Authorea (Authorea), Год журнала: 2022, Номер unknown

Опубликована: Ноя. 7, 2022

Running title: Evolution of Arabian mangrovesGuillermo Friis*, Edward G. Smith, Catherine E. Lovelock, Alejandra Ortega, Alyssa Marshell, Carlos M. Duarte, John A. Burt*Corresponding author: Center for Genomics and Systems Biology, New York University — Abu Dhabi, PO Box 129188, United Arab Emirates; Email: [email protected]; Tel: +97126286739. Summary· Plant systems occurring in ecologically heterogeneous spatially discontinuous habitats provide an ideal opportunity to investigate the relative roles neutral selective factors driving lineage diversification. Here, we analyzed fully sequenced genomes study diversification mechanisms gray mangroves [Avicennia marina (Forssk.) Vierh.] Arabia, where they occur at edge species’ range are subject variable, often extreme, environmental conditions. · We conducted population structure, phylogenomic demographic analyses reconstruct evolutionary history species across Arabia. also applied genotype-environment association methods adaptive Our revealed marked genetic structure highly supported clades among within seas surrounding Peninsula. Inferred divergence times were consistent with recent periods low marine connectivity during glacial periods, revealing presence (cryptic) refugia Red Sea Persian/Arabian Gulf. Genetic‐environment high levels differentiation, detected signs multi-loci local adaptation driven by temperature extremes hypersalinity. These results support a process rapid resulting from combined effects historical ecological selection, reveal mangrove peripheral environments as relevant drivers diversity. IntroductionLineage plants involves both (Rieseberg & Willis, 2007), elucidating their is essential understand underlying early stages speciation (Coyne Orr, 2004). Evolutionary may result accumulation differences caused drift geographic isolation or isolation-by-distance (IBD, Wright, 1943; 1946), mode (Mayr, 1954; Mayr, 1963). In turn, variation conditions can divergent selection (Darwin, 1859; Coyne 2004), diversifying that drives (Nosil, 2012). models, reproductive barriers arise by-product cumulative, changes 1947; Schluter, 2000; Rundle Nosil, 2005) enabling genome‐wide differentiation selected loci (Nosil et al., 2008; Funk 2011; Shafer Wolf, 2013; Wang Bradburd, 2014). Ecological theoretically uncontroversial, considered key some most remarkable radiations angiosperms (Baldwin Sanderson, 1998; Hughes Eastwood, 2006). However, whether environment-driven processes commonly nature absence long-term reduced gene flow remains debated evolution research (Butlin Fitzpatrick Papadopulos Foote, 2018). The interactions between stochastic derived such founder events, bottlenecks remain unclear, difficult assess natural (Barton Charlesworth, 1984; Kliber Eckert, 2005; Crepet Niklas, 2009).Plant environmentally extreme edges suitable models questions related environment tends be stressful discontinuous, well temporally unstable (Lesica Allendorf, 1995), frequently dynamic settings multiple isolated populations strong differential selection. severe character hypothesized generate interplay (Hardie Hutchings, 2010), providing research. One system Peninsula (Avicennia var. marina). has broadest distribution any (Spalding 2010; Hogarth, 2015; Tomlinson, 2016), extending Indian Ocean into West Pacific far Japan Zealand (Fouda AI-Muharrami, 1996; Sheppard Spalding Khalil, 2015). Gray present several morphological physiological adaptations harsh intertidal habitat (Tomlinson, which makes them compelling model functional genes biological pathways involved stress tolerance (Urashi Xu 2017). represents one northernmost (Duke, 1991; characterized temperatures, aridity, salinity, known limiting growth (Ball, 1988; 1992; Lovelock 2016). domains diverse within, among, main water bodies bordering peninsula, define three biogeographic regions: (i) Sea, presents opposing gradients salinity temperature, highest lowest shallow southern basin, while deeper northern basin cooler temperatures but limited precipitation evaporation (Carvalho 2019; Anton 2020); (ii) Gulf (referred ‘PAG’ hereafter) northeast Peninsula, arid (<250 mm) hyper-arid (<100 rainfall regimes, experience widest air region throughout year (Böer, 1997; Whitford Duval, 2019); (iii) (here including Oman), contrast former regions, normal oceanic summer buffered cold-water upwelling monsoon, more moderate (Claereboudt, 2019).The experienced large fluctuations spatial glacio-eustatic cycles largely impacted biodiversity region, particular enclosed PAG (DiBattista 2016a). Throughout last 400,000 years remained connected Ocean, yet cross-sectional area along Strait Bab al Mandab connects these was, maxima, 2% today, major increases near-complete (Lambeck 2011). For sustained two cycles, minimum channel width connecting was less than 4 km wide narrow whenever sea 50 meters below current contrast, show nearly completely drained peak glaciation until c.a. 14,000 ago (Lambeck, 1996). A incursion started approximately 12,500 ago, towards over following millennia, day shorelines forming just 6,000 open ocean habitat, coast only vertical migration without isolation.The combination conditions, variable world, potential 2016b). Although phylogenetic relationships varieties congeneric have been reported other regions (Duke Nettel Li extensive coasts rarely included DNA sequence-based (see Duke Maguire 2016; Al-Qthanin Alharbi, 2020). specific molecular basis understudied Arabia its global distribution.Here, used complex examine how shaped diversity using whole genome georeferenced data. First, patterns reconstructed Two general competing hypotheses about tested this study: extirpated Pleistocene, followed recolonization after maximum (LGM); expanded once rose. Second, studied variability applying (GEA) analysis. redundancy analysis (RDA) combining single nucleotide polymorphisms (SNP) data survey jointly identify variables potentially divergence. Materials MethodsPopulation samplingWe sampled total 200 Avicennia individuals 19 sites (var. marina, N = 190), site Australia australasica, 10) (Table 1, Fig. 1; Table S1, Supporting Information). Leaf tissue collected trees separated least 20 meters, preserved silica beads up ten days before extraction. Geographic coordinates each tree recorded. Genomic extracted ground leaf DNeasy 96 plant kit (Qiagen, Valencia, CA) according manufacturer’s protocol. Genome resequencing variant calling Illumina paired-end 150 bp libraries insert size equal 350 prepared Novaseq platform. Reads mapped against previously published reference (Friis 2020), SNP carried out GATK Analysis Toolkit (GATK; McKenna 2010). dataset consisted 178 Information) 15,702,886 biallelic SNPs per-individual average coverage 16.8 missing rate 0.11. This further filtered customized downstream (See details Information).Population To explore genome-wide mangroves, first generated quality, independent putatively SNPs, consisting matrix 143,900 170 samples S2, principal components (PCA) implemented R package SNPRelate (Zheng, examined sparse non-negative factorization method (SNMF; Frichot ran program five per K value, ranging 2 20. Similarity scores runs graphics computed CLUMPAK (Kopelman al. IBD dataset. pairwise Nei’s distance values hierfstat (Goudet By-sea, distances measured based coordinates. Mantel test implemented, significance through 9,999 permutations.Phylogenetic analysisA likelihood phylogeny produced IQ-TREE (Nguyen analysis, same filters tests, retained Brisbane outgroup (SNP 29,433, 178; ascertainment bias correction generalized time-reversible substitution implemented.Population analysesWe performed comparisons under framework developed fastSIMCOAL2 v2.6 (Excoffier 2013) estimate parameters date cladogenetic events populations, colonization LGM versus around Informed results), sets independently plus Oman, entire Three representatives set models. again calibrate divergence, coalescence time lineages 2.7 million all (Li He Topologies scenarios ‘strict isolation’ ‘isolation migration’. Overall, six, twelve compared respectively S4, As input folded frequency spectra (SFS) easySFS (https://github.com/isaacovercast/easySFS). Details analyses, data, sketches parameter files provided Information.TreeMix v1.13 (Pickrell Pritchard, 2012) populations. corresponding built phylogeny, exemption linkage disequilibrium it controlled TreeMix command line 797,949; 178). 0–15 migrations, grouping blocks 50. Migration plotted 99.8% variance ancestry explained consistency evaluated running replicates added number different, randomly seed. Results seed yielded reported.Candidate identification analysisWe candidate evolving pressures, contribution approach (Van Den Wollenberg, 1977; Legendre Legendre, Borcard 2011) vegan (Oksanen explanatory variables, sampling averaged surface months MARSPEC database (Sbrocco Barber, 2013)]; isothermality warmest month WorldClim (Hijmans Fick Hijmans, 2017)]. response allele frequencies position 2,488,560 (N 170; Information).Two GEA implemented: simple RDA associations predictors; partial (pRDA), addition, effects. Covariates accounting PCs PCA on filtering positions Following procedure described Capblancq (2018), Mahalanobis estimated center space (Capblancq Forester, 2021), p-value threshold < 0.01 Bonferroni testing. individual level, complementary genotypes outliers variables. axes visual inspection, Euclidean ordination Further Information. ResultsPopulation analysesA structure. plot recovered pattern clustering matched Populations clustered apart, showing overlapping region. showed structure: west (Salalah Taqah) grouped together apart remaining clusters, Oman east (Shinas Qurm) close PAG. intermediate Filim occupied central PC2. third fourth regions. Northern basins PC3, lesser extent. differentiated PC4 (Fig. 2A).A SNMF results. At 2, groups separating 3 isolated, adjacent group, decreasing degrees shared ancestry. 4, (Bahrain Dammam) appeared cluster. 5, (Duba, Al Wajh 1 2) genetically cluster, signal coancestry latitude proximal (Al Kharrar King Abdullah Economic City, hereafter KAEC) extent, Lith. 6, Qurm Shinas, Filim, Shinas cluster Ras Khaimah (hereafter RAK), Umm Quawain UAQ), Ghurab Suweihat. 7, Lith, Farasan Banks 2; FB1 FB2) Lith presented KAEC 2B).A selectively neutral, significant correlation by-sea (r 0.765, 10-4; S3, Information).Phylogenetic reconstruction almost resolved monophyletic node support. major, reciprocally lineages: (Major Clade I), II) III). Within Sea’s Major I, sequence split those south FB2); little clade. II encompassed Salalah, Taqah sister group III, includes III divided (RAK, UAQ, Suweihat) (Qurm Shinas). latter subregions, side Hormuz, monophyletic, 3).Population mangroveDemographic fastSIMCOAL2. greatest score (ΔAIC 318, 4; event scenario, splitting dating back 99,200 (95% CI [40,062 – 295,152]), rapid, simultaneous differentiation. Gene exchange particularly entrance (MIG → FB2 60, 95% [13 109] migrants generation). bands, confidence intervals varied orders magnitude near zero, impact SFS S5, case best fitted our 1,615, scenario cladogenesis 37,760 [18,950-161,565]), prior maximum. Signs lineages. While narrower estimates, ranges zero cases, reducing certainty corresponded 1,067, Information), 70,180 [14,074-161,976]) 153,140 [90,714-416,863]) IQ-TREE. variance, contemporary bands ancestral seemed unlikely, so should interpreted caution 5).Candidate mangrovesEnvironmental predictors 33.2% (Adjusted R2 0.332, 0.01). distinct high, negative loading axis (RD) correlated positively axis, heavily basin. RD2, positive much lower values. pRDA, 6.4%of controlling 0.064, Scores scattered pRD1, Central limited, pRD2, Qurm, correlation, Suweihat, negatively S6, Information).The (2018). accounted unadjusted proportion 38.8% (R2 0.388) 48.0% full model. four 32.3% 0.323). RDA, respectively, thereby identification. 446 variants pRDA (NRDA 3,015; NpRDA 73,671; Njoint 446; Of outliers, 70 located 31 functionally annotated genes. Reported functions identified flowering marginal include following: chronic heat (MGE2; Hu 2012); drought resistance stomatal aperture density regulation, root development (ABIL2; 2015); hydrotropism tolerance; transport osmotic pressure control salt (PIP; Katsuhara Hanba, Mahdieh Rodríguez-Gamir 2011); cell wall biosynthesis (BXL2; Goujon 2003; Zhao 2010); organ adjustments (MOB1A; Pinosa 2013); Nitrogen uptake coordination biotic (WRK50; Cheng 2021); (SQS2; Shirazi regulation reactive oxygen sterol (SQE2; Posé 2009); terpenoid metabolism (4CLL7; Madritsch Zhang 2022); flower bud light (AI5L5; Yi 2021; Liu sensitivity ABA signaling pathway (PUM23; Huang 2018) S7, Information).To visually structured alone. distinctive partially region: gradient values, origin coordinates, correlations. southwest (Taqah Salalah) strong, isothermality, gradient. opposite differentiating salinity/isothermality gradient, weaker 6A). Individual similar trends 6B), within-region, outrunning 6B). DiscussionMarked IBD/geographic isolatio

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