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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) sex chromosome evolution and (ii) the speciation and adaptation processes in plants. 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: 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.
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.
Publications (while at this department)
Nevado B, Atchison GW, Hughes CE, Filatov DA (2016) Widespread adaptive evolution during repeated evolutionary radiations in New World lupins. Nature Communications 7:12384.
Sobczyk MK, Smith JAC, Pollard AJ, Filatov DA (2016) Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex. Heredity, in press.
Gan X, Hay A, Kwantes M, Haberer G, Hallab A, Ioio RD, Hofhuis H, Pieper B, Cartolano M, Neumann U, Nikolov LA, Song B, Hajheidari M, Briskine R, Kougioumoutzi E, Vlad D, Broholm S, Hein J, Meksem K, Lightfoot D, Shimizu KK, Shimizu-Inatsugi R, Imprialou M, Kudrna D, Wing R, Sato S, Huijser P, Filatov DA, Mayer KF, Mott R, Tsiantis M. (2016) The Cardamine hirsuta genome offers insight into the evolution of morphological diversity. Nature Plants. 2(11):16167.
Vuolo F, Mentink RA, Hajheidari M, Bailey CD, Filatov DA, Tsiantis M. (2016) Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity. Genes and Development 30(21):2370-2375.
Atchison G.W., Nevado B., Eastwood RJ, Contreras-Ortiz N, Reynel C; Madriñán S, Filatov DA, Hughes CE (2016) Lost crops of the Incas: origins of domestication of the Andean pulse crop 'tarwi', Lupinus mutabilis. American Journal of Botany, 103(9):1592-1606.
Kazama Y, Ishii K, Aonuma W, Ikeda T, Kawamoto H, Koizumi A, Filatov DA, Chibalina M, Bergero R, Charlesworth D, Abe T, Kawano S. (2016) A new physical mapping approach refines the sex-determining gene positions on the Silene latifolia Y-chromosome. Scientific Reports 6:18917.
Filatov DA, Osborne OG, Papadopoulos AST (2016) Demographic history of ecological speciation in Senecio altitudinal hybrid zone on Mt. Etna. Molecular Ecology 25 (11): 2467-2481.
Osborne OG, Chapman M, Nevado B, Filatov DA (2016) Maintenance of species boundaries despite ongoing gene flow in ragworts. Genome Biology and Evolution 8 (4):1038-1047.
Flegontov P, Butenko A, Firsov S, Kraeva N, Eliáš M, Field MC, Filatov D, Flegontova O, Gerasimov ES, Hlaváčová J, Ishemgulova A, Jackson AP, Kelly S, Kostygov AY, Logacheva MD, Maslov DA, Opperdoes FR, O'Reilly A, Sádlová J, Ševčíková T, Venkatesh D, Vlček Č, Volf P, Votýpka J, Záhonová K, Yurchenko V, Lukeš J (2016) Genome of Leptomonas pyrrhocoris: a high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania. Scientific Reports 6:23704.
Hu XS, Filatov DA. (2016) The large-X effect in plants: Increased species divergence and reduced gene flow on the Silene X-chromosome. Molecular Ecology 25 (11): 2609-2619.
Papadopulos AS, Chester M, Ridout K, Filatov DA. (2015) Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proc Natl Acad Sci USA 112 (42):13021-13026.
Chapman MA, Hiscock SJ, Filatov DA (2016) The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae). Journal of Evolutionary Biology 29 (1): 98-113.
Filatov DA (2015) Homomorphic plant sex chromosomes are coming of age. Molecular Ecology 24 (13): 3217-3219.
Whittle CA, Votintseva A, Ridout K, Filatov DA (2015) Recent and massive expansion of the mating-type-specific region in the smut fungus Microbotryum. Genetics 199 (3): pp 809-816.
Hay AS, Pieper B, Cooke E, Mandakova T, Cartolano M, Tattersall AD, Ioio RD, McGowan SJ, Barkoulas M, Galinha C, Rast MI, Hofhuis H, Then C, Plieske J, Ganal M, Mott R, Martinez-Garcia JF, Carine MA, Scotland RW, Gan X, Filatov DA, Lysak MA, Tsiantis M. (2014) Cardamine hirsuta: A versatile genetic system for comparative studies. Plant Journal 78 (1): 1-15.
Chapman MA, Hiscock SJ, Filatov DA (2013) Genomic divergence during speciation driven by adaptation to altitude. Molecular Biology and Evolution 30 (12): 2553-2567.
Kapralov MV, Votintseva AA, Filatov DA (2013) Molecular adaptation during a rapid adaptive radiation. Molecular Biology and Evolution 30 (5): 1051-1059.
Muir G, Osborne OG, Sarasa J, Hiscock SJ, Filatov DA (2013) Recent ecological selection on regulatory divergence is shaping clinal variation in Senecio on mount Etna. Evolution 67(10):3032-3042.
Osborne OG, Batstone TE, Hiscock SJ, Filatov DA. (2013) Rapid speciation with gene flow following the formation of Mt. Etna. Genome Biology and Evolution 5 (9): 1704-1715.
Filatov DA (2012) How much do we know about evolution of sex chromosomes in plants? New Insights on Plant Sex Chromosomes. Nova Science Publishers, Inc. ISBN: 9781614702368. pp 35-50
Kapralov MV, Smith JAC, Filatov DA (2012) Rubisco evolution in C4 Eudicots: An analysis of Amaranthaceae sensu lato. PLoS ONE. 7 (12): e52974.
Muir G, Dixon, CJ, Harper, AL, Filatov DA (2012) Dynamics of drift, gene flow, and selection during speciation in Silene. Evolution. 66(5): 1447-1458.
Young JN, Rickaby REM, Kapralov MV, Filatov DA. (2012) Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide. Philosophical Transactions of the Royal Society B: Biological Sciences. 367 (1588): 483-492.
Chibalina MV, Filatov DA (2011) Plant Y chromosome degeneration is retarded by haploid purifying selection. Current Biology 21 (17): 1475-1479.
Dixon CJ, Kapralov MV, Filatov DA (2011) Gene flow and species cohesion following the spread of Schiedea globosa (Caryophyllaceae) across the Hawaiian Islands. Journal of Evolutionary Biology 24 (1): 1-11.
Howell EC, Armstrong SJ, Filatov DA (2011) Dynamic gene order on the Silene latifolia Y chromosome. Chromosoma 120(3): 287-296.
Kapralov MV, Kubien DS, Andersson I, Filatov DA (2011) Changes in Rubisco kinetics during the evolution of C4 Photosynthesis in Flaveria (Asteraceae) are associated with positive selection on genes encoding the enzyme. Molecular Biology and Evolution. 28 (4): 1491-1503.
Muir G, Bergero R, Charlesworth D, Filatov DA (2011) Does local adaptation cause high population differentiation of Silene latifolia Y chromosomes? Evolution 65(12): 3368-3380.
Votintseva AA, Filatov DA (2011) DNA polymorphism in recombining and non-recombing mating-type-specific loci of the smut fungus Microbotryum. Heredity. 106 (6): 936-944.
Gossmann TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A (2010) Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Molecular Biology and Evolution. 27 (8): 1822-1832.
Piazza P, Bailey CD, Cartolano M, Krieger J, Cao J, Ossowski S, Schneeberger K, He F, De, Meaux J, Hall N, MacLeod N, Filatov D, Hay A, Tsiantis M. (2010) Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep. Current Biology 20 (24): 2223-2228.
Ridout KE, Dixon CJ, Filatov DA (2010) Positive selection differs between protein secondary structure elements in Drosophila. Genome Biology and Evolution 2 (1): 166-179.
Bernasconi, G, Antonovics, J, Biere, A, Charlesworth, D, Delph, L.F, Filatov D, Giraud, T, Hood, M.E, Marais, G.A.B, McCauley, D, Pannell, J.R, Shykoff, J.A, Vyskot, B, Wolfe, L.M, Widmer, A. (2009) Silene as a model system in ecology and evolution. Heredity 103 (1): 5-14.
Filatov DA (2009) Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics 25 (23): 3189-3190.
Filatov DA, Howell EC, Groutides C, Armstrong SJ (2009) Recent spread of a retrotransposon in the Silene latifolia genome, apart from the Y chromosome. Genetics. 181 (2): 811-817.
Floyd N, Oldham NJ, Eyles CJ, Taylor S, Filatov DA, Brouard M, Davis B.G. (2009) Photoinduced, family-specific, site-selective cleavage of TIM-barrel proteins. Journal of the American Chemical Society. 131 (35): 12518-12519.
Howell, EC, Armstrong, SJ, Filatov DA (2009) Evolution of neo-sex chromosomes in Silene diclinis. Genetics. 182 (4): 1109-1115.
Kapralov MV, Stift M, Filatov DA (2009) Evolution of genome size in Hawaiian endemic genus Schiedea (Caryophyllaceae). Tropical Plant Biology 2 (2): 77-83.
Votintseva AA, Filatov DA (2009) Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics. 182 (4): 1391-1396.
Armstrong SJ, Filatov DA. (2008) A cytogenetic view of sex chromosome evolution in plants. Cytogenetic and Genome Research 120: 241-246.
Filatov DA (2008) A selective sweep in or near the Silence latifolia X-linked gene SlssX. Genetics Research. 90 (1): 85-95.
Muir G, Filatov DA (2007) A selective sweep in the chloroplast DNA of dioecious Silene (Section Elisanthe). Genetics. 177 (2): pp 1239-1239.