Sexual intraspecific recombination but not de novo origin governs the genesis of new apomictic genotypes in Potentilla puberula (Rosaceae)

Abstract

Apomixis – asexual reproduction via seeds – might arise de novo following polyploidisation events, or via reproductive transfer of apomixis. Both processes can be obtained within species or via hybridisation. We aimed to determine the origin of apomictic genotypes in Potentilla puberula, a rosaceous species showing reproductive differentiation with ploidy: sexual tetraploids and apomictic pentato octoploids, which regularly co‐occur in sympatry. The study is based on 726 individuals, comprising all cytotypes, collected from 138 populations in the Eastern European Alps. We established relationships of cytotypes based on AFLP fingerprinting and cpDNA sequencing to test (1) whether the apomicts are of recurrent allopolyploid origin or originated from within the species via autopolyploidy, and (2) whether there are indications for reproductive transfer versus de novo origin of apomixis. Three principal pathways were identified which explain the origin of new apomictic genotypes, all involving at least one apomictic parent and thus compatible with the idea of reproductive transfer of the apomictic trait to the progeny: (1) self‐fertilisation of unreduced egg cells in apomicts; (2) cross‐fertilisation among apomicts; and (3) occasionally, heteroploid crosses among sexuals and apomicts. Autopolyploids derived from tetraploid sexuals were repeatedly observed, but did not express apomixis. Finally, our results suggest no role of other species in the origin of extant apomictic genotypes of P. puberula, although local hybrids with P. crantzii were identified. In conclusion, our results show that the formation of new apomictic genotypes required a genetic contribution from at least one apomictic parent. This finding is in accordance with the idea that apomixis is inheritable in P. puberula. On the contrary, lack of apomixis in penta‐ and hexaploids derived from sexual backgrounds did not support the hypothesis of a de novo origin of apomixis. Relatively high frequency of remnant sexuality in the apomicts involving different cytological pathways of seed formation can explain their high cytological and genotypic diversity. Finally, lack of global introgression from a third taxon is in support of P. puberula as a concise, although highly diverse, species.

Difference in reproductive mode rather than ploidy explains niche differentiation in sympatric sexual and apomictic populations ofPotentilla puberula

“…All cytotypes were present across the whole study area, but sexual tetraploids tended to occur in populations geographically separated from the apomictic ones (102, 74.45%), which were—in turn—usually formed by more than one cytotype (102, 76.12%; Figure ). Individual flow cytometric measurements of the 115 populations not analyzed by Nardi et al () are available on Dryad (http://dx.doi.org/10.5061/dryad.bj0436h).…”

“…Apomictic allopolyploids such as Antennaria rosea (Bayer, Purdy, & Lebedyk, ) and Crataegus suksdorfii and Crataegus douglasii (Coughlan, Han, Stefanović, & Dickinson, ) occupy ecological niches intermediate to those of the parental species, a hint that ecological niche shifts of those taxa indeed may be owing to their hybrid origin, rather than to apomixis itself. Contrariwise, in Potentilla puberula , the apomictic cytotypes are autopolyploid and genetically very similar to the sexual tetraploids (Nardi et al, ), ruling out strong effects of hybridization.…”

“…It exhibits a series of reproductively differentiated ploidy levels comprising tetra‐ ( x = 7; 2 n = 28), penta‐ (2 n = 35), hexa‐ (2 n = 42), hepta‐ (2 n = 49), and octoploids (2 n = 56; Dobeš, ). Tetraploid individuals reproduce almost exclusively sexually and are self‐incompatible, whereas higher ploids are predominantly self‐compatible and pseudogamous apomicts (Dobeš et al, ; Nardi et al, ). For hexaploids, both reproductive modes are documented, with apomictic individuals usually clustering with other apomictic cytotypes, and sexual individuals occurring in low frequencies within sexual tetraploid populations (which probably originate frequently de novo as autohexaploids, Nardi et al, ).…”

“…Tetraploid individuals reproduce almost exclusively sexually and are self‐incompatible, whereas higher ploids are predominantly self‐compatible and pseudogamous apomicts (Dobeš et al, ; Nardi et al, ). For hexaploids, both reproductive modes are documented, with apomictic individuals usually clustering with other apomictic cytotypes, and sexual individuals occurring in low frequencies within sexual tetraploid populations (which probably originate frequently de novo as autohexaploids, Nardi et al, ). No fine‐scale cytogeography has ever been obtained across the whole distributional range (see Kurtto et al, ), although data collected by Dobeš () suggest that only the apomictic cytotypes are present in Eastern Austria.…”

“…Given the strong correspondence between ploidy level and reproductive mode, with more than 90% of seeds by cytotype being derived by either reproductive mode (Dobeš et al, ; Nardi et al, ), we considered henceforth tetraploid individuals to be sexual and penta‐, hepta‐, and octoploids to be apomicts. According to Nardi et al (), hexaploids comprise sexual autohexaploids (ca. 40% of genotypes) and apomicts (ca.…”