Assignment of Homoeologs to Parental Genomes in Allopolyploids for Species Tree Inference, with an Example from Fumaria (Papaveraceae)

Abstract

There is a rising awareness that species trees are best inferred from multiple loci while taking into account processes affecting individual gene trees, such as substitution model error (failure of the model to account for the complexity of the data) and coalescent stochasticity (presence of incomplete lineage sorting [ILS]). Although most studies have been carried out in the context of dichotomous species trees, these processes operate also in more complex evolutionary histories involving multiple hybridizations and polyploidy. Recently, methods have been developed that accurately handle ILS in allopolyploids, but they are thus far restricted to networks of diploids and tetraploids. We propose a procedure that improves on this limitation by designing a workflow that assigns homoeologs to hypothetical diploid ancestral genomes prior to genome tree construction. Conflicting assignment hypotheses are evaluated against substitution model error and coalescent stochasticity. Incongruence that cannot be explained by stochastic mechanisms needs to be explained by other processes (e.g., homoploid hybridization or paralogy). The data can then be filtered to build multilabeled genome phylogenies using inference methods that can recover species trees, either in the face of substitution model error and coalescent stochasticity alone, or while simultaneously accounting for hybridization. Methods are already available for folding the resulting multilabeled genome phylogeny into a network. We apply the workflow to the reconstruction of the reticulate phylogeny of the plant genus Fumaria (Papaveraceae) with ploidal levels ranging from 2[Formula: see text] to 14[Formula: see text]. We describe the challenges in recovering nuclear NRPB2 homoeologs in high ploidy species while combining in vivo cloning and direct sequencing techniques. Using parametric bootstrapping simulations we assign nuclear homoeologs and chloroplast sequences (four concatenated loci) to their common hypothetical diploid ancestral genomes. As these assignments hinge on effective population size assumptions, we investigate how varying these assumptions impacts the recovered multilabeled genome phylogeny.

Hybridization and long‐distance colonization in oat‐like grasses of South and East Asia, including an amended circumscription of Helictotrichon and the description of the new genus Tzveleviochloa (Poaceae)

“…They contribute, especially when complemented by plastid DNA data, to establish true species trees in instances where genealogies from different genes are discordant as reported for several groups of grasses (e.g., Danthonioideae, Hordeum L., Oryza L.; Pirie & al., 2009;Brassac & Blattner, 2015;Zwickl & al. 2014) and many other groups of angiosperms (Bertrand & al., 2015;Roy & al., 2015). Discordance may be caused by a number of different processes such as stochastic coalescence of gene lineages within a species phylogeny (incomplete lineage sorting) but also selection, hybridization, horizontal gene transfer, gene duplication/extinction, recombination and phylogenetic estimation error (Reid & al., 2014;Mugrabi de Kuppler & al., 2015).…”

Dating the Species Network: Allopolyploidy and Repetitive DNA Evolution in American Daisies (Melampodium sect. Melampodium, Asteraceae)

“…Hypotheses of parental origin can be tested and refined by genomic in situ hybridization (GISH; i.e., mapping of genomic DNAs of the putative parental taxa to allopolyploid chromosomes; Jang and Weiss-Schneeweiss 2015 ), additionally allowing for the assessment of the extent of interactions between the parental subgenomes in allopolyploids ( Chester et al 2012 , 2015 ; Mandáková et al 2013 , 2014 ). Several phylogenetic methods for reconstructing species networks have been developed that can address, for instance, the assignment of allopolyploid homoeologues to their corresponding parental genomes and building the species networks from multilabeled trees ( Than et al 2008 ; Jones et al 2013 ; Marcussen et al 2012 , 2015 ; Bertrand et al 2015 ). A fully Bayesian approach incorporating assignment of all homoeologues and the multispecies coalescent to reconstruct allopolyploid species networks has recently been developed (AlloppNET and AlloppMUL models of Jones et al 2013 ; Jones 2017 ), but it is currently available only for allotetraploids.…”

“…Various aspects of the mechanisms of allopolyploid formation, including number of origins, the extinction of parental taxa (incomplete sampling) and the presence of multiple subgenomes in a single species complicate and bias a divergence time analysis ( Doyle and Egan 2010 ). Bertrand et al (2015) use the divergence times of parental and allopolyploid alleles in a simple Bayesian model to determine ages for the allopolyploidy events, but this may introduce bias as divergence times of genes do not necessarily correspond to those of the lineages ( Kellogg 2016 ). This issue can be circumvented in the framework of the multispecies coalescent, where under the same assumptions made by most of the previous phylogenetic approaches applied to allopolyploids, that is, extant parental ancestors and disomic inheritance, the allopolyploid subgenomes may be treated as distinct “species” ( Fig.…”

Inferring Patterns of Hybridization and Polyploidy in the Plant GenusPenstemon(Plantaginaceae)

“…Some of these are not coalescent-based, but instead try to reconstruct a network from gene trees that have all of the haplotypes from a polyploid sampled (a so called "multi-labeled" tree; Lott et al 2009;Marcussen et al 2012). Other studies have relied on coalescent-based assignment of homoeologous haplotypes into putative, diploid subgenomes, but these approaches can be computationally limited due to the cost of exploring all permutations of haplotypes assignments (Bertrand et al 2015;Oberpieler et al 2017). The only approach to simultaneously infer a network topology and homoeolog assignment in a coalescent framework is the method of Jones et al (2013).…”