Seeing through the hedge: Phylogenomics of Thuja (Cupressaceae) reveals prominent incomplete lineage sorting and ancient introgression for Tertiary relict flora

Abstract

The Eastern Asia (EA) -North America (NA) disjunction is a well-known biogeographic pattern of the Tertiary relict flora; however, few studies have investigated the evolutionary history of this disjunction using a phylogenomic approach. Here, we used 2369 single copy nuclear genes and nearly full plastomes to reconstruct the evolutionary history of the small Tertiary relict genus Thuja, which consists of five disjunctly distributed species. The nuclear species tree strongly supported an EA clade Thuja standishii-Thuja sutchuenensis and a "disjunct clade", where western NA species T. plicata is sister to an EA-eastern NA disjunct Thuja occidentalis-Thuja koraiensis group. Our results suggested that the observed topological discordance among the gene trees as well as the cytonuclear discordance is mainly due to incomplete lineage sorting, probably facilitated by the fast diversification of Thuja around the Early Miocene and the large effective population sizes of ancestral lineages. Furthermore, approximately 20% of the T. sutchuenensis nuclear genome is derived from an unknown ancestral lineage of Thuja, which might explain the close resemblance of its cone morphology to that of an ancient fossil species. Overall, our study demonstrates that single genes may not resolve interspecific relationships for disjunct taxa, and that more reliable results will come from hundreds or thousands of loci, revealing a more complex evolutionary history. This will steadily improve our understanding of their origin and evolution.

When tropical and subtropical congeners met: Multiple ancient hybridization events within Eriobotrya in the Yunnan‐Guizhou Plateau, a tropical‐subtropical transition area in China

“…Incongruence among gene trees can be explained by introgressive hybridization or incomplete lineage sorting (ILS) (Maddison, 1997). To test whether ILS alone can explain incongruence between chloroplast and nuclear phylogenetic trees, DendroPy 4.4.0 (Sukumaran & Holder, 2010) was applied to simulate 20,000 chloroplast trees under the coalescent scenario, using the species tree as a guide tree with branch lengths scaled by four to account for the fact that any uniparentally inherited organelle genome has one fourth of the effective population size of the biparentally inherited autosomal nuclear genes (Folk et al, 2017; Li et al, 2021). The clade frequency of the simulated chloroplast genes was summarized on an empirical chloroplast tree with Phyparts (Smith et al, 2015).…”

Detection of Ghost Introgression from Phylogenomic Data Requires a Full-Likelihood Approach

“…The simulation studies conducted by Tricou et al (2022bTricou et al ( , 2022a suggest that ghost introgressions are probably more likely to occur than ingroup introgressions. In recent years, empirical evidence for ghost introgression begins to appear in phylogenomic datasets such as those on Jaltomata species (Tiley et al 2023) and on Thuja species (Li et al 2022). But it is notable that most of such studies relied heavily on heuristic methods such as PhyloNet/MPL and SNaQ as they are computationally tractable for large-scale genomic data involving more than a few taxa.…”

“…We also reanalyzed the ghost introgression event among Thuja species as discovered by Li et al (2022) (more details given in Supplementary Note 3 and Table S4). Our results, which were obtained using the selected species trio, indicated once again that HyDe and PhyloNet/MPL performed poorly, while BPP provided strong evidence in favor of the ghost introgression model, a conclusion also drawn from analyzing all Thuja species using PhyloNet/MPL in the original study.…”

“…introgression in plants (e.g., Ding et al 2022;Li et al 2022;Tiley et al 2023) and animals (e.g., Ai et al 2015;Kuhlwilm et al 2019;Rocha et al 2022), including humans (Green et al 2010;Sankararaman et al 2014).…”

Hyb‐Seq provides new insights into the phylogeny and evolution of the Chrysanthemum zawadskii species complex in China

“…Additionally, because Hyb‐Seq can be applied to historical specimens, as well as to existing nonmodel organisms, it has been used extensively in plant phylogenetics (Prata et al., 2018; Tomasello et al., 2020; Villaverde et al., 2018). Therefore, an integrative study using Hyb‐Seq data, species distribution modelling (SDM) and morphological comparisons can more powerfully infer phylogenetic relationships and the evolutionary history of a species complex than can previous techniques (Ennos et al., 2005; Hendry et al., 2009; Li et al., 2022; Mee et al., 2015; Mérot et al., 2017; Sytsma and Schaal, 1985; Tomasello et al., 2020; Zhou et al., 2012).…”