Seascape Genomics and Phylogeography of the Sailfish (Istiophorus platypterus)

Abstract Permeable phylogeographic barriers characterize the vast open ocean, boosting gene flow and counteracting population differentiation and speciation of widely distributed and migratory species. However, many widely distributed species consists of distinct populations throughout their distribution, evidencing that our understanding of how the marine environment triggers population and species divergence are insufficient. The sailfish is a circumtropical and highly migratory billfish that inhabits warm and productive areas. Despite its ecological and socioeconomic importance as a predator and fishery resource, the species is threatened by overfishing, requiring innovative approaches to improve their management and conservation status. Thus, we presented a novel high-quality reference genome for the species and applied a seascape genomics approach to understand how marine environmental features may promote local adaptation and how it affects gene flow between populations. We delimit two populations between the Atlantic and Indo-Western Pacific oceans and detect outlier loci correlated with sea surface temperature, salinity, oxygen, and chlorophyll concentrations. However, the most significant explanatory factor that explains the differences between populations was isolation by distance. Despite recent population drops, the sailfish populations are not inbred. For billfishes in general, genome-wide heterozygosity was found to be relatively low compared to other marine fishes, evidencing the need to counteract overfishing effects. In addition, in a climate change scenario, management agencies must implement state-of-the-art sequencing methods, consider our findings in their management plans, and monitor genome-wide heterozygosity over time to improve sustainable fisheries and the long-term viability of its populations.

[1]  J. Weir,et al.  The role of divergent ecological adaptation during allopatric speciation in vertebrates , 2022, Science.

[2]  N. Dulvy,et al.  Seventy years of tunas, billfishes, and sharks as sentinels of global ocean health , 2022, Science.

[3]  J. Kriwet,et al.  Fossil Evidence for Earlier Radiation in Istiophorid Billfishes (Teleostei, Istiophoriformes) Uncovered by Comparative Morphology of the Caudal Vertebrae , 2022, Journal of Vertebrate Paleontology.

[4]  Menno J. de Jong,et al.  Genomic Impact of Whaling in North Atlantic Fin Whales , 2022, Molecular biology and evolution.

[5]  C. Möllmann,et al.  Environmental controls of billfish species in the Indian Ocean and implications for their management and conservation , 2022, Diversity and Distributions.

[6]  P. Unmack,et al.  Genomics outperforms genetics to manage mistakes in fisheries stocking of threatened species , 2022, Biodiversity and Conservation.

[7]  Robert M. Waterhouse,et al.  The era of reference genomes in conservation genomics. , 2022, Trends in ecology & evolution.

[8]  P. Gagnaire,et al.  Age-specific survivorship and fecundity shape genetic diversity in marine fishes , 2021 .

[9]  J. DeWoody,et al.  The long‐standing significance of genetic diversity in conservation , 2021, Molecular ecology.

[10]  Felipe A. Simão,et al.  BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes , 2021, Molecular biology and evolution.

[11]  J. Weir,et al.  Character displacement drives trait divergence in a continental fauna , 2021, Proceedings of the National Academy of Sciences.

[12]  A. F. de Amorim,et al.  Global phylogeography of sailfish: deep evolutionary lineages with implications for fisheries management , 2021, Hydrobiologia.

[13]  N. Stenseth,et al.  Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic , 2021, Proceedings of the National Academy of Sciences.

[14]  Maurizio Rossetto,et al.  A conservation genomics workflow to guide practical management actions , 2021, Global Ecology and Conservation.

[15]  Menno J. de Jong,et al.  Detecting genetic signals of selection in heavily bottlenecked reindeer populations by comparing parallel founder events , 2021, Molecular ecology.

[16]  Yuan Yuan,et al.  The Genomes of Two Billfishes Provide Insights into the Evolution of Endothermy in Teleosts , 2021, Molecular biology and evolution.

[17]  R. Freckleton,et al.  Overfishing and habitat loss drive range contraction of iconic marine fishes to near extinction , 2021, Science Advances.

[18]  M. Musyl,et al.  Current status and potential contributions of fisheries statistics from artisanal fisheries for managing juvenile istiophorid billfishes in Southern Brazil , 2021, Environmental biology of fishes.

[19]  Menno J. de Jong,et al.  SambaR: An R package for fast, easy and reproducible population‐genetic analyses of biallelic SNP data sets , 2021, Molecular ecology resources.

[20]  D. Madigan,et al.  Water column structure defines vertical habitat of twelve pelagic predators in the South Atlantic , 2020, ICES Journal of Marine Science.

[21]  D. Abecasis,et al.  Reduced Global Genetic Differentiation of Exploited Marine Fish Species , 2020, Molecular biology and evolution.

[22]  Yun-Xin Fu,et al.  Stairway Plot 2: demographic history inference with folded SNP frequency spectra , 2020, Genome Biology.

[23]  J. Dekker,et al.  Chromosome-Level Assembly of the Atlantic Silverside Genome Reveals Extreme Levels of Sequence Diversity and Structural Genetic Variation , 2020, bioRxiv.

[24]  G. Luikart,et al.  IUCN Red List and the value of integrating genetics , 2020, Conservation Genetics.

[25]  S. Koren,et al.  Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies , 2020, Genome Biology.

[26]  Xun Xu,et al.  TGS-GapCloser: A fast and accurate gap closer for large genomes with low coverage of error-prone long reads , 2020, GigaScience.

[27]  A. Pardiñas,et al.  Recent demographic history inferred by high-resolution analysis of linkage disequilibrium. , 2020, Molecular biology and evolution.

[28]  N. Wambiji,et al.  Potential for conflicts in recreational and artisanal billfish fisheries on the coast of Kenya , 2020 .

[29]  Sergey Koren,et al.  Towards complete and error-free genome assemblies of all vertebrate species , 2020, Nature.

[30]  M. Blum,et al.  Performing highly efficient genome scans for local adaptation with R package pcadapt version 4. , 2020, Molecular biology and evolution.

[31]  W. Funk,et al.  Population genomics for wildlife conservation and management , 2020, Molecular ecology.

[32]  T. Herbert,et al.  Plio‐Pleistocene Hemispheric (A)Symmetries in the Northern and Southern Hemisphere Midlatitudes , 2020, Paleoceanography and Paleoclimatology.

[33]  Christopher M. Anderson,et al.  Effective fisheries management instrumental in improving fish stock status , 2020, Proceedings of the National Academy of Sciences.

[34]  Andrew G. Clark,et al.  RepeatModeler2: automated genomic discovery of transposable element families , 2019, bioRxiv.

[35]  Olga Chernomor,et al.  IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era , 2019, bioRxiv.

[36]  Parice A. Brandies,et al.  The Value of Reference Genomes in the Conservation of Threatened Species , 2019, Genes.

[37]  C. dePamphilis,et al.  GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes , 2019, bioRxiv.

[38]  Tyler K. Chafin,et al.  BA3‐SNPs: Contemporary migration reconfigured in BayesAss for next‐generation sequence data , 2019, Methods in Ecology and Evolution.

[39]  B. K. Hand,et al.  Aquatic Landscape Genomics and Environmental Effects on Genetic Variation. , 2019, Trends in ecology & evolution.

[40]  V. Heikinheimo,et al.  Identifying global centers of unsustainable commercial harvesting of species , 2019, Science Advances.

[41]  Matteo Fumagalli,et al.  ngsLD: evaluating linkage disequilibrium using genotype likelihoods , 2019, Bioinform..

[42]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[43]  A. Rijnsdorp,et al.  Seascape genetics of a flatfish reveals local selection under high levels of gene flow , 2018 .

[44]  H. Verbruggen,et al.  Bio‐ORACLE v2.0: Extending marine data layers for bioclimatic modelling , 2018 .

[45]  John F. Walter,et al.  Factors related to the decline and rebuilding of billfish stocks in the Atlantic and Indian oceans , 2018 .

[46]  D. Bailey,et al.  A physiological perspective on fisheries‐induced evolution , 2018, Evolutionary applications.

[47]  Peter Haase,et al.  A suite of essential biodiversity variables for detecting critical biodiversity change , 2018, Biological reviews of the Cambridge Philosophical Society.

[48]  D. Dunn,et al.  A review of the impacts of fisheries on open-ocean ecosystems , 2017 .

[49]  K. Shimizu,et al.  Reference-guided de novo assembly approach improves genome reconstruction for related species , 2017, BMC Bioinformatics.

[50]  R. Evans,et al.  Seascape genomics reveals fine‐scale patterns of dispersal for a reef fish along the ecologically divergent coast of Northwestern Australia , 2017, Molecular ecology.

[51]  D. Kobayashi,et al.  Tropical Marine Fishes and Fisheries and Climate Change , 2017 .

[52]  Heng Li,et al.  Minimap2: pairwise alignment for nucleotide sequences , 2017, Bioinform..

[53]  Neva C. Durand,et al.  De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds , 2016, Science.

[54]  Niranjan Nagarajan,et al.  Fast and accurate de novo genome assembly from long uncorrected reads. , 2017, Genome research.

[55]  J. Lynch‐Stieglitz The Atlantic Meridional Overturning Circulation and Abrupt Climate Change. , 2017, Annual review of marine science.

[56]  A. Meyer,et al.  How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations , 2017, Molecular ecology.

[57]  Benjamin Galuardi,et al.  Sailfish migrations connect productive coastal areas in the West Atlantic Ocean , 2016, Scientific Reports.

[58]  N. Galtier,et al.  Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence , 2016, bioRxiv.

[59]  B. Bowen,et al.  Fishes that rule the world: circumtropical distributions revisited , 2016 .

[60]  Eric D. Crandall,et al.  A decade of seascape genetics: contributions to basic and applied marine connectivity , 2016 .

[61]  J. Graves,et al.  Secondary contact and asymmetrical gene flow in a cosmopolitan marine fish across the Benguela upwelling zone , 2016, Heredity.

[62]  R. Toonen,et al.  Comparative phylogeography of the ocean planet , 2016, Proceedings of the National Academy of Sciences.

[63]  James T. Robinson,et al.  Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom. , 2016, Cell systems.

[64]  Neva C. Durand,et al.  Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. , 2016, Cell systems.

[65]  F. García-Rodríguez,et al.  Genetic diversity and population structure of Indo-Pacific sailfish Istiophorus platypterus in the eastern Pacific , 2016, Fisheries Science.

[66]  Yali Xue,et al.  BCFtools/RoH: a hidden Markov model approach for detecting autozygosity from next-generation sequencing data , 2016, Bioinform..

[67]  D. Pauly,et al.  Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining , 2016, Nature Communications.

[68]  U. Dieckmann,et al.  Fisheries-induced evolution , 2015 .

[69]  J. DeWoody,et al.  The reduction of genetic diversity in threatened vertebrates and new recommendations regarding IUCN conservation rankings , 2015 .

[70]  Ana Conesa,et al.  Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data , 2015, Bioinform..

[71]  M. Whitlock,et al.  Reliable Detection of Loci Responsible for Local Adaptation: Inference of a Null Model through Trimming the Distribution of FST* , 2015, The American Naturalist.

[72]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[73]  W. Chiang,et al.  Analysis of sailfish (Istiophorus platypterus) population structure in the North Pacific Ocean , 2015 .

[74]  J. Graves,et al.  Population structure of istiophorid billfishes , 2015 .

[75]  André E. Punt,et al.  Assessing billfish stocks: A review of current methods and some future directions , 2015 .

[76]  Joel K Llopiz,et al.  Satellite telemetry reveals physical processes driving billfish behavior , 2015, Animal Biotelemetry.

[77]  M. Pinsky,et al.  Marine defaunation: Animal loss in the global ocean , 2015, Science.

[78]  W. B. Ludt,et al.  Shifting seas: the impacts of Pleistocene sea‐level fluctuations on the evolution of tropical marine taxa , 2015 .

[79]  L. Lisiecki,et al.  A Late Pleistocene sea level stack , 2014 .

[80]  Gideon S. Bradburd,et al.  Isolation by environment , 2014, Molecular ecology.

[81]  Anders Albrechtsen,et al.  ANGSD: Analysis of Next Generation Sequencing Data , 2014, BMC Bioinformatics.

[82]  Christina A. Cuomo,et al.  Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement , 2014, PloS one.

[83]  W. Pirovano,et al.  SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information , 2014, BMC Bioinformatics.

[84]  Dong Xie,et al.  BEAST 2: A Software Platform for Bayesian Evolutionary Analysis , 2014, PLoS Comput. Biol..

[85]  A. Hoffmann,et al.  GENETIC ISOLATION BY ENVIRONMENT OR DISTANCE: WHICH PATTERN OF GENE FLOW IS MOST COMMON? , 2014, Evolution; international journal of organic evolution.

[86]  R. Zahn,et al.  Millennial-scale Agulhas Current variability and its implications for salt-leakage through the Indian–Atlantic Ocean Gateway , 2013 .

[87]  F. Santini,et al.  First molecular timetree of billfishes (Istiophoriformes: Acanthomorpha) shows a Late Miocene radiation of marlins and allies , 2013 .

[88]  T. Korneliussen,et al.  Estimating Individual Admixture Proportions from Next Generation Sequencing Data , 2013, Genetics.

[89]  P. Gibbard,et al.  Timing of glaciation during the last glacial cycle: evaluating the concept of a global 'Last Glacial Maximum' (LGM) , 2013 .

[90]  M. Miya,et al.  MitoFish and MitoAnnotator: A Mitochondrial Genome Database of Fish with an Accurate and Automatic Annotation Pipeline , 2013, Molecular biology and evolution.

[91]  Alexey A. Gurevich,et al.  QUAST: quality assessment tool for genome assemblies , 2013, Bioinform..

[92]  S. Beissinger,et al.  Inferring recent historic abundance from current genetic diversity , 2013, Molecular ecology.

[93]  Roger Bivand,et al.  Community ecology in the age of multivariate multiscale spatial analysis , 2012 .

[94]  J. Pauli,et al.  Reliability of genetic bottleneck tests for detecting recent population declines , 2012, Molecular ecology.

[95]  P. Cury,et al.  Biogeography of tuna and billfish communities , 2012 .

[96]  E. Palkovacs The overfishing debate: an eco-evolutionary perspective. , 2011, Trends in ecology & evolution.

[97]  Thibaut Jombart,et al.  adegenet 1.3-1: new tools for the analysis of genome-wide SNP data , 2011, Bioinform..

[98]  Heng Li,et al.  A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data , 2011, Bioinform..

[99]  R. Durbin,et al.  Inference of human population history from individual whole-genome sequences. , 2011, Nature.

[100]  D. Tittensor,et al.  Range contraction in large pelagic predators , 2011, Proceedings of the National Academy of Sciences.

[101]  Josyf Mychaleckyj,et al.  Robust relationship inference in genome-wide association studies , 2010, Bioinform..

[102]  E. Prince,et al.  Ocean scale hypoxia‐based habitat compression of Atlantic istiophorid billfishes , 2010 .

[103]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[104]  Anne Kuhn,et al.  Population genetic diversity and fitness in multiple environments , 2010, BMC Evolutionary Biology.

[105]  Peter Beerli,et al.  Unified Framework to Evaluate Panmixia and Migration Direction Among Multiple Sampling Locations , 2010, Genetics.

[106]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[107]  D. Charlesworth,et al.  The genetics of inbreeding depression , 2009, Nature Reviews Genetics.

[108]  Peter J. Bradbury,et al.  The Last Glacial Maximum , 2009, Science.

[109]  T. Price,et al.  Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. , 2009, Trends in ecology & evolution.

[110]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[111]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[112]  A. Drummond,et al.  Bayesian inference of population size history from multiple loci , 2008, BMC Evolutionary Biology.

[113]  G. Luikart,et al.  Genetic effects of harvest on wild animal populations. , 2008, Trends in ecology & evolution.

[114]  B. Bowen,et al.  Speciation in coral-reef fishes , 2008 .

[115]  Richard Law,et al.  Fisheries-induced evolution: present status and future directions , 2007 .

[116]  Arnaud Estoup,et al.  Geneland: a computer package for landscape genetics , 2005 .

[117]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[118]  J. Hoolihan,et al.  Intraspecific phylogeographic isolation of Arabian Gulf sailfish Istiophorus platypterus inferred from mitochondrial DNA , 2004 .

[119]  E. Prince,et al.  Global overview of the major constituent-based billfish tagging programs and their results since 1954 , 2003 .

[120]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[121]  I. Nakamura SYSTEMATICS OF THE BILLFISHES (XIPHIIDAE AND ISTIOPHORIDAE) , 1983 .

[122]  S. Wright,et al.  Isolation by Distance. , 1943, Genetics.

[123]  E. Michel,et al.  Impact of the Agulhas Return Current on the oceanography of the Kerguelen Plateau region, Southern Ocean, over the last 40 kyrs , 2021 .

[124]  C. Riginos,et al.  Seascape Genomics: Contextualizing Adaptive and Neutral Genomic Variation in the Ocean Environment , 2019, Population Genomics.

[125]  M. Pinsky,et al.  Meta-analysis reveals lower genetic diversity in overfished populations. , 2014, Molecular ecology.

[126]  M. Visbeck,et al.  Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes , 2012 .

[127]  J. Graves,et al.  PHYLOGENY OF RECENT BILLFISHES (XIPHIOIDEI) , 2006 .