Phylogenomic Relationships of Diploids and the Origins of Allotetraploids in Dactylorhiza (Orchidaceae).

Marie K Brandrud,Ovidiu Paun,Maria T Lorenzo,Mark W Chase,Mikael Hedrén,Richard M Bateman,Alexander Athanasiadis,Juliane Baar,Vincent Savolainen

doi:10.1093/sysbio/syz035

Marie K Brandrud, Ovidiu Paun + Show 7 more

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https://doi.org/10.1093/sysbio/syz035

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Abstract

Disentangling phylogenetic relationships proves challenging for groups that have evolved recently, especially if there is ongoing reticulation. Although they are in most cases immediately isolated from diploid relatives, sets of sibling allopolyploids often hybridize with each other, thereby increasing the complexity of an already challenging situation. Dactylorhiza (Orchidaceae: Orchidinae) is a genus much affected by allopolyploid speciation and reticulate phylogenetic relationships. Here, we use genetic variation at tens of thousands of genomic positions to unravel the convoluted evolutionary history of Dactylorhiza. We first investigate circumscription and relationships of diploid species in the genus using coalescent and maximum likelihood methods, and then group 16 allotetraploids by maximum affiliation to their putative parental diploids, implementing a method based on genotype likelihoods. The direction of hybrid crosses is inferred for each allotetraploid using information from maternally inherited plastid RADseq loci. Starting from age estimates of parental taxa, the relative ages of these allotetraploid entities are inferred by quantifying their genetic similarity to the diploids and numbers of private alleles compared with sibling allotetraploids. Whereas northwestern Europe is dominated by young allotetraploids of postglacial origins, comparatively older allotetraploids are distributed further south, where climatic conditions remained relatively stable during the Pleistocene glaciations. Our bioinformatics approach should prove effective for the study of other naturally occurring, nonmodel, polyploid plant complexes.

Highlights

IntroductionUnderstanding evolutionary histories is further complicated by hybrid and polyploid entities that exhibit mixed ancestral alleles and inheritance (Dufresne et al 2014; Meirmans et al 2018)
Whereas northwestern Europe is dominated by young allotetraploids of postglacial origins, comparatively older allotetraploids are distributed further south, where climatic conditions remained relatively stable during the Pleistocene glaciations
We explore the utility of restriction site-associated DNA sequencing (RADseq; Baird et al 2008) for inferring evolutionary patterns in an orchid genus (Dactylorhiza Necker ex Nevski) that comprises numerous allotetraploids, an autotetraploid, and their putative diploid progenitors

Summary

Introduction

Understanding evolutionary histories is further complicated by hybrid and polyploid entities that exhibit mixed ancestral alleles and inheritance (Dufresne et al 2014; Meirmans et al 2018). As sequentially produced allotetraploids may subsequently interbreed, genetic diversity and genome complexity of these allopolyploids is enhanced (Soltis and Soltis 1999; Soltis et al 2014). In some cases, such recurrently produced allopolyploids establish independent species that remain genetically distinct, even in sympatry, for example in Achillea (Guo et al 2013), Asplenium (Perrie et al 2010), Leucaena (Govindarajulu et al 2011), and Oryza (Zou et al 2015). The parental taxa of allopolyploids typically have been genetically isolated for a relatively long period (e.g., Paun et al 2009). RADseq has been estimated to be useful for resolving divergences as old as 63 myr (Cariou et al 2013; Heckenhauer et al 2018), while efficiently resolving recently radiating groups (e.g., Cruaud et al 2014; Paun et al 2016; Trucchi et al 2017; Bateman et al 2018b; Brandrud et al 2019)

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