Reconstructing geographical parthenogenesis: effects of niche differentiation and reproductive mode on Holocene range expansion of an alpine plant

Abstract

Asexual taxa often have larger ranges than their sexual progenitors, particularly in areas affected by Pleistocene glaciations. The reasons given for this ‘geographical parthenogenesis’ are contentious, with expansion of the ecological niche or colonisation advantages of uniparental reproduction assumed most important in case of plants. Here, we parameterized a spread model for the alpine buttercup Ranunculus kuepferi and reconstructed the joint Holocene range expansion of its sexual and apomictic cytotype across the European Alps under different simulation settings. We found that, rather than niche broadening or a higher migration rate, a shift of the apomict's niche towards colder conditions per se was crucial as it facilitated overcoming of topographical barriers, a factor likely relevant for many alpine apomicts. More generally, our simulations suggest potentially strong interacting effects of niche differentiation and reproductive modes on range formation of related sexual and asexual taxa arising from their differential sensitivity to minority cytotype disadvantage.

Phenotypic Responses, Reproduction Mode and Epigenetic Patterns under Temperature Treatments in the Alpine Plant Species Ranunculus kuepferi (Ranunculaceae)

“…Regarding the response of the four selected morphological traits to the treatments, our findings support the hypothesis of a niche preference depending on the cytotype documented by Kirchheimer et al [ 63 , 66 ]. The observed ploidy effect under warm treatment and the treatment effect for the tetraploids under cold treatment imply a potential of phenotypic plasticity, which could sustain fitness under shifted environmental conditions [ 85 ].…”

“…Comparing the growth response of the two cytotypes under warm conditions, diploids did better than tetraploids. This prominent reaction of the tetraploid cytotype to the cold treatment, in addition to the slightly better performance of the diploid cytotype under warm treatment, strengthens the hypothesis of the ecological background of the geographical parthenogenesis pattern of the species [ 47 , 66 ]. This hypothesis proposes the occurrence of the diploid cytotype in the warmer climate of the southwestern Alps and of the tetraploid cytotype in colder conditions at higher elevations in the rest of the Alps.…”

“…This distribution pattern indicates a pronounced geographical parthenogenesis pattern in the European Alps [ 64 ], where diploid populations are restricted to the southwestern Alps and tetraploid populations have colonized previously glaciated areas, i.e., northern, central, and eastern Alps [ 60 , 62 , 65 ]. Tetraploids exhibit a pronounced niche shift toward higher elevations and colder temperatures [ 47 , 63 ], which are associated with their reproduction mode and, in that regard, seem to provide asexual taxa with a distributional advantage [ 66 ].…”

“…Previous studies on wild populations showed that genetic differentiation between cytotypes is very low, and that within cytotypes is on a similar level (Fsts are around 0.3 for both cytotypes), independent of their reproduction mode [ 64 ]. A molecular dating revealed that the tetraploid cytotype originated only 10–80 thousand years ago [ 66 ], probably via multiple and recurrent polyploidization events [ 61 , 67 ]. Epigenetic studies using methylation-sensitive amplified fragment-length polymorphisms (MS-AFLPs) on the species suggested differential profiles in the cytotypes and a connection to abiotic environmental conditions of the epigenetic variation in natural populations and experimental treatments [ 68 , 69 ].…”

Epigenetic Patterns and Geographical Parthenogenesis in the Alpine Plant Species Ranunculus kuepferi (Ranunculaceae)

“…To improve our understanding of the relationships between ploidy, reproduction mode, extreme environments and methylation patterns, we studied natural diploid and tetraploid populations of the alpine perennial species Ranunculus kuepferi Greuter and Burdet along an elevational gradient. This species is a model system for geographical parthenogenesis [58][59][60][61], with diploid populations confined to the southwestern European Alps, while tetraploids inhabit previously glaciated areas of higher elevations in the central and eastern Alps, the Apennines, and on Corsica (maps in References [45,58,61,62]). Triploids occur only in a small sympatric contact zone of diploid and tetraploid populations [58].…”