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How Predictable Is Genome Evolution?

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How Predictable Is Genome Evolution? INSIGHT SPECIATION How predictable is genome evolution? Similar patterns of genomic divergence have been observed in the evolution of plant species separated by oceans. MATTHEW J COATHUP, OWEN G OSBORNE AND VINCENT SAVOLAINEN researchers from the United States, China and Related research article Dong Y, Chen S, Canada – including Yibo Dong (North Carolina Cheng S, Zhou W, Ma Q, Chen Z, Fu CX, State University) and Shichao Chen (University of Liu X, Zhao YP, Soltis PS, Wong GKS, Soltis Florida and Tongji University) as joint first DE, Xiang J. 2019. Natural selection and authors – report how pairs of closely related repeated patterns of molecular evolution flowering plants which live thousands of miles following allopatric divergence. eLife 8: apart genetically diverged during evolution e45199. DOI: 10.7554/eLife.45199 (Dong et al., 2019). Dong et al. systematically collected and sequenced 20 pairs of closely related species, including 16 pairs that diverged between 2 and 10 million years ago as a result of the Eastern nderstanding the formation of new spe- Asian–Eastern North American floristic disjunc- cies – a process called speciation – is a tion (Figure 1). These pairs of species are the U central challenge in evolutionary biol- ideal system in which to study allopatric specia- ogy and genomics, but many questions remain tion (that is, speciation in geographically isolated (Arnegard et al., 2014; Riesch et al., 2017). In populations). particular, are there certain patterns of genome Dong et al. examined divergence in thou- evolution that are repeated? And, if there are, sands of genes by measuring the rate at which can we predict how genomes will change as new nucleotide substitutions resulted in a change in species emerge and diverge? the amino acid coded for (Ka), and the rate of To date, most studies have focused on the nucleotide substitutions that did not result in genomes of pairs of closely related species living such a change (Ks). The ratio Ka/Ks is a common in close proximity (such as two species of white- index for identifying the selective pressure on a fish living in the same set of lakes; gene: values significantly above one indicate Gagnaire et al., 2013), or on the genomes of positive selection (i.e. an increase in the fre- different lineages within a single species (such as quency of beneficial mutations), and values sig- one species of stick insect living on two different nificantly below one indicate purifying selection host plants; Soria-Carrasco et al., 2014), and (i.e. the removal of deleterious mutations). have predominantly investigated scenarios Despite investigating a diverse range of taxa, Copyright Coathup et al. This where there is some degree of gene flow Dong et al. found that all species pairs experi- article is distributed under the terms between the different species or lineages enced similar patterns of genomic divergence of the Creative Commons Attribution (Wolf and Ellegren, 2017). However, it is and selection, regardless of their ecologies and License, which permits unrestricted thought that most new species emerge in geo- use and redistribution provided that morphologies. the original author and source are graphically isolated populations and in the In fact, most of the genes measured showed credited. absence of gene flow. Now, in eLife, a team of little divergence and, intriguingly, the peak Coathup et al. eLife 2019;8:e50784. DOI: https://doi.org/10.7554/eLife.50784 1 of 3 Insight Speciation How predictable is genome evolution? Figure 1. Geographical distribution of closely related plant species. Map showing floristic disjunctions – geographically separated regions than contain closely related plant species: 1) the Eastern Asian–Eastern North American floristic disjunction (blue; Dong et al., 2019); 2) the American Amphitropical floristic disjunction (pink; Raven, 1963); 3) the Madrean–Tethyan floristic disjunction (black; Wen and Ickert-Bond, 2009); 4) the Australia– South America floristic disjunction (green; van den Ende et al., 2017); 5) the Northern–Southern Africa floristic disjunction (yellow; Ju¨rgens, 1997); 6) the disjunction between Linospadix minor in North-East Queensland and L. albertisianus in New Guinea (brown; Osborne et al., 2019). Image credit: Matthew Coathup. frequencies of Ks, Ka and Ka/Ks for each pair speciation. Many other disjunctions exist around clustered within narrow ranges of small values. the world (Figure 1), and similar analyses of This is indicative of a common pattern in the rel- these would determine whether the findings of ative numbers of genes at different levels of Dong et al. represent a common rule of genomic divergence during allopatric speciation, with divergence. Indeed, recent work by some of the only a small number of loci in the genome dis- present authors and colleagues has shown that playing high levels of divergence. Furthermore, two pairs of palm species – one widely sepa- by categorising the Ka/Ks ratios into six groups, rated, the other not – have values of Ka, Ks and Dong et al. found that in all pairs of species the Ka/Ks similar to those reported by Dong et al. relative number of genes under different selec- (Osborne et al., 2019). This supports the idea tion pressures followed the same order. Moder- that these patterns may be common to genomic ate purifying selection was most common, divergence in general, regardless of geography. followed by strong purifying selection, relaxed purifying selection, weak/moderate positive Matthew J Coathup is in the Department of Life selection, putatively neutral selection and, Sciences, Silwood Park Campus, Imperial College finally, strong positive selection. Overall the pat- London, London, United Kingdom terns observed by Dong et al. suggest that it https://orcid.org/0000-0002-4152-3049 might be possible to make predictions about Owen G Osborne is in the School of Natural Sciences, genome evolution. Bangor University, Bangor, United Kingdom While the study focused on the Eastern https://orcid.org/0000-0002-1213-1169 Asian–Eastern North American floristic disjunc- Vincent Savolainen is in the Department of Life tion, it is likely that these patterns of genome Sciences, Silwood Park Campus, Imperial College evolution are a common feature of allopatric London, London, United Kingdom Coathup et al. eLife 2019;8:e50784. DOI: https://doi.org/10.7554/eLife.50784 2 of 3 Insight Speciation How predictable is genome evolution? [email protected] Raven PH. 1963. Amphitropical relationships in the https://orcid.org/0000-0001-5350-9984 floras of North and South America. The Quarterly Review of Biology 38:151–177. DOI: https://doi.org/ Competing interests: The authors declare that no 10.1086/403797 competing interests exist. Riesch R, Muschick M, Lindtke D, Villoutreix R, Published 13 September 2019 Comeault AA, Farkas TE, Lucek K, Hellen E, Soria- Carrasco V, Dennis SR, de Carvalho CF, Safran RJ, References Sandoval CP, Feder J, Gries R, Crespi BJ, Gries G, Arnegard ME, McGee MD, Matthews B, Marchinko Gompert Z, Nosil P. 2017. Transitions between phases KB, Conte GL, Kabir S, Bedford N, Bergek S, Chan YF, of genomic differentiation during stick-insect Jones FC, Kingsley DM, Peichel CL, Schluter D. 2014. speciation. Nature Ecology & Evolution 1:0082. Genetics of ecological divergence during speciation. DOI: https://doi.org/10.1038/s41559-017-0082 Nature 511:307–311. DOI: https://doi.org/10.1038/ Soria-Carrasco V, Gompert Z, Comeault AA, Farkas nature13301, PMID: 24909991 TE, Parchman TL, Johnston JS, Buerkle CA, Feder JL, Dong Y, Chen S, Cheng S, Zhou W, Ma Q, Chen Z, Fu Bast J, Schwander T, Egan SP, Crespi BJ, Nosil P. CX, Liu X, Zhao YP, Soltis PS, Wong GKS, Soltis DE, 2014. Stick insect genomes reveal natural selection’s Xiang J. 2019. Natural selection and repeated patterns role in parallel speciation. Science 344:738–742. of molecular evolution following allopatric divergence. DOI: https://doi.org/10.1126/science.1252136, eLife 8:e45199. DOI: https://doi.org/10.7554/eLife. PMID: 24833390 45199, PMID: 31373555 van den Ende C, White LT, van Welzen PC. 2017. The Gagnaire PA, Pavey SA, Normandeau E, Bernatchez L. existence and break-up of the Antarctic land bridge as 2013. The genetic architecture of reproductive indicated by both amphi-Pacific distributions and isolation during speciation-with-gene-flow in lake tectonics. Gondwana Research 44:219–227. whitefish species pairs assessed by RAD sequencing. DOI: https://doi.org/10.1016/j.gr.2016.12.006 Evolution 67:2483–2497. DOI: https://doi.org/10.1111/ Wen J, Ickert-Bond SM. 2009. Evolution of the evo.12075, PMID: 24033162 Madrean-Tethyan disjunctions and the North and Ju¨ rgens N. 1997. Floristic biodiversity and history of South American amphitropical disjunctions in plants. African arid regions. Biodiversity and Conservation 6: Journal of Systematics and Evolution 47:331–348. 495–514. DOI: https://doi.org/10.1023/a: DOI: https://doi.org/10.1111/j.1759-6831.2009.00054. 1018325026863 x Osborne OG, Ciezarek A, Wilson T, Crayn D, Hutton I, Wolf JB, Ellegren H. 2017. Making sense of genomic Baker WJ, Turnbull CGN, Savolainen V. 2019. islands of differentiation in light of speciation. Nature Speciation in Howea palms occurred in sympatry, was Reviews Genetics 18:87–100. DOI: https://doi.org/10. preceded by ancestral admixture, and was associated 1038/nrg.2016.133, PMID: 27840429 with edaphic and phenological adaptation. Molecular Biology and Evolution:msz166. DOI: https://doi.org/ 10.1093/molbev/msz166, PMID: 31318434 Coathup et al. eLife 2019;8:e50784. DOI: https://doi.org/10.7554/eLife.50784 3 of 3.
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