No evidence of intrinsic reproductive isolation between two reciprocally non-monophyletic, ecologically differentiated mountain plants at an early stage of speciation

Abstract

Adaptation to dissimilar habitats can trigger phenotypic and genetic differences between populations, which may, in the absence of gene flow, ultimately lead to ecological speciation. Reproductive isolation of diverging populations is a critical step at the onset of speciation. An excellent example for exploring the extent of reproductive isolation at early stages of speciation is provided by Heliosperma pusillum and H. veselskyi (Caryophyllaceae), two reciprocally non-monophyletic, ecologically differentiated species from the Alps. Interspecific gene flow-as revealed by recent genetic studies-is rare even between geographically close populations. Cross pollinations and fitness experiments revealed no evidence of intrinsic reproductive barriers, since fitness parameters measured under uniform conditions were not lower in inter-than in intraspecific crosses. Further, morphometric analyses of the offspring clearly showed that the differentiation of parental species is heritable. As parental phenotypes are likely adaptive, the intermediate morphology of hybrids may lead to reduced hybrid fitness in parental habitats. Altogether, H. pusillum and H. veselskyi provide an increasingly well characterised model system offering exciting insights into early stages of ecological speciation.

Parallel colonization of subalpine habitats in the central European mountains by Primula elatior

“…elatior due to the lack of any long-distance seed dispersal adaptation 48 . In the mountains, seed flow may be further enhanced by washing downslope by mountain streams, but pollen flow may be restricted along an elevational gradient due to differences in flowering phenology between populations at different elevations 4 . In the closely related species P .…”

“…Local adaptation to these environmental stresses often results in the evolution of specific morphological and/or physiological traits that confer increased fitness in these challenging environments 2,3 . Populations characterized by these adaptations are often called “ecotypes” and their level of overall genetic differentiation from ancestral populations may be still very low 2,4 . In cases where reproductive barriers arise between ecotypes and their ancestral populations, either as a consequence of natural selection or simply due to spatial isolation, the ecotype may represent the first step towards the founding of a new species 5,6 .…”

Natural selection drives parallel divergence in the mountain plant Heliosperma pusillum s.l

“…Adaptation to different environments -alpine screes and montane rock overhangs separated by a broad, uninhabitable forest belt -likely prevents gene flow between montane and alpine populations of H. pusillum s.l. Pronounced environmental divergence within population pairs and reduced establishment success of non-native individuals strongly support that reproductive isolation, which has been shown to be based solely on extrinsic barriers, most prominently spatial isolation (Bertel et al 2016b), is enforced by immigrant and hybrid inviability. In the same line, the strength of ecological barriers to gene flow likely increases with the extent of habitat differentiation (Ramsey et al 2003).…”

“…Although both entities are treated as independent species in national floras (Poldini 2002, Fischer 2008, DNA sequence data (Frajman andOxelman 2007, Frajman et al 2009) as well as restriction site associated DNA (RAD) markers (Trucchi et al 2017) indicate that the disjunct populations of H. veselskyi are inextricably nested within widespread H. pusillum, suggesting that the populations of the former have evolved at multiple localities in parallel from the latter, most likely after the Last Glacial Maximum. Further, H. pusillum and H. veselskyi lack intrinsic reproductive isolation and retain their morphological differences over several generations when grown under uniform conditions (Bertel et al 2016b). For the reasons outlined above, the species rank is highly debatable and we thus term the two entities in the following montane populations (corresponding to 'H.…”

Genomic analyses suggest parallel ecological divergence in Heliosperma pusillum (Caryophyllaceae)

“…The montane ecotype has instead a dense indumentum with long multicellular sticky glandular trichomes and is found in canyons and below cliff overhangs with dry soils and poor light conditions far below the timberline. Phenotypic differences between the two ecotypes remain stable after cultivation under uniform conditions for at least three generations but inter-ecotype crossings produce viable and fertile offspring (Bertel et al, 2016a). Available phylogenies (Frajman & Oxelman, 2007;Frajman et al, 2009) suggest that the relationships among populations of both ecotypes may be governed by geographic proximity rather than by ecological preference, implying that the disjunct populations of the montane ecotype could have originated more than once from the widespread alpine populations.…”