic divergence, incomplete lineage sorting (ILS), gene flow, and partial hybridogenic origins (Hörandl 2018;Pease et al 2018;Wagner et al 2019;Karbstein et al 2020aKarbstein et al , 2020b. The use of 'OMICS'-data provides orders of magnitude more information compared with traditional genetic markers (Harrison and Kidner 2011;Soltis et al 2013).…”

“…Most of these taxa are tetra-to hexaploid and apomictic (Jalas and Suominen 1989;Karbstein et al 2021). Only four di-and one tetraploid, genetically and geographically distinct, sexual species were detected so far and originated 0.83-0.58 Mya (Karbstein et al 2020a(Karbstein et al , 2020bTomasello et al 2020): R. cassubicifolius s.l. (di-and autotetraploid) and R. notabilis s.l.…”