Disentangling Reticulate Evolution in an Arctic–Alpine Polyploid Complex

Abstract

Although polyploidy plays a fundamental role in plant evolution, the elucidation of polyploid origins is fraught with methodological challenges. For example, allopolyploid species may confound phylogenetic reconstruction because commonly used methods are designed to trace divergent, rather than reticulate patterns. Recently developed techniques of phylogenetic network estimation allow for a more effective identification of incongruence among trees. However, incongruence can also be caused by incomplete lineage sorting, paralogy, concerted evolution, and recombination. Thus, initial hypotheses of hybridization need to be examined via additional sources of evidence, including the partitioning of infraspecific genetic polymorphisms, morphological characteristics, chromosome numbers, crossing experiments, and distributional patterns. Primula sect. Aleuritia subsect. Aleuritia (Aleuritia) represents an ideal case study to examine reticulation because specific hypotheses have been derived from morphology, karyology, interfertility, and distribution to explain the observed variation of ploidy levels, ranging from diploidy to 14-ploidy. Sequences from 5 chloroplast and 1 nuclear ribosomal DNA (nrDNA) markers were analyzed to generate the respective phylogenies and consensus networks. Furthermore, extensive cloning of the nrDNA marker allowed for the identification of shared nucleotides at polymorphic sites, investigation of infraspecific genetic polymorphisms via principal coordinate analyses PCoAs, and detection of recombination between putative progenitor sequences. The results suggest that most surveyed polyploids originated via hybridization and that 2 taxonomic species formed recurrently from different progenitors, findings that are congruent with the expectations of speciation via secondary contact. Overall, the study highlights the importance of using multiple experimental and analytical approaches to disentangle complex patterns of reticulation.

Heterostyly accelerates diversification via reduced extinction in primroses

“…in Primula section Aleuritia [35,51,61,62]) is well established as a major force in angiosperm evolution [63] that potentially impacts diversification rates [64]. However, analyses accounting for polyploidy yielded results that were congruent with analyses agnostic to ploidy level (electronic supplementary material, text S1 and table S3).…”

“…R. Soc. B 281: 20140075 isolation between cytotypes can lead to rapid speciation [51,61,62]. Indeed, the clade within /Primula for which a shift to higher net-diversification rates was detected by MEDUSA (brown clade, figure 2) mainly comprises non-heterostylous, polyploid species, suggesting a link between loss of heterostyly, polyploidy and immediate increases in diversification.…”

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

“…(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).…”

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

“…In addition, interpreting the fate of duplicate genes in polyploids is complicated by the fact that hybridization is often associated with WGD and so it can be difficult to disentangle the effects of combining and duplicating genomes on patterns of duplicate gene expression or dynamics of gene families (e.g., Evans, 2007;Guggisberg et al, 2009;Mable, 2013). Fortunately, rapid advances in sequencing technology and bioinformatic processing mean that the toolbox available to resolve such challenges continues to improve.…”