Phylogenetic and cytogenetic studies reveal hybrid speciation inSaxifragasubsect.Triplinervium(Saxifragaceae)

Abstract

Hybridization has played an important role in Saxifraga evolution causing reticulation and a high number of described hybrids, but little is known about how hybrid speciation had occurred in the genus. We focus on a group of closely related Saxifraga species of the subsection Triplinervium from Pyrenees, the phylogenetic relationships of which remain unsolved. Trying to unmask cryptic (or ancient) hybridization processes, we analyze one nuclear (ITS) and three plastid regions (rpl32‐trnL, trnS‐trnG‐trnG, and 3′trnV‐ndhC), as well as nuclear DNA content. Pollen and seed morphology and viability studies were carried out to evaluate the status of spontaneous hybrids. DNA ploidy levels were also inferred for the two Madeiran taxa (of the same Saxifraga subsection), where recent hybridization processes are not expected. Molecular markers revealed multiple reticulation events, which, as suggested by DNA content and chromosome numbers, have occurred in homoploidy (without genome doubling after hybridization). In addition, autopolyploidy has occurred in some species or populations, especially in the Madeiran archipelago colonization. Chromosome number variation appears to be related to centric fission events, which also could lead to the formation of the B chromosomes inferred in some taxa. Spontaneous hybrids do not produce viable seeds and this could be due to differences in parental chromosome numbers. Hybrid speciation has probably been successful by chromosomal arrangements, which also generated new, more or less intermediate, chromosomal numbers in this group of taxa.

Molecular phylogenetics, morphology and a revised classification of the complex genus Saxifraga (Saxifragaceae)

“…Saxifraga. -Hybridisation between closely and even distantly related species is a frequent and common process in Saxifraga (Engler & Irmscher, 1916Böcher, 1983;Webb & Gornall, 1989;Brochmann & al., 1996;Vargas, 1997Vargas, , 2000Zhmylev, 2002;Mas de Xaxars & al., 2015) that also explains the popularity of this genus in horticulture with more than 2000 known hybrids (Horný & al., 1986;McGregor, 2008). Hybridisation in Saxifraga is associated with extensive cytogenetic variation including dysploid change of chromosome numbers, aneuploidy, occurrence of supernumerary chromosomes and polyploidy (Wakabayashi & Ohba, 1988;Vargas & Nieto Feliner, 1995;Vargas, 2000;Mas de Xaxars & al., 2015).…”

“…-Hybridisation between closely and even distantly related species is a frequent and common process in Saxifraga (Engler & Irmscher, 1916Böcher, 1983;Webb & Gornall, 1989;Brochmann & al., 1996;Vargas, 1997Vargas, , 2000Zhmylev, 2002;Mas de Xaxars & al., 2015) that also explains the popularity of this genus in horticulture with more than 2000 known hybrids (Horný & al., 1986;McGregor, 2008). Hybridisation in Saxifraga is associated with extensive cytogenetic variation including dysploid change of chromosome numbers, aneuploidy, occurrence of supernumerary chromosomes and polyploidy (Wakabayashi & Ohba, 1988;Vargas & Nieto Feliner, 1995;Vargas, 2000;Mas de Xaxars & al., 2015). Both types of polyploidy occur in Saxifraga, for example, autopolyploidy in S. moschata (Mas de Xaxars & al., 2015) and allopolyploidy in S. osloensis (S. adscendens × S. tridactylites;Brochmann & al., 1996), S. opdalensis A.Blytt and S. svalbardensis Øvstedal (both S. cernua × S. rivularis;Brochmann & al., 1998;Steen & al., 2000).…”

“…Hybridisation in Saxifraga is associated with extensive cytogenetic variation including dysploid change of chromosome numbers, aneuploidy, occurrence of supernumerary chromosomes and polyploidy (Wakabayashi & Ohba, 1988;Vargas & Nieto Feliner, 1995;Vargas, 2000;Mas de Xaxars & al., 2015). Both types of polyploidy occur in Saxifraga, for example, autopolyploidy in S. moschata (Mas de Xaxars & al., 2015) and allopolyploidy in S. osloensis (S. adscendens × S. tridactylites;Brochmann & al., 1996), S. opdalensis A.Blytt and S. svalbardensis Øvstedal (both S. cernua × S. rivularis;Brochmann & al., 1998;Steen & al., 2000). Since F 2 plants from artificially generated and natural hybrids are difficult to obtain in Saxifraga (Wakabayashi & Ohba, 1988;Vargas & Nieto Feliner, 1995;Mas de Xaxars & al., 2015), spontaneous hybrids constituting an F 1 generation are unlikely to complete a homoploid hybrid speciation process.…”

“…Both types of polyploidy occur in Saxifraga, for example, autopolyploidy in S. moschata (Mas de Xaxars & al., 2015) and allopolyploidy in S. osloensis (S. adscendens × S. tridactylites;Brochmann & al., 1996), S. opdalensis A.Blytt and S. svalbardensis Øvstedal (both S. cernua × S. rivularis;Brochmann & al., 1998;Steen & al., 2000). Since F 2 plants from artificially generated and natural hybrids are difficult to obtain in Saxifraga (Wakabayashi & Ohba, 1988;Vargas & Nieto Feliner, 1995;Mas de Xaxars & al., 2015), spontaneous hybrids constituting an F 1 generation are unlikely to complete a homoploid hybrid speciation process. Missing self-perpetuation of hybrids can be overcome by allopolyploidy, which overcomes F 1 sterility and generates offspring that is genetically isolated from its parents and is not backcrossing.…”

Past climate changes facilitated homoploid speciation in three mountain spiny fescues (Festuca, Poaceae)

“…Homoploid hybrid speciation (HHS), where interspecific gene flow leads to the formation of a novel and stable lineage without a change in chromosome number123 has traditionally been defended as rare in relation to the more common allopolyploid hybrid speciation45. But perspectives on the importance of homoploid speciation have drastically changed in the past decades since it has been documented in a wide number of plants and metazoan taxa67.…”