HoloChromEvol Project Holocentric chromosome evolution and the origins of biodiversity in a hyper-diverse plant lineage
The evolution and conservation of biodiversity is at a crossroads: human population growth and development has already wreaked havoc on species diversity and the genetic diversity of populations, affecting evolutionary trajectories of species and whole ecosystems far into the future. At the same time, biodiversity research has seen a surge in visibility, as the public concern for the environment shifts toward an interest in preserving all branches of the tree of life; and in strength, as new genomic and bioinformatics tools for biodiversity research come into increasingly common use. At the heart of biodiversity research is the study of the evolution of species, which is providing exciting new insights into the drivers of biological diversification. Chromosome evolution is one of the most important drivers of biodiversity. Much research into chromosome evolution has focused on physiological and ecological implications of polyploidy. Because polyploidy entails changes in DNA content and gene number, expression differences associated with polyploidization can have dramatic effects on phenotype. Another important body of research has focused on the effects of chromosome inversions on promoting species differentiation through the protection of ecologically significant gene combinations from recombination. Almost completely ignored have been the biodiversity implications of other types of chromosome rearrangements that result in chromosome number changes with little or no change in DNA content (viz., fission and fusion). HoloChromEvol project propose a unique integration of genomic, cytogenetic, and ecological experiments to investigate the effects of chromosome evolution on the biodiversity of the largest flowering plant genus of the temperate zone, the sedges of genus Carex (Cyperaceae). The genus is emerging as a model system for studying chromosomal speciation in holocentric species, species in which the centromere is not a localized structure, but distributed along the entire length of the chromosome. Our research will provide novel insights into the relationship between chromosome evolution, recombination rate, local adaptation, and life history strategies: ultimately, the ecological underpinnings of biodiversity. It will also provide the genomic and genetic resources needed to establish Carex as a model system for understanding chromosome evolution across the tree of life, in all lineages in which chromosome evolution proceeds primarily by fission, fusion, and translocations. The overarching goal of our long-term research program is to elucidate how chromosome evolution affects biodiversity patterns across the tree of life. HoloChromEvol is an important key to this goal, and will place us in a position to make substantial, career-long contributions in the field of biodiversity science. Through an integration of cutting-edge genomic and ecological experiments in a hyper-diverse flowering plant genus with exceptional chromosomal variation, this project will tease apart the mechanisms by which holocentric chromosome evolution drives genetic diversification and identify the population dynamic elements that allow for chromosomal diversification in sedges. The result will be a model of diversification in this keystone genus that integrates the dynamics of population establishment, migration, and persistence with the chromosomal and genomic architecture of population divergence.
Background: holocentric chromosomes In holocentric chromosomes—chromosomes with diffuse centromeres—microtubule attachment during mitosis is distributed along the length of the chromosome. In contrast, monocentric chromosomes have microtubule attachment localized to one region. Holocentric chromosome organization has been described for three of the six supergroups in the domain Eukarya (the Eukaryotes): plants (angiosperms, algae and mosses); animals (at least six numerous arthropod clades, plus velvet worms and nematodes); and Rhizaria. It has long been recognized that chromosome fragments that would be lost in monocentric chromosomes may be propagated and become fixed in organisms with holocentric chromosomes, and inherited in Mendelian fashion. Likewise, chromosomes resulting from fusion of two holocentric chromosomes typically align and segregate correctly, whereas in organisms with monocentric chromosomes, the linkage of two chromosomes often results in the formation of dicentric chromosomes that fail to segregate properly. The result is tremendous variation in rates of chromosome evolution, including hyper-variable groups such as Agrodiaetus butterflies (2n = 10 to 250) and sedges (2n = 4 to 226). The implications of holocentry are potentially profound, but largely unstudied. In Lepidoptera, phylogenetic comparative evidence suggests that chromosome rearrangements that accrue in allopatry play a role in reinforcing speciation. In the sedge genus Carex (Cyperaceae), chromosome rearrangements contribute to genetic diversity within species as well as lineage diversification, suggesting that holocentry is an important determinant of biodiversity patterns. But as yet, no experimental studies have confirmed experimentally that chromosome diversification drives biodiversity patterns in holocentric clades. HoloChromEvol project will fill this gap, as the first study to test the mechanism by which chromosome rearrangements affect patterns of gene flow among populations, and subsequently speciation, the engine of biodiversity.
Why Carex? Carex has several properties that make it an ideal model for testing the evolutionary implications of holocentric chromosome rearrangements: 1. Exceptionally high rate of chromosome rearrangements. Carex exhibits exceptionally high chromosome diversity, even among holocentric lineages. The two species focused on in this project (Carex scoparia and C. laevigata) exhibit high chromosome number variation. In C. scoparia, we find chromosome variants in nearly every population we study, and a phenomenal diversification among populations that diverged from each other less than 15,000 years ago. Moreover, this variation is known to be due to fissions and fusions, not polyploidy. In Carex, we are truly capturing a snapshot of chromosome speciation in process, not studying it after-the-fact. 2. High species and lineage diversity. At more than 2,000 species, Carex is among the four most speciesrich angiosperm genera worldwide. The genus’s center of diversity lies in the temperate regions of northern Hemisphere, where it dominates a wide range of wetland plant communities, and it is one of the richest angiosperm genera in North America (ca. 500 species) and the European Union (ca. 250 species). This diversity makes Carex both an important genus from a conservation standpoint and an ideal system for studying how chromosome evolution affects processes and rates of species diversification. 3. Amenable to experimentation. Our proposed study entails crosses and hybridization and F1 and F2 generation which are much more easily executed with non-woody plants than with woody plants or animals. Ability to grow plants in greenhouses for genotyping and second-generation crosses is crucial to understanding how these chromosome rearrangements affect recombination rates and diversification.