Disparate genetic divergence patterns in three corals across a pan-Pacific environmental gradient highlight species-specific adaptation.
Journal
npj biodiversity
ISSN: 2731-4243
Titre abrégé: NPJ Biodivers
Pays: England
ID NLM: 9918804277406676
Informations de publication
Date de publication:
07 Jul 2023
07 Jul 2023
Historique:
received:
22
02
2023
accepted:
13
06
2023
medline:
7
7
2023
pubmed:
7
7
2023
entrez:
6
9
2024
Statut:
epublish
Résumé
Tropical coral reefs are among the most affected ecosystems by climate change and face increasing loss in the coming decades. Effective conservation strategies that maximize ecosystem resilience must be informed by the accurate characterization of extant genetic diversity and population structure together with an understanding of the adaptive potential of keystone species. Here we analyzed samples from the Tara Pacific Expedition (2016-2018) that completed an 18,000 km longitudinal transect of the Pacific Ocean sampling three widespread corals-Pocillopora meandrina, Porites lobata, and Millepora cf. platyphylla-across 33 sites from 11 islands. Using deep metagenomic sequencing of 269 colonies in conjunction with morphological analyses and climate variability data, we can show that despite a targeted sampling the transect encompasses multiple cryptic species. These species exhibit disparate biogeographic patterns and, most importantly, distinct evolutionary patterns in identical environmental regimes. Our findings demonstrate on a basin scale that evolutionary trajectories are species-specific and can only in part be predicted from the environment. This highlights that conservation strategies must integrate multi-species investigations to discern the distinct genomic footprints shaped by selection as well as the genetic potential for adaptive change.
Identifiants
pubmed: 39242808
doi: 10.1038/s44185-023-00020-8
pii: 10.1038/s44185-023-00020-8
doi:
Types de publication
Journal Article
Langues
eng
Pagination
15Subventions
Organisme : University of Konstanz
ID : AFF funding
Organisme : Agence Nationale de la Recherche
ID : "France Génomique" ANR-10-INBS-09
Organisme : Agence Nationale de la Recherche
ID : "Coralgene"ANR-17-CE02-0020
Organisme : Agence Nationale de la Recherche
ID : "Coralgene"ANR-17-CE02-0020
Organisme : Agence Nationale de la Recherche
ID : "Coralgene"ANR-17-CE02-0020
Organisme : JST Spring
ID : JPMJSP2124
Organisme : Labex Signalife
ID : ANR-11-LABX-0028
Organisme : Labex Signalife
ID : ANR-11-LABX-0028
Organisme : Labex Signalife
ID : ANR-11-LABX-0028
Organisme : IDEX UCAJedi
ID : ANR-15-IDEX-0001
Organisme : IDEX UCAJedi
ID : ANR-15-IDEX-0001
Organisme : IDEX UCAJedi
ID : ANR-15-IDEX-0001
Organisme : H2020 Marie Skłodowska-Curie Actions
ID : MC-CIG-618480
Informations de copyright
© 2023. The Author(s).
Références
Fisher, R. et al. Species richness on coral reefs and the pursuit of convergent global estimates. Curr. Biol. 25, 500–505 (2015).
pubmed: 25639239
doi: 10.1016/j.cub.2014.12.022
Smith, S. V. Coral-reef area and the contributions of reefs to processes and resources of the world’s oceans. Nature 273, 225–226 (1978).
doi: 10.1038/273225a0
Gattuso, J.-P. et al. OCEANOGRAPHY. Contrasting futures for ocean and society from different anthropogenic CO
pubmed: 26138982
doi: 10.1126/science.aac4722
Eddy, T. D. et al. Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4, 1278–1285 (2021).
doi: 10.1016/j.oneear.2021.08.016
Kleypas, J. et al. Designing a blueprint for coral reef survival. Biol. Conserv. 257, 109107 (2021).
doi: 10.1016/j.biocon.2021.109107
Voolstra, C. R., Peixoto, R. S. & Ferrier-Pagès, C. Mitigating the ecological collapse of coral reef ecosystems. EMBO Rep. 24, e56826 (2023).
pubmed: 36862379
pmcid: 10074092
doi: 10.15252/embr.202356826
Wilkinson, C. Status of Coral Reefs of the World: 2008 (Australian Institue of Marine Science, 2008).
Mcleod, E. et al. The future of resilience-based management in coral reef ecosystems. J. Environ. Manage. 233, 291–301 (2019).
pubmed: 30583103
doi: 10.1016/j.jenvman.2018.11.034
Voolstra, C. R. et al. Extending the natural adaptive capacity of coral holobionts. Nat. Rev. Earth Environ. 2, 747–762 (2021).
doi: 10.1038/s43017-021-00214-3
Peixoto, R. S., & Voolstra, C. R. (2023). The baseline is already shifted: marine microbiome restoration and rehabilitation as essential tools to mitigate ecosystem decline. Frontiers in Marine Science, 10. https://doi.org/10.3389/fmars.2023.1218531 .
Beger, M. et al. Evolving coral reef conservation with genetic information. Bull. Mar. Sci. 90, 159–185 (2014).
doi: 10.5343/bms.2012.1106
Almany, G. R. et al. Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28, 339–351 (2009).
doi: 10.1007/s00338-009-0484-x
Fontoura, L. et al. Protecting connectivity promotes successful biodiversity and fisheries conservation. Science 375, 336–340 (2022).
pubmed: 35050678
doi: 10.1126/science.abg4351
Pante, E. et al. Species are hypotheses: avoid connectivity assessments based on pillars of sand. Mol. Ecol. 24, 525–544 (2015).
pubmed: 25529046
doi: 10.1111/mec.13048
Selkoe, K. A. et al. The DNA of coral reef biodiversity: predicting and protecting genetic diversity of reef assemblages. Proc. Biol. Sci. 283, 20160354 (2016).
Buitrago-López, C. et al. Disparate population and holobiont structure of pocilloporid corals across the Red Sea gradient demonstrate species-specific evolutionary trajectories. Mol. Ecol. 32, 2151–2173 (2023).
pubmed: 36869609
doi: 10.1111/mec.16871
Flot, J.-F., Couloux, A. & Tillier, S. Haplowebs as a graphical tool for delimiting species: a revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evol. Biol. 10, 372 (2010).
pubmed: 21118572
pmcid: 3022603
doi: 10.1186/1471-2148-10-372
Richards, Z. T., Berry, O. & van Oppen, M. J. H. Cryptic genetic divergence within threatened species of Acropora coral from the Indian and Pacific Oceans. Conserv. Genet. 17, 577–591 (2016).
doi: 10.1007/s10592-015-0807-0
Pinzón, J. H. et al. Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia). J. Biogeogr. 40, 1595–1608 (2013).
doi: 10.1111/jbi.12110
Pante, E. et al. Use of RAD sequencing for delimiting species. Heredity 114, 450–459 (2015).
pubmed: 25407078
doi: 10.1038/hdy.2014.105
Erickson, K. L., Pentico, A., Quattrini, A. M. & McFadden, C. S. New approaches to species delimitation and population structure of anthozoans: two case studies of octocorals using ultraconserved elements and exons. Mol. Ecol. Resour. 21, 78–92 (2021).
pubmed: 32786110
doi: 10.1111/1755-0998.13241
Cowman, P. F. et al. An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives. Mol. Phylogenet. Evol. 153, 106944 (2020).
pubmed: 32860973
doi: 10.1016/j.ympev.2020.106944
Grinblat, M. et al. Biogeography, reproductive biology and phylogenetic divergence within the Fungiidae (mushroom corals). Mol. Phylogenet. Evol. 164, 107265 (2021).
pubmed: 34274488
doi: 10.1016/j.ympev.2021.107265
Ramírez-Portilla, C. et al. Solving the coral species delimitation conundrum. Syst. Biol. 71, 461–475 (2022).
pubmed: 34542634
doi: 10.1093/sysbio/syab077
Carstens, B. C., Pelletier, T. A., Reid, N. M. & Satler, J. D. How to fail at species delimitation. Mol. Ecol. 22, 4369–4383 (2013).
pubmed: 23855767
doi: 10.1111/mec.12413
Planes, S. et al. The Tara Pacific expedition—a pan-ecosystemic approach of the “-omics” complexity of coral reef holobionts across the Pacific Ocean. PLoS Biol. 17, e3000483 (2019).
pubmed: 31545807
pmcid: 6776362
doi: 10.1371/journal.pbio.3000483
Belser, C. et al. Integrative omics framework for characterization of coral reef ecosystems from the Tara Pacific expedition. Sci Data 10, 326 (2023).
pubmed: 37264047
pmcid: 10235121
doi: 10.1038/s41597-023-02204-0
Oury, N., Noël, C., Mona, S., Aurelle, D. & Magalon, H. From genomics to integrative species delimitation? The case study of the Indo-Pacific Pocillopora corals. Mol. Phylogenet. Evol. 184, 107803 (2023).
pubmed: 37120114
doi: 10.1016/j.ympev.2023.107803
Gélin, P., Postaire, B., Fauvelot, C. & Magalon, H. Reevaluating species number, distribution and endemism of the coral genus Pocillopora Lamarck, 1816 using species delimitation methods and microsatellites. Mol. Phylogenet. Evol. 109, 430–446 (2017).
pubmed: 28219759
doi: 10.1016/j.ympev.2017.01.018
Schmidt-Roach, S., Miller, K. J., Lundgren, P. & Andreakis, N. With eyes wide open: a revision of species within and closely related to the Pocillopora damicornis species complex (Scleractinia; Pocilloporidae) using morphology and genetics. Zool. J. Linn. Soc. 170, 1–33 (2014).
doi: 10.1111/zoj.12092
Johnston, E. C., Wyatt, A. S. J., Leichter, J. J. & Burgess, S. C. Niche differences in co-occurring cryptic coral species (Pocillopora spp.). Coral Reefs 41, 767–778 (2022).
doi: 10.1007/s00338-021-02107-9
Hellberg, M. E., Prada, C., Tan, M. H., Forsman, Z. H. & Baums, I. B. Getting a grip at the edge: recolonization and introgression in eastern Pacific Porites corals. J. Biogeogr. 43, 2147–2159 (2016).
doi: 10.1111/jbi.12792
Boissin, E., Leung, J. K. L., Denis, V., Bourmaud, C. A. F. & Gravier-Bonnet, N. Morpho-molecular delineation of structurally important reef species, the fire corals, Millepora spp., at Réunion Island, Southwestern Indian Ocean. Hydrobiologia 847, 1237–1255 (2020).
doi: 10.1007/s10750-020-04179-0
Reich, D., Thangaraj, K., Patterson, N., Price, A. L. & Singh, L. Reconstructing Indian population history. Nature 461, 489–494 (2009).
pubmed: 19779445
pmcid: 2842210
doi: 10.1038/nature08365
Ellis, N., Smith, S. J. & Pitcher, C. R. Gradient forests: calculating importance gradients on physical predictors. Ecology 93, 156–168 (2012).
pubmed: 22486096
doi: 10.1890/11-0252.1
Lombard, F. et al. Open science resources from the Tara Pacific expedition across coral reef and surface ocean ecosystems. Sci. Data 10, 324 (2023).
pubmed: 37264023
pmcid: 10235096
doi: 10.1038/s41597-022-01757-w
Johnston, E. C. et al. A genomic glance through the fog of plasticity and diversification in Pocillopora. Sci. Rep. 7, 5991 (2017).
pubmed: 28729652
pmcid: 5519588
doi: 10.1038/s41598-017-06085-3
Marti-Puig, P. et al. Extreme phenotypic polymorphism in the coral genus Pocillopora; micro-morphology corresponds to mitochondrial groups, while colony morphology does not. Bull. Mar. Sci. 90, 211–231 (2014).
doi: 10.5343/bms.2012.1080
Paz-García, D. A. et al. Morphological variation and different branch modularity across contrasting flow conditions in dominant Pocillopora reef-building corals. Oecologia 178, 207–218 (2015).
pubmed: 25556295
doi: 10.1007/s00442-014-3199-9
Todd, P. A. Morphological plasticity in scleractinian corals. Biol. Rev. Camb. Philos. Soc. 83, 315–337 (2008).
pubmed: 18979594
doi: 10.1111/j.1469-185X.2008.00045.x
Voolstra, C. R. et al. Consensus guidelines for advancing coral holobiont genome and specimen voucher deposition. Front. Mar. Sci. 8, 1029 (2021).
doi: 10.3389/fmars.2021.701784
Bongaerts, P. et al. Morphological stasis masks ecologically divergent coral species on tropical reefs. Curr. Biol. 31, 2286–2298.e8 (2021).
pubmed: 33811819
doi: 10.1016/j.cub.2021.03.028
Boulay, J. N., Hellberg, M. E., Cortés, J. & Baums, I. B. Unrecognized coral species diversity masks differences in functional ecology. Proc. Royal Soc. B: Biol. Sci. 281, 20131580 (2014).
doi: 10.1098/rspb.2013.1580
Baums, I. B., Boulay, J. N., Polato, N. R. & Hellberg, M. E. No gene flow across the Eastern Pacific Barrier in the reef building coral Porites lobata. Mol. Ecol. 21, 5418–5433 (2012).
pubmed: 22943626
doi: 10.1111/j.1365-294X.2012.05733.x
Palumbi, S. R. Population genetics, demographic connectivity, and the design of marine reserves. Ecol. Appl. 13, 146–158 (2003).
doi: 10.1890/1051-0761(2003)013[0146:PGDCAT]2.0.CO;2
Van Oppen, M. J. H. & Gates, R. D. Conservation genetics and the resilience of reef-building corals. Mol. Ecol. 15, 3863–3883 (2006).
pubmed: 17054489
doi: 10.1111/j.1365-294X.2006.03026.x
Colton, M. A. et al. Coral conservation in a warming world must harness evolutionary adaptation. Nat. Ecol. Evol. 6, 1405–1407 (2022).
pubmed: 36114282
doi: 10.1038/s41559-022-01854-4
Brown, N. P., Forsman, Z. H., Tisthammer, K. T. & Richmond, R. H. A resilient brooding coral in the broadcast spawning Porites lobata species complex: a new endemic, introduced species, mutant, or new adaptive potential? Coral Reefs 39, 809–818 (2020).
doi: 10.1007/s00338-020-01922-w
Richmond, R. & Hunter, C. Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar. Ecol. Prog. Ser. 60, 185–203 (1990).
doi: 10.3354/meps060185
Fadlallah, Y. H. Reproduction in the coral Pocillopora verrucosa on the reefs adjacent to the industrial city of Yanbu (Red Sea, Saudi Arabia). Proc. Fifth Int. Coral Reef Cong., Tahiti 4, 313–318 (1985).
Sier, C. J. S. & Olive, P. J. W. Reproduction and reproductive variability in the coral Pocillopora verrucosa from the Republic of Maldives. Mar. Biol. 118, 713–722 (1994).
doi: 10.1007/BF00347520
Stimson, J. S. Mode and timing of reproduction in some common hermatypic corals of Hawaii and Enewetak. Mar. Biol. 48, 173–184 (1978).
doi: 10.1007/BF00395017
Schmidt-Roach, S., Miller, K. J., Woolsey, E., Gerlach, G. & Baird, A. H. Broadcast spawning by Pocillopora species on the Great Barrier Reef. PLoS ONE 7, e50847 (2012).
pubmed: 23227215
pmcid: 3515527
doi: 10.1371/journal.pone.0050847
Polato, N. R., Concepcion, G. T., Toonen, R. J. & Baums, I. B. Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol. Ecol. 19, 4661–4677 (2010).
pubmed: 20887361
doi: 10.1111/j.1365-294X.2010.04836.x
Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E. & Cupul-Magaña, A. L. Differential response to cold and warm water conditions in Pocillopora colonies from the Central Mexican Pacific. J. Exp. Mar. Bio. Ecol. 391, 57–64 (2010).
doi: 10.1016/j.jembe.2010.06.006
Magalon, H., Adjeroud, M. & Veuille, M. Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol. Ecol. 14, 1861–1868 (2005).
pubmed: 15910311
doi: 10.1111/j.1365-294X.2005.02430.x
Shinzato, C. et al. Whole-genome sequencing highlights conservative genomic strategies of a stress-tolerant, long-lived Scleractinian coral, Porites australiensis Vaughan, 1918. Genome Biol. Evol. 13, evab270 (2021).
Ziegler, M., Roder, C. M., Büchel, C. & Voolstra, C. R. Limits to physiological plasticity of the coral Pocillopora verrucosa from the central Red Sea. Coral Reefs 33, 1115–1129 (2014).
doi: 10.1007/s00338-014-1192-8
Darling, E. S. et al. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15, 1378–1386 (2012).
pubmed: 22938190
doi: 10.1111/j.1461-0248.2012.01861.x
Sawall, Y. et al. Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci. Rep. 5, 8940 (2015).
pubmed: 25754672
pmcid: 5155415
doi: 10.1038/srep08940
D’Croz, L. & Maté, J. L. Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23, 473–483 (2004).
doi: 10.1007/s00338-004-0397-7
Bairos-Novak, K. R., Hoogenboom, M. O., van Oppen, M. J. H. & Connolly, S. R. Coral adaptation to climate change: meta-analysis reveals high heritability across multiple traits. Glob. Chang. Biol. 27, 5694–5710 (2021).
pubmed: 34482591
doi: 10.1111/gcb.15829
Sully, S., Burkepile, D. E., Donovan, M. K., Hodgson, G. & van Woesik, R. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 1264 (2019).
pubmed: 30894534
pmcid: 6427037
doi: 10.1038/s41467-019-09238-2
Kopylova, E., Noé, L. & Touzet, H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28, 3211–3217 (2012).
pubmed: 23071270
doi: 10.1093/bioinformatics/bts611
Noel, B. et al. Pervasive tandem duplications and convergent evolution shape coral genomes. Genome Biol. 24, 123 (2023).
pubmed: 37264421
pmcid: 10236652
doi: 10.1186/s13059-023-02960-7
Van der Auwera, G. A. & O’Connor, B. D. Genomics in the Cloud: Using Docker, GATK, and WDL in Terra (O’Reilly Media, Inc., 2020).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Li, H. et al. The sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).
pubmed: 21221095
pmcid: 3346182
doi: 10.1038/nbt.1754
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).
Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).
pubmed: 21903627
pmcid: 3198575
doi: 10.1093/bioinformatics/btr509
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 21572440
pmcid: 3571712
doi: 10.1038/nbt.1883
Sonnhammer, E. L. L. & Östlund, G. InParanoid 8: orthology analysis between 273 proteomes, mostly eukaryotic. Nucleic Acids Res. 43, D234–D239 (2015).
pubmed: 25429972
doi: 10.1093/nar/gku1203
Hume, B. C. C. et al. Resources from: disparate patterns of genetic divergence in three widespread corals across a pan-pacific environmental gradient highlights species-specific adaptation trajectories. https://doi.org/10.5281/zenodo.7180966 (2022).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Lischer, H. E. L. & Excoffier, L. PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics 28, 298–299 (2012).
pubmed: 22110245
doi: 10.1093/bioinformatics/btr642
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
pubmed: 29722887
pmcid: 5967553
doi: 10.1093/molbev/msy096
Chifman, J. & Kubatko, L. Quartet inference from SNP data under the coalescent model. Bioinformatics 30, 3317–3324 (2014).
pubmed: 25104814
pmcid: 4296144
doi: 10.1093/bioinformatics/btu530
Swofford, D. L., PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. (Sinauer Associates, Sunderland, Massachusetts, 2003).
Frichot, E., Mathieu, F., Trouillon, T., Bouchard, G. & François, O. Fast and efficient estimation of individual ancestry coefficients. Genetics 196, 973–983 (2014).
pubmed: 24496008
pmcid: 3982712
doi: 10.1534/genetics.113.160572
Frichot, E. & François, O. LEA: An R package for landscape and ecological association studies. Methods Ecol. Evol. 6, 925–929 (2015).
doi: 10.1111/2041-210X.12382
Bailleul, D., Stoeckel, S. & Arnaud-Haond, S. RClone: a package to identify MultiLocus Clonal Lineages and handle clonal data sets in r. Methods Ecol. Evol. 7, 966–970 (2016).
doi: 10.1111/2041-210X.12550
Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281 (2014).
pubmed: 24688859
pmcid: 3961149
doi: 10.7717/peerj.281
Kamvar, Z. N., Brooks, J. C. & Grünwald, N. J. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6, 208 (2015).
pubmed: 26113860
pmcid: 4462096
doi: 10.3389/fgene.2015.00208
Jombart, T. & Ahmed, I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).
pubmed: 21926124
pmcid: 3198581
doi: 10.1093/bioinformatics/btr521
Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).
pubmed: 18397895
doi: 10.1093/bioinformatics/btn129
Grummer, J. A., Bryson, R. W. Jr & Reeder, T. W. Species delimitation using Bayes factors: simulations and application to the Sceloporus scalaris species group (Squamata: Phrynosomatidae). Syst. Biol. 63, 119–133 (2014).
pubmed: 24262383
doi: 10.1093/sysbio/syt069
Bryant, D., Bouckaert, R., Felsenstein, J., Rosenberg, N. A. & RoyChoudhury, A. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Mol. Biol. Evol. 29, 1917–1932 (2012).
pubmed: 22422763
pmcid: 3408069
doi: 10.1093/molbev/mss086
Bouckaert, R. et al. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).
pubmed: 30958812
pmcid: 6472827
doi: 10.1371/journal.pcbi.1006650
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Katoh, K., Misawa, K., Kuma, K.-I. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).
pubmed: 12136088
pmcid: 135756
doi: 10.1093/nar/gkf436
Tamura, K., Stecher, G. & Kumar, S. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Joly, S. & Bruneau, A. Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: an example from Rosa in North America. Syst. Biol. 55, 623–636 (2006).
pubmed: 16969938
doi: 10.1080/10635150600863109
Bonito, V. E., Baird, A. H., Bridge, T., Cowman, P. F. & Fenner, D. Types, topotypes and vouchers are the key to progress in coral taxonomy: comment on Wepfer et al. (2020). Mol. Phylogenet. Evol. 159, 107104 (2021).
pubmed: 33609706
doi: 10.1016/j.ympev.2021.107104
LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580.e6 (2018).
pubmed: 30100341
doi: 10.1016/j.cub.2018.07.008
Louis, M. et al. Selection on ancestral genetic variation fuels repeated ecotype formation in bottlenose dolphins. Sci. Adv. 7, eabg1245 (2021).
pubmed: 34705499
pmcid: 8550227
doi: 10.1126/sciadv.abg1245
Pickrell, J. K. & Pritchard, J. K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012).
pubmed: 23166502
pmcid: 3499260
doi: 10.1371/journal.pgen.1002967
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pubmed: 17701901
pmcid: 1950838
doi: 10.1086/519795
Fitak, R. R. OptM: estimating the optimal number of migration edges on population trees using Treemix. Biol. Methods Protoc. 6 https://doi.org/10.1093/biomethods/bpab017 (2021).
Milanesi, M. et al. BITE: an R package for biodiversity analyses. Preprint at bioRxiv https://doi.org/10.1101/181610 (2017).
Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).
pubmed: 28563791
Rousset, F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228 (1997).
pubmed: 9093870
pmcid: 1207888
doi: 10.1093/genetics/145.4.1219
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6. 2019. https://CRAN.Rproject.org/package=vegan (2020).
Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).
doi: 10.18637/jss.v025.i01
Capblancq, T. & Forester, B. R. Redundancy analysis: a Swiss Army Knife for landscape genomics. Methods Ecol. Evol. 12, 2298–2309 (2021).
doi: 10.1111/2041-210X.13722
Galimberti, M. et al. Detecting selection from linked sites using an F-model. Genetics 216, 1205–1215 (2020).
pubmed: 33067324
pmcid: 7768260
doi: 10.1534/genetics.120.303780
Link, V. et al. ATLAS: analysis tools for low-depth and ancient samples. Preprint at bioRxiv https://doi.org/10.1101/105346 (2017).
Di Tommaso, P. et al. Nextflow enables reproducible computational workflows. Nat. Biotechnol. 35, 316–319 (2017).
pubmed: 28398311
doi: 10.1038/nbt.3820
Tara Pacific Consortium. Tara Pacific Expedition Participants. at https://doi.org/10.5281/ZENODO.3777760 (2020).
Spalding, M., Mark D. Spalding, M. A., Ravilious, C., Green, E. P. & United Nations Environment Programme. World Atlas of Coral Reefs (University of California Press, 2001).
UNEP-WCMC, WorldFish Centre, WRI, TNC. Global distribution of warm-water coral reefs, compiled from multiple sources (listed in “Coral_Source.mdb”), and including IMaRS-USF and IRD (2005), IMaRS-USF (2005) and Spalding et al. (2001). data.unepwcmc.org/datasets/13 (Cambridge (UK): UNEP World Conservation Monitoring Centre, 2010).
Hume, B. C. C. & Voolstra, C. R. didillysquat/reefMapMaker: v0.1.10. https://doi.org/10.5281/zenodo.6826381 (2022).