Abstract:Changes in chromosome numbers, including polyploidy and dysploidy events, play a key role in eukaryote evolution as they could expediate reproductive isolation and have the potential to foster phenotypic diversification. Deciphering the pattern of chromosome-number change within a phylogeny currently relies on probabilistic evolutionary models. All currently available models assume time homogeneity, such that the transition rates are identical throughout the phylogeny.Here, we develop heterogeneous models of c… Show more
“…Carex-the largest genus in Cyperaceae-is particularly well suited to studying the effect of dysploidy on plant diversification because all Carex have holocentric chromosomes, the genus represents 40% of the third most species-rich monocot family (among the tenth in angiosperms, POWO 2023) and well-developed phylogenetic and chromosome number datasets for the genus to facilitate macroevolutionary studies (Martín-Bravo et al 2019. In Carex, karyotype evolves mainly through fusion, fission, and translocations, in contrast to in other sedge lineages where karyotype evolves through both dysploidy and polyploidy (Márquez-Corro, Martín-Bravo, Spalink, Luce ño & Escudero 2019, Elliott et al 2022, Shafir et al 2023. Carex also has exceptional variability in chromosome number, ranging from 2n = 10 to 2n = 132 (Márquez-Corro et al 2021).…”
Section: Dysploidy and Holocentric Chromosomesmentioning
Recent studies of angiosperm diversification have focused on the role of polyploidy as a driver of diversification. However, we know far less about the effects of single changes in chromosome number---dysploidy, which can mediate lineage diversification by affecting recombination rates, linkage, and/or reproductive isolation. Modeling the effects of dysploidy on diversification is mathematically and computationally challenging because many states and parameters are required to track changes in individual chromosomes, especially in lineages that have high variability in chromosome number. Additionally, we expect the processes of diversification and dysploidy to vary across clades, which requires modeling process variation to disentangle the effects of the observed trait (chromosome number) from the effects of unobserved traits on diversification. In this work, we propose a new state-dependent diversification model of chromosome evolution that includes numerous character states and explicitly models heterogeneity in the diversification process. Our model includes parameters that functionally link diversification rates to dysploidy rates and differentiate between anagenetic and cladogenetic changes. We apply this model to Carex (Cyperaceae), a model lineage for understanding dysploidy and diversification, leveraging chromosome number information and the most recent time-calibrated phylogenetic tree for over 700 species and subspecies. We recover distinct modes of chromosomal speciation across Carex. In one mode, dysploidy occurs very frequently and drives faster diversification rates. In the other mode, dysploidy is rare and diversification is driven by other factors, unmeasured in our analysis. This study is the first to demonstrate that dysploidy drives diversification in plants while considering unmeasured factors affecting diversification.
“…Carex-the largest genus in Cyperaceae-is particularly well suited to studying the effect of dysploidy on plant diversification because all Carex have holocentric chromosomes, the genus represents 40% of the third most species-rich monocot family (among the tenth in angiosperms, POWO 2023) and well-developed phylogenetic and chromosome number datasets for the genus to facilitate macroevolutionary studies (Martín-Bravo et al 2019. In Carex, karyotype evolves mainly through fusion, fission, and translocations, in contrast to in other sedge lineages where karyotype evolves through both dysploidy and polyploidy (Márquez-Corro, Martín-Bravo, Spalink, Luce ño & Escudero 2019, Elliott et al 2022, Shafir et al 2023. Carex also has exceptional variability in chromosome number, ranging from 2n = 10 to 2n = 132 (Márquez-Corro et al 2021).…”
Section: Dysploidy and Holocentric Chromosomesmentioning
Recent studies of angiosperm diversification have focused on the role of polyploidy as a driver of diversification. However, we know far less about the effects of single changes in chromosome number---dysploidy, which can mediate lineage diversification by affecting recombination rates, linkage, and/or reproductive isolation. Modeling the effects of dysploidy on diversification is mathematically and computationally challenging because many states and parameters are required to track changes in individual chromosomes, especially in lineages that have high variability in chromosome number. Additionally, we expect the processes of diversification and dysploidy to vary across clades, which requires modeling process variation to disentangle the effects of the observed trait (chromosome number) from the effects of unobserved traits on diversification. In this work, we propose a new state-dependent diversification model of chromosome evolution that includes numerous character states and explicitly models heterogeneity in the diversification process. Our model includes parameters that functionally link diversification rates to dysploidy rates and differentiate between anagenetic and cladogenetic changes. We apply this model to Carex (Cyperaceae), a model lineage for understanding dysploidy and diversification, leveraging chromosome number information and the most recent time-calibrated phylogenetic tree for over 700 species and subspecies. We recover distinct modes of chromosomal speciation across Carex. In one mode, dysploidy occurs very frequently and drives faster diversification rates. In the other mode, dysploidy is rare and diversification is driven by other factors, unmeasured in our analysis. This study is the first to demonstrate that dysploidy drives diversification in plants while considering unmeasured factors affecting diversification.
“…For example, polyploidy occurrence is strikingly low in the Carex genus, despite the high volume of species diversity (∼2,000) and an exceptional chromosome number variation (2 n = 10 to 132) ( Márquez-Corro et al 2021 ). However, it may not hold for other Cyperid species, as the chromosome number could evolve at heterogeneous rates along different clades ( Márquez-Corro et al 2019 ; Shafir et al 2023 ). Notably, previous studies have provided some clues for polyploidization in the Schoenoplectus genus.…”
Schoenoplectus tabernaemontani (C. C. Gmelin) Palla is a typical macrophyte in diverse wetland ecosystems. This species holds great potential in decontamination applications and carbon sequestration. Previous studies have shown that this species may have experienced recent polyploidization. This would make S. tabernaemontani a unique model to study the processes and consequences of whole genome duplications in the context of the well-documented holocentric chromosomes and dysploidy events in Cyperaceae. However, the inference was not completely solid because it lacked homology information which is essential to ascertain polyploidy. We present here the first chromosome-level genome assembly for S.tabernaemontani. By combining ONT long-reads and Illumina short-reads, plus chromatin conformation via the Hi-C method, we assembled a genome spanning 507.96 Mb, with 99.43% of Hi-C data accurately mapped to the assembly. The assembly contig N50 value was 3.62 Mb. The overall BUSCO score was 94.40%. About 68.94% of the genome was comprised of repetitive elements. 36994 protein-coding genes were predicted and annotated. Long terminal repeat retrotransposons (LTR-rts) accounted for approximate 26.99% of the genome, surpassing the content observed in most sequenced Cyperid genomes. Our well-supported haploid assembly comprised 21 pseudochromosomes, each harboring putative holocentric centromeres. Our findings corroborated a karyotype of 2n=2X=42. We also confirmed a recent whole genome duplication (WGD) occurring after the divergence between Schoenoplecteae and Bolboschoeneae. Our genome assembly expands the scope of sequenced genomes within the Cyperaceae family, encompassing the fifth genus. It also provides research resources on Cyperid evolution and wetland conservation.
“…Accordingly, botanists often study chromosome number evolution within their clades of interest. The Mayrose group at Tel‐Aviv University has developed several open resources that facilitate research into the diversity and evolution of chromosome number in plants: (1) chrom E vol (Mayrose et al ., 2010; Glick & Mayrose, 2014; Shafir et al ., 2023), a program that models the evolution of chromosome numbers along a phylogeny; (2) The Chromosome Counts Database (CCDB; Rice et al ., 2015), a regularly updated database of plant chromosome counts; and (3) O ne T wo T ree (OTT; Drori et al ., 2018), an online resource for automated phylogeny reconstruction.‘P loi DB is a highly useful synthesis of existing resources that will help generate hypotheses and enable novel, broad‐scale studies of polyploidy in spermatophytes.’…”
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confidence: 99%
“…In some cases, the authors rightly excluded datasets where this modeling approach has been shown to be inadequate (e.g. in Cyperaceae, which have holocentric chromosomes and heterogeneous patterns of dysploid evolution; Shafir et al ., 2023). This approach may also fail in groups where other data are critical for understanding the history of WGDs.…”
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