Professor Dmitry Filatov
Population genetics and molecular evolution
The overarching aim of my research is to understand how the evolutionary processes shape the world around us. More specifically, I’m interested in how evolutionary forces, such as natural selection, drive the change at the levels of genes and genomes. I’ve been developing two main directions of research: (i) genome evolution (with the focus on evolution of sex chromosomes) and (ii) the speciation and adaptation processes in plants (in the wide sense – including phytoplankton, see below). Over the years these research directions have been funded grants from the BBSRC, NERC and the Leverhulme Trust.
Sex chromosome evolution
Males and females differ significantly in their appearance, behaviour and physiology (they are sexually dimorphic). This is more surprising than it may seem as the two sexes share almost identical sets of genes. It is thought that cosexual/hermaphroditic state is ancestral and separate males and females evolved later, which happened many times independently in different organismal groups. How long does it take to evolve sexual dimorphism when a species switches from a hermaphroditic state to separate sexes (dioecy)? What happens at the genome level when such transition occurs? We are addressing these questions using White Campion (Silene latifolia), a plant that evolved separate sexes and sex chromosomes (determining development as a male or a female) only a few million years ago (MYA) – much more recently compared to sex chromosomes in mammals (including humans; ~160MYA) and birds (~100 MYA). Recent origin of sex chromosomes in White Campion makes it particularly useful for studying the early evolutionary stages, as well as the generality of evolutionary forces that drive independent evolution of sex chromosomes in different life forms.
The most significant of our findings include the discovery that alteration of generations in the plant life cycle leads to different dynamics in sex chromosome evolution in plants, compared to animals (Chibalina and Filatov 2011 Current Biology). We discovered that plant Y-chromosomes are undergoing genetic degeneration (Filatov et al 2000 Nature; Papadopulos et al 2015 PNAS) and that this Y-degeneration is already balanced by dosage compensation system that arose surprisingly early in the history of plant sex chromosomes (Papadopulos et al 2015 PNAS). These findings are important because they shed light on evolutionary processes shaping sex chromosomes at the very early stage of their evolution. These processes were only hypothesised or inferred, but could not be studied directly in humans or other mammals that have very old (~165 million years) sex chromosomes. Our work on much younger (<10million years old) plant sex chromosomes revealed that the same or very similar evolutionary processes are driving independent evolution of sex chromosomes in plant and animal kingdoms, albeit the fundamental differences in plant and animal lifecycle cause differences in evolutionary dynamics between the kingdoms.
Adaptation and speciation
Ecological speciation of Senecio on Mt Etna: It is often assumed (by non-specialists) that species are separate entities and hybridisation between them is rare, if at all possible. Indeed, until recently this was the predominant view even among the scholars in speciation field (e.g. E. Mayr). In fact, most closely related species (particularly in plants) can, and often do hybridise, and interspecific gene flow can be quite active. What role does this gene exchange between the species play in adaptation and speciation? I’ve been focusing on this question using a pair of closely related Senecio (ragwort) species adapted to different altitudes on Mt. Etna, Sicily. This volcano has rapidly risen in the last half-million years. We demonstrated that the high- and low-altitude Senecio species have diverged within this period and adapted to contrasting conditions at the top and bottom of the volcano despite on-going hybridisation at intermediate altitudes (Chapman et al 2013; Muir et al 2013; Osborne et al 2013; Filatov et al 2016). We discovered that dramatic ecological and phenotypic differences between the high- and low- altitude species have evolved due to strong selection at only few key genes, while the rest of the genome shows no differences between these species (Chapman et al 2016). This project is being developed in collaboration with the director of the Oxford Botanic Garden, Prof. Hiscock.
Rapid plant radiations: Another fundamental question we are addressing in our work is why some groups of organisms are incredibly diverse and species rich (e.g. there are thousands of beetle species), while the other fairly ancient branches of the tree of life are represented by only one (e.g. ginkgo) or a few species. In particular, we are studying what evolutionary processes drive and accompany rapid adaptive radiations – near simultaneous formation of many species in a short evolutionary time. Many major organismal groups, including most of modern birds (Neoaves) and flowering plants, have formed during such ‘bursts of speciation’. To understand the evolutionary processes during such events we are focusing on very recent (and possibly on-going) rapid plant radiations, such as found on isolated oceanic islands (e.g. Hawaii), or rapidly rising mountain ranges (e.g. Andes). While previous work has focused mainly on phenotypic evolution (e.g. beak size in Darwin’s finches) during adaptive specie radiations, very little is known about selective pressures at the level of individual genes involved in adaptations. We studied this question using a handful of genes in Hawaiian endemic genus Schiedea (Kapralov et al 2013) and now have scaled up to the whole genome analysis in New World lupins that formed independent extensive species radiations in the Andes as well as in Central and North America. We discovered a dramatic difference in the amount and strength of adaptive evolution across the genome between rapidly and slowly diversifying groups of lupin species (in prep). The lupin adaptation and speciation project was developed in collaboration with Dr Colin Hughes (Univ. Zurich), who is an expert in lupin taxonomy.
Adaptation and speciation in marine phytoplankton: Photosynthesis in marine phytoplankton is responsible for about half of newly produced organic matter on the planet. The amount of CO2 they fix in this process is thought to significantly affect the global carbon cycle and climate. Yet, surprisingly little is known about how new plankton species originate and adapt to ever changing environment. While evolutionary process in terrestrial populations have been actively studied in many animal and plant species, little is known about population genetic processes underpinning adaptation and speciation in astronomically large populations of marine plankton species. To address this gap in our knowledge, we combine fossil and climatic records from the late Quaternary with genome-wide evolutionary genetic analyses of adaptation and speciation in a major group of oceanic phytoplankton, the coccolithophores (Haptophyta; see Bendif et al 2019 Nature Comm).
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Evolution of mutation rate in astronomically large phytoplankton populations
July 2020|Journal article|al Genome Biology and Evolution -
The Location of the Pseudoautosomal Boundary in Silene latifolia
May 2020|Journal article|Genes<jats:p>Y-chromosomes contain a non-recombining region (NRY), and in many organisms it was shown that the NRY expanded over time. How and why the NRY expands remains unclear. Young sex chromosomes, where NRY expansion occurred recently or is on-going, offer an opportunity to study the causes of this process. Here, we used the plant Silene latifolia, where sex chromosomes evolved ~11 million years ago, to study the location of the boundary between the NRY and the recombining pseudoautosomal region (PAR). The previous work devoted to the NRY/PAR boundary in S. latifolia was based on a handful of genes with locations approximately known from the genetic map. Here, we report the analysis of 86 pseudoautosomal and sex-linked genes adjacent to the S. latifolia NRY/PAR boundary to establish the location of the boundary more precisely. We take advantage of the dense genetic map and polymorphism data from wild populations to identify 20 partially sex-linked genes located in the “fuzzy boundary”, that rarely recombines in male meiosis. Genes proximal to this fuzzy boundary show no evidence of recombination in males, while the genes distal to this partially-sex-linked region are actively recombining in males. Our results provide a more accurate location for the PAR boundary in S. latifolia, which will help to elucidate the causes of PAR boundary shifts leading to NRY expansion over time.</jats:p> -
Senecio as a model system for integrating studies of genotype, phenotype and fitness.
January 2020|Journal article|The New phytologistTwo major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories and morphologies, and occupy a multitude of environments. Common within the genus are species that have hybridised naturally, undergone polyploidisation, and colonised diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology.Senecio, hybrid speciation, Asteraceae, model system, adaptive radiation, self-incompatibility, genomics, quantitative genetics -
Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna.
January 2020|Journal article|Molecular ecologyRecently diverged species present particularly informative systems for studying speciation and maintenance of genetic divergence in the face of gene flow. We investigated speciation in two closely related Senecio species, S. aethnensis and S. chrysanthemifolius, which grow at high and low elevations, respectively, on Mount Etna, Sicily and form a hybrid zone at intermediate elevations. We used a newly generated genome-wide single nucleotide polymorphism (SNP) dataset from 192 individuals collected over 18 localities along an elevational gradient to reconstruct the likely history of speciation, identify highly differentiated SNPs, and estimate the strength of divergent selection. We found that speciation in this system involved heterogeneous and bidirectional gene flow along the genome, and species experienced marked population size changes in the past. Furthermore, we identified highly-differentiated SNPs between the species, some of which are located in genes potentially involved in ecological differences between species (such as photosynthesis and UV response). We analysed the shape of these SNPs' allele frequency clines along the elevational gradient. These clines show significantly variable coincidence and concordance, indicative of the presence of multifarious selective forces. Selection against hybrids is estimated to be very strong (0.16-0.78) and one of the highest reported in literature. The combination of strong cumulative selection across the genome and previously identified intrinsic incompatibilities probably work together to maintain the genetic and phenotypic differentiation between these species - pointing to the importance of considering both intrinsic and extrinsic factors when studying divergence and speciation.Senecio, Adaptation, Physiological, Gene Frequency, Polymorphism, Single Nucleotide, Gene Flow -
Evolution of Codon Usage Bias in Diatoms.
November 2019|Journal article|GenesCodon usage bias (CUB)-preferential use of one of the synonymous codons, has been described in a wide range of organisms from bacteria to mammals, but it has not yet been studied in marine phytoplankton. CUB is thought to be caused by weak selection for translational accuracy and efficiency. Weak selection can overpower genetic drift only in species with large effective population sizes, such as Drosophila that has relatively strong CUB, while organisms with smaller population sizes (e.g., mammals) have weak CUB. Marine plankton species tend to have extremely large populations, suggesting that CUB should be very strong. Here we test this prediction and describe the patterns of codon usage in a wide range of diatom species belonging to 35 genera from 4 classes. We report that most of the diatom species studied have surprisingly modest CUB (mean Effective Number of Codons, ENC = 56), with some exceptions showing stronger codon bias (ENC = 44). Modest codon bias in most studied diatom species may reflect extreme disparity between astronomically large census and modest effective population size (Ne), with fluctuations in population size and linked selection limiting long-term Ne and rendering selection for optimal codons less efficient. For example, genetic diversity (pi ~0.02 at silent sites) in Skeletonema marinoi corresponds to Ne of about 10 million individuals, which is likely many orders of magnitude lower than its census size. Still, Ne ~107 should be large enough to make selection for optimal codons efficient. Thus, we propose that an alternative process-frequent changes of preferred codons, may be a more plausible reason for low CUB despite highly efficient selection for preferred codons in diatom populations. The shifts in the set of optimal codons should result in the changes of the direction of selection for codon usage, so the actual codon usage never catches up with the moving target of the optimal set of codons and the species never develop strong CUB. Indeed, we detected strong shifts in preferential codon usage within some diatom genera, with switches between preferentially GC-rich and AT-rich 3rd codon positions (GC3). For example, GC3 ranges from 0.6 to 1 in most Chaetoceros species, while for Chaetoceros dichaeta GC3 = 0.1. Both variation in selection intensity and mutation spectrum may drive such shifts in codon usage and limit the observed CUB. Our study represents the first genome-wide analysis of CUB in diatoms and the first such analysis for a major phytoplankton group.Diatoms, Codon, Evolution, Molecular, Mutation, Selection, Genetic, Biological Evolution, Codon Usage -
One thousand plant transcriptomes and the phylogenomics of green plants.
October 2019|Journal article|NatureGreen plants (Viridiplantae) include around 450,000-500,000 species1,2 of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life.One Thousand Plant Transcriptomes Initiative, Evolution, Molecular, Phylogeny, Genome, Plant, Databases, Genetic, Biological Evolution, Viridiplantae, Transcriptome -
Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa.
September 2019|Journal article|Nature communicationsPhytoplankton account for nearly half of global primary productivity and strongly affect the global carbon cycle, yet little is known about the forces that drive the evolution of these keystone microscopic organisms. Here we combine morphometric data from the fossil record of the ubiquitous coccolithophore genus Gephyrocapsa with genomic analyses of extant species to assess the genetic processes underlying Pleistocene palaeontological patterns. We demonstrate that all modern diversity in Gephyrocapsa (including Emiliania huxleyi) originated in a rapid species radiation during the last 0.6 Ma, coincident with the latest of the three pulses of Gephyrocapsa diversification and extinction documented in the fossil record. Our evolutionary genetic analyses indicate that new species in this genus have formed in sympatry or parapatry, with occasional hybridisation between species. This sheds light on the mode of speciation during evolutionary radiation of marine phytoplankton and provides a model of how new plankton species form.Phytoplankton, Marine Biology, Evolution, Molecular, Phylogeny, Genome, Genetic Variation, Haptophyta -
Adaptive Evolution Is Common in Rapid Evolutionary Radiations.
September 2019|Journal article|Current biology : CBOne of the most long-standing and important mysteries in evolutionary biology is why biological diversity is so unevenly distributed across space and taxonomic lineages. Nowhere is this disparity more evident than in the multitude of rapid evolutionary radiations found on oceanic islands and mountain ranges across the globe [1-5]. The evolutionary processes driving these rapid diversification events remain unclear [6-8]. Recent genome-wide studies suggest that natural selection may be frequent during rapid evolutionary radiations, as inferred from work in cichlid fish [9], white-eye birds [10], new world lupins [11], and wild tomatoes [12]. However, whether frequent adaptive evolution is a general feature of rapid evolutionary radiations remains untested. Here we show that adaptive evolution is significantly more frequent in rapid evolutionary radiations compared to background levels in more slowly diversifying lineages. This result is consistent across a wide range of angiosperm lineages analyzed: 12 evolutionary radiations, which together comprise 1,377 described species, originating from some of the most biologically diverse systems on Earth. In addition, we find a significant negative correlation between population size and frequency of adaptive evolution in rapid evolutionary radiations. A possible explanation for this pattern is that more frequent adaptive evolution is at least partly driven by positive selection for advantageous mutations that compensate for the fixation of slightly deleterious mutations in smaller populations.Animals, Biodiversity, Population Density, Adaptation, Biological, Adaptation, Physiological, Evolution, Molecular, Phylogeny, Genetic Speciation, Selection, Genetic, Biological Evolution, Phylogeography, Islands, Magnoliopsida
E: | dmitry.filatov@plants.ox.ac.uk |
T: | +44 (0) 1865 275051 |