Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex

Ma, Tao; Wang, Kun; Hu, Quanjun; Xi, Zhenxiang; Wan, Dongshi; Wang, Qian; Feng, Jiexiong; Jiang, Dechun; Ahani, Hamid; Abbott, Richard J.; Lascoux, Martin; Nevo, Eviatar; Liu, Jianquan

doi:10.1073/pnas.1713288114

Cited by 100 publications

(169 citation statements)

References 62 publications

(104 reference statements)

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“…Such selection could accelerate lineage sorting and will hence inevitably result in increased genetic differentiation between species in these regions (Burri, 2017). Furthermore, the long‐term action of linked selection in ancestral as opposed to extant lineages can also affect the amount and distribution of ancestral polymorphisms (Ma et al, 2018; Munch, Nam, Schierup, & Mailund, 2016; Scally et al, 2012), which can further result in heterogeneous patterns of genealogical relationships among closely related species (Mailund, Munch, & Schierup, 2014; Pease & Hahn, 2013). Despite widespread interest in speciation genomics, there remains little consensus as to how various evolutionary processes have shaped the genomic landscape during the speciation process that eventually gives rise to new species (Ravinet et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

Wang

Street

Park³

et al. 2020

Molecular Ecology

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Increasing our understanding of how evolutionary processes drive the genomic landscape of variation is fundamental to a better understanding of the genomic consequences of speciation. However, genome‐wide patterns of within‐ and between‐ species variation have not been fully investigated in most forest tree species despite their global ecological and economic importance. Here, we use whole‐genome resequencing data from four Populus species spanning the speciation continuum to reconstruct their demographic histories and investigate patterns of diversity and divergence within and between species. Using Populus trichocarpa as an outgroup species, we further infer the genealogical relationships and estimate the extent of ancient introgression among the three aspen species (Populus tremula, Populus davidiana and Populus tremuloides) throughout the genome. Our results show substantial variation in these patterns along the genomes with this variation being strongly predicted by local recombination rates and the density of functional elements. This implies that the interaction between recurrent selection and intrinsic genomic features has dramatically sculpted the genomic landscape over long periods of time. In addition, our findings provide evidence that, apart from background selection, recent positive selection and long‐term balancing selection have also been crucial components in shaping patterns of genome‐wide variation during the speciation process.

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Section: Introductionmentioning

confidence: 99%

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

Wang

Street

Park³

et al. 2020

Molecular Ecology

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“…(3) linked selection, background selection, selection at non-targeted loci and selection from standing variation (Schluter and Conte, 2009;Charlesworth, 2012;Cutter and Payseur, 2013;Burri et al, 2015;Christe et al, 2017); (4) demographic and evolutionary histories, including ancient introgression and introgression from other sister species (Fraïsse et al, 2014Nadeau et al, 2016;Ma et al, 2018); (5) gene density (Nordborg et al, 2005;Yeaman, 2013); or (6) the genetic architecture of adaptive and/or barrier loci (Le Corre and Flaxman et al, 2014;Conte et al, 2015;Yeaman, 2015). GEA models have evolved with the aim to reduce false-positives from diverse sources of confounding, such as patterns of isolation-by-distance (IBD), alignment of environmental and genetic gradients, or cryptic relatedness (Frichot et al, 2013;Rellstab et al, 2015;de Villemereuil et al, 2015) and they probably outperform GS models in identifying environmentally-driven local adaptation (De Mita et al, 2013;Payseur and Rieseberg, 2016).…”

Section: Introductionmentioning

confidence: 99%

Adaptive Introgression Promotes Fast Adaptation In Oaks Marginal Populations

Goicoechea

Guillardín

Fernández‐Ibarrondo

et al. 2019

Preprint

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Range shifts and species range limits are two fundamental, related processes in population and evolutionary genetics that have received much attention since a large impact of climate change in species' distributions was predicted. In general, there is a broad consensus on the effects of abiotic interactions on range limits, but comprehensive evidence supporting/rejecting the impact of biotic interactions is lacking. Hybridization has long been recognized as a biotic interaction favoring marginal populations establishment and range expansion through transgressive segregation or adaptive introgression, but recently new roles have been claimed for hybridization, such as the trigger of adaptive radiations, or indirect effects on population sizes that would allow persistence until new mutations arises or the environment changes. In this work, we selected two Mediterranean oak species with ecological discrimination based on soil pH, and intensively sampled three interspecific pairs of marginal populations from taxon-extreme environments under heterogeneous climate conditions. We genotyped 110 EST-SSR markers evenly distributed across their genomes and applied a variety of population and landscape genetics models to validate candidate genes for local adaptation. Then, several introgression screens on shared candidates showed that the three inter-specific population pairs contain evidences of adaptive introgression and that events occur in both directions. Other significant findings from our work are: (i) Aproximate Bayesian Computation coupled to coalescent simulations supports small hybridization rates since recent secondary contact in two population pairs affected by Quaternary climatic oscillations but continuous old interspecific gene flow in the pair less affected by climate, (ii) introgression at loci involved in local adaptations leads to strong geographic structure of marginal oak populations when sampling is large enough, and (iii) sampling efforts can be targeted to reveal different components of populations structure. Finally, we review evidences that support our conclusions and discuss some evolutionary implications of adaptive introgression on range expansion. Latitude Cross validation score Populations Populations K = 4 K = 5 d e f CAB CJA SN E FRO Q.faginea Q.pyrenaica

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“…These non-introgressable segments are often referred to as "genomic islands" which are, in theory, the most divergent portion of the genome 1,9,[12][13][14][15][16][17][18] . Based on this conjecture, genomic islands have been identified either by the relative level of divergence or by the absolute divergence 12,13,15,[17][18][19][20][21][22][23] . The former procedure has been questioned 24 and the absolute divergence has also been cast in doubt 25 .…”

Section: Introductionmentioning

confidence: 99%

In the absence of reproductive isolation – Extensive gene flow after speciation

Wang¹,

Z²,

He³

et al. 2019

Preprint

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In the biological species concept, much of the genomes cannot be exchanged between species 1,2 . In the modern genic view, species are distinct as long as genes that delineate the morphological, ecological and reproductive differences remain distinct 2 . The rest (or the bulk) of the genomes should be freely interchangeable. The core of the species concept therefore demands finding out the full potential of introgressions between species. In a survey of two closely related mangrove species (Rhizophora mucronata and R. stylosa) on the coasts of the western Pacific and Indian oceans, we found that the genomes are well delineated in allopatry, echoing their morphological and ecological divergence. The two species are sympatric/parapatric in the Daintree River area of northeastern Australia. In sympatry, their genomes harbor 7,700 and 3,100 introgression blocks, respectively, with each block averaging about 3-4 Kb. These fine-grained and strongly-penetrant introgressions suggest that each species must have evolved many differentially-adaptive (and, hence, non-introgressable) genes that contribute to speciation. We identify 30 such genes, seven of which are about flower development, within small genomic islets with a mean size of 1.4 Kb. In sympatry, the species-specific genomic islets account for only a small fraction (< 15%) of the genomes while the rest appears interchangeable.

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Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex

Cited by 100 publications

References 62 publications

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

Adaptive Introgression Promotes Fast Adaptation In Oaks Marginal Populations

In the absence of reproductive isolation – Extensive gene flow after speciation

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