Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae). New Phytol

Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide University, Seville, Spain.
New Phytologist (Impact Factor: 7.67). 04/2012; 195(1):237-47. DOI: 10.1111/j.1469-8137.2012.04137.x
Source: PubMed

ABSTRACT • Changes in chromosome number as a result of fission and fusion in holocentrics have direct and immediate effects on the recombination rate. We investigate the support for the classic hypothesis that environmental stability selects for increased recombination rates. • We employed a phylogenetic and cytogenetic data set from one of the most diverse angiosperm genera in the world, which has the largest nonpolyploid chromosome radiation (Carex, Cyperaceae; 2n = 12-124; 2100 spp.). We evaluated alternative Ornstein-Uhlenbeck models of chromosome number adaptation to the environment in an information-theoretic framework. • We found moderate support for a positive influence of lateral inflorescence unit size on chromosome number, which may be selected in a stable environment in which resources for reproductive investment are larger. We found weak support for a positive influence on chromosome number of water-saturated soils and among-month temperature constancy, which would be expected to be negatively select for pioneering species. Chromosome number showed a strong phylogenetic signal. • We argue that our finding of small but significant effects of life history and ecology is compatible with our original hypothesis regarding selection of optima in recombination rates: low recombination rate is optimal when inmediate fitness is required. By contrast, high recombination rate is optimal when stable environments allow for evolutionary innovation.

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Available from: Marcial Escudero, Sep 04, 2015
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    • "amphiatlantic, bipolar, Gondwanan; Raymond, 1951; Croizat, 1952) and intriguing cytology (holocentric chromosomes: N = 6 to 56; Davies, 1956). These characteristics should make Cariceae an ideal system for studying the evolution of biodiversity, and studies are increasingly focusing on biogeographical, ecological, and evolutionary questions (Escudero et al., 2010, 2012a, b; Gehrke & Linder, 2011). However, characteristics such as their cosmopolitan distribution, high diversity, and, "
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    ABSTRACT: With approximately 2000 species, tribe Cariceae (Cyperaceae) comprises a morphologically distinctive cosmopolitan clade, with holocentric chromosomes (N = 6 to 56), complex biogeographical patterns, and habitat diversity ranging from rainforests to deserts. Such a remarkable combination of characteristics should make Cariceae an ideal model for studying the evolution of biodiversity, although they also obscure their relationships in Cyperaceae, complicating attempts to identify the contributing factors to diversity of Cariceae. Recent molecular studies place Cariceae in a strongly supported clade consisting of tribes Dulichieae, Scirpeae s.s, and the enigmatic monotypic genus Khaosokia, although relationships in this clade are unresolved. Using the plastid genes matK and ndhF and a greatly improved taxonomic sampling covering 16 of 17 genera and 55% of the species outside Cariceae, our analyses firmly position Dulichieae and Khaosokia (79% and 85% bootstrap support) as successive sisters to a clade consisting of five major lineages (Calliscirpus, Trichophorum + Oreobolopsis + Cypringlea, Cariceae, Scirpus + Eriophorum, and Amphiscirpus + Phylloscirpus + Zameioscirpus), the first four of which receive good to strong support (> 80% bootstrap support). Cariceae are sister to the Trichophorum clade, although topological tests cannot exclude either Calliscirpus or a Scirpus clade + Zameioscirpus clade as sister to the tribe. Trichophorum appears to be paraphyletic and Eriophorum is firmly nested in Scirpus. There appears to be a trend in the increase of chromosome numbers in Scirpus and Eriophorum and a trend in the reduction and proliferation of the inflorescence throughout the major Cariceae-Dulichieae-Scirpeae clades. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, ●●, ●●–●●.
    Botanical Journal of the Linnean Society 09/2014; 176(1). DOI:10.1111/boj.12193 · 2.70 Impact Factor
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    • "Reduced-representation sequencing datasets nonetheless have collective potential to detect many informative markers across the genome. With more than 2000 species, Carex (Cyperaceae) is one of the most species-rich genera of angiosperms (Judd et al., 2007) and the most diverse in the northern temperate zone (Escudero et al., 2012). Several recent studies have illuminated important mechanisms that shape Carex population genetic structure and are potential drivers of diversification: isolation-by-distance (Escudero et al., 2010b; Gehrke and Linder, 2011; Jiménez- Mejías et al., 2011); long-distance dispersal and vicariance (Escudero et al., 2010b,c, 2009; Gehrke and Linder, 2011; Jiménez-Mejías et al., 2012, 2011); self-compatibility and high selfing rates (Arens et al., 2005; Escudero et al., 2010b; Friedman and Barrett, 2009; Whitkus, 1988b); chromosome differentiation (Escudero et al., 2013a,b; 2012a,b, 2010a; Hipp, 2007; Hipp et al., 2010; Jiménez-Mejías et al., 2011; Whitkus, 1988a; and current or ancestral hybridization and introgression (Cayouette and Catling, 1992; Dragon and Barrington, 2009; Hipp et al., 2006; Jiménez- Mejías et al., 2011). "
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    ABSTRACT: Determining phylogenetic relationships among very closely related species has remained a challenge for evolutionary biologists due to interlocus phylogenetic discordance and the difficulty of obtaining variable markers. Here, we used a Genotyping-by-Sequencing (GBS) approach to sample a reduced representation genomic data set and infer the phylogeny of seven closely related species in the genus Carex (Cyperaceae). Past attempts to reconstruct phylogenetic relationships among these species produced conflicting and poorly-supported results. We inferred a robust phylogeny based on >3,000 GBS loci and >1,300 SNPs (with a minimum sequence depth within individuals of 10) using maximum likelihood and Bayesian inference. We also tested for historical introgression using the D-statistic test. We compared these analyses with partitioned RAD analysis, which is designed to identify suboptimal trees reflecting secondary phylogenetic signal that may be obscured by the dominant signal in the data. Phylogenetic analyses yielded fully resolved trees with high support. We found two main clades, one grouping Carex scoparia populations and C. waponahkikensis, and a second clade grouping C. longii, C. vexans, C. suberecta and C. albolutescens. We detected marginal significant signals of introgression between C. scoparia and C. suberecta or C. albolutescens, and we rejected a hybrid origin hypothesis for C. waponahkikensis. Our results demonstrate the power of NGS data sets for resolving some of the most difficult phylogenetic challenges where traditional phylogenetic markers have failed.
    Molecular Phylogenetics and Evolution 07/2014; 79. DOI:10.1016/j.ympev.2014.06.026 · 4.02 Impact Factor
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    • "The holokinetic structure of chromosomes allows only one or two cross-overs per chromosome, regardless of their size (Nordenskiöld 1962; Nokkala et al. 2004; Monen et al. 2005); therefore, the selection for a higher or lower recombination rate would favor chromosome fissions or fusions, respectively (Escudero et al. 2012; Bureš et al. 2013). Indeed, the selection on lower numbers of chromosomes (i.e., a lower recombination rate) to preserve advantageous allelic combinations in species growing in unstable habitats has been documented in the genus Carex, although this selection only explained a small portion of the overall karyotype variation in the genus (Escudero et al. 2012). Natural selection might also favor adaptive mutations that are generated by the amplification of TE and might enlarge the holokinetic chromosomes as a side effect (Zedek et al. 2010), which would contribute to the chromosomal size divergence (Fig. 1B). "
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    ABSTRACT: Similar to how the model of centromere drive explains the size and complexity of centromeres in monocentrics (organisms with localized centromeres), our model of holokinetic drive is consistent with the divergent evolution of chromosomal size and number in holocentrics (organisms with non-localized centromeres) exhibiting holokinetic meiosis (holokinetics). Holokinetic drive is proposed to facilitate chromosomal fission and/or repetitive DNA removal (or any segmental deletion) when smaller homologous chromosomes are preferentially inherited or chromosomal fusion and/or repetitive DNA proliferation (or any segmental duplication) when larger homologs are preferred. The hypothesis of holokinetic drive is supported primarily by the negative correlation between chromosome number and genome size that is documented in holokinetic lineages. The supporting value of two older cross-experiments on holokinetic structural heterozygotes (the rush Luzula elegans and butterflies of the genus Antheraea) that indicate the presence of size-preferential homolog transmission via female meiosis for holokinetic drive is discussed, along with the potential negative consequences of holokinetic drive in comparison with centromere drive. This article is protected by copyright. All rights reserved.
    Evolution 04/2014; 68(8). DOI:10.1111/evo.12437 · 4.66 Impact Factor
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