Evolution of biogeographic patterns, ploidy levels, and breeding systems in a diploid–polyploid species complex of Primula

Abstract

Summary• Primula sect. Aleuritia subsect. Aleuritia ( Aleuritia ) includes diploid, self-incompatible heterostyles and polyploid, self-compatible homostyles, the latter generally occurring at higher latitudes than the former. This study develops a phylogenetic hypothesis for Aleuritia to elucidate the interactions between Pleistocene glacial cycles, biogeographic patterns, ploidy levels and breeding systems.• Sequences from five chloroplast DNA loci were analyzed with parsimony to reconstruct a phylogeny, haplotype network, and ancestral states for ploidy levels and breeding systems.• The results supported the monophyly of Aleuritia and four major biogeographic lineages: an amphi-Pacific, a South American, an amphi-Atlantic and a European/ North American lineage. At least four independent switches to homostyly and five to polyploidy were inferred.• An Asian ancestor probably gave origin to an amphi-Pacific clade and to a lineage that diversified on the European and American continents. Switches to homostyly occurred exclusively in polyploid lineages, which mainly occupy previously glaciated areas. The higher success of the autogamous polyploid species at recolonizing habitats freed by glacial retreat might be explained in terms of selection for reproductive assurance.

Production of Diploid Male Gametes in Arabidopsis by Cold-Induced Destabilization of Postmeiotic Radial Microtubule Arrays

“…Our results, together with the relatively high number of polyploid plant species in areas with extreme environments (Flovik, 1940;Stebbins, 1984;Guggisberg et al, 2006) and the notion that ancient polyploidization events often coincided with adverse climatic events (e.g. glaciation periods; Brochmann et al, 2004;Van de Peer et al, 2009), support the hypothesis that stress-induced formation of diploid gametes may have substantially contributed to plant polyploidization and associated speciation (Wood et al, 2009).…”

Heterostyly accelerates diversification via reduced extinction in primroses

“…The apparent impact of heterostyly on extinction rate translates to a 2.3-to 4.4-fold higher net-diversification rate, depending on specific analytical settings (table 1; electronic supplementary material, table S3). This result did not change qualitatively when we accounted for polyploidy (which is sometimes associated with loss of heterostyly [35,51]), by either excluding polyploids from analyses, or by assigning them to distinct states under a multi-state speciation and extinction model (MuSSE [52]; details and caveats of this approach are discussed in the electronic supplementary material, text S1).…”

Mixed Mating in Homostylous Species: Genetic and Experimental Evidence from an Alpine Plant with Variable Herkogamy,Primula halleri

“…Homostyly has been interpreted as an adaptation to promote autonomous selfing in marginal environments with low pollinator availability (e.g., in Primula [Guggisberg et al 2006;Carlson et al 2008] and Nymphoides [Haddadchi and Fatemi 2015]), but variation in herkogamy in homostylous species challenges this predominant view. Homostylous plants often present variation in the positions of anthers and stigmas within flowers (e.g., Barrett and Shore 1987;Johnston and Schoen 1996;Medrano et al 2005;de Vos et al 2014b;Sosenski et al 2016), including P. halleri 2014b; note that we use homostyly and monomorphy in the context of heterostyly interchangeably, as both terms refer to presence of one, rather than multiple, style morphs, irrespective of stigma position relative to anthers).…”

“…(Primulaceae). The species is a classic example of the evolution of self-compatiblity in marginal environments in the form of homostyly, from a heterostylous, obligately outcrossing ancestor (Guggisberg et al 2006(Guggisberg et al , 2009de Vos et al 2014a). Distylous (i.e., dimorphic heterostylous) species are obligately outcrossing, with plants differing in the reciprocal positioning of anthers and stigmas in the two complementary floral morphs and characterized by a genetic incompatibility system that prevents pollen germination within the same individual or floral morph (reviewed, e.g., in Darwin 1877;Barrett 1992;Cohen 2010).…”