Drivers of neutral and adaptive differentiation in pike (Esox lucius) populations from contrasting environments

Understanding how eco‐evolutionary processes and environmental factors drive population differentiation and adaptation are key challenges in evolutionary biology of relevance for biodiversity protection. Differentiation requires at least partial reproductive separation, which may result from different modes of isolation such as geographic isolation (allopatry) or isolation by distance (IBD), resistance (IBR), and environment (IBE). Despite that multiple modes might jointly influence differentiation, studies that compare the relative contributions are scarce. Using RADseq, we analyse neutral and adaptive genetic diversity and structure in 11 pike (Esox lucius) populations from contrasting environments along a latitudinal gradient (54.9–63.6°N), to investigate the relative effects of IBD, IBE and IBR, and to assess whether the effects differ between neutral and adaptive variation, or across structural levels. Patterns of neutral and adaptive variation differed, probably reflecting that they have been differently affected by stochastic and deterministic processes. The importance of the different modes of isolation differed between neutral and adaptive diversity, yet were consistent across structural levels. Neutral variation was influenced by interactions among all three modes of isolation, with IBR (seascape features) playing a central role, wheares adaptive variation was mainly influenced by IBE (environmental conditions). Taken together, this and previous studies suggest that it is common that multiple modes of isolation interactively shape patterns of genetic variation, and that their relative contributions differ among systems. To enable identification of general patterns and understand how various factors influence the relative contributions, it is important that several modes are simultaneously investigated in additional populations, species and environmental settings.

[1]  M. Pilot.  Disentangling the admixed trails of grey wolf evolution , 2021, Molecular ecology.

[2]  F. Lei,et al.  Most Genomic Loci Misrepresent the Phylogeny of an Avian Radiation Because of Ancient Gene Flow , 2021, Systematic biology.

[3]  R. Arlinghaus,et al.  Genetic population structure of a top predatory fish (northern pike, Esox lucius ) covaries with anthropogenic alteration of freshwater ecosystems , 2021, Freshwater Biology.

[4]  C. Haddad,et al.  Isolation by environment and recurrent gene flow shaped the evolutionary history of a continentally distributed Neotropical treefrog , 2020, Journal of Biogeography.

[5]  A. Lima,et al.  The influence of environmental variation on the genetic structure of a poison frog distributed across continuous Amazonian rainforest. , 2020, The Journal of heredity.

[6]  A. Forsman,et al.  Comparing the Performance of Microsatellites and RADseq in Population Genetic Studies: Analysis of Data for Pike (Esox lucius) and a Synthesis of Previous Studies , 2020, Frontiers in Genetics.

[7]  P. Larsson,et al.  Genetic differentiation between and within ecotypes of pike (Esox lucius) in the Baltic Sea , 2019, Aquatic Conservation: Marine and Freshwater Ecosystems.

[8]  R. Tinghitella,et al.  Geography is more important than host plant use for the population genetic structure of a generalist insect herbivore , 2019, Molecular ecology.

[9]  Shan Jiang,et al.  Isolation-by-environment as a driver of genetic differentiation among populations of the only broad-leaved evergreen shrub Ammopiptanthus mongolicus in Asian temperate deserts , 2019, Scientific Reports.

[10]  B. Walsh,et al.  Evolutionary Quantitative Genetics , 2019, Handbook of Statistical Genomics.

[11]  P. Larsson,et al.  Adaptations of early development to local spawning temperature in anadromous populations of pike (Esox lucius) , 2019, BMC Evolutionary Biology.

[12]  P. Tibblin,et al.  Predator-prey role reversal may impair the recovery of declining pike populations. , 2019, The Journal of animal ecology.

[13]  J. Höglund,et al.  Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation , 2019, Molecular ecology.

[14]  Yaqing Chang,et al.  The Impact of Chronic Heat Stress on the Growth, Survival, Feeding, and Differential Gene Expression in the Sea Urchin Strongylocentrotus intermedius , 2019, Front. Genet..

[15]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v4: recent updates and new developments , 2019, Nucleic Acids Res..

[16]  J. Olsson.  Past and Current Trends of Coastal Predatory Fish in the Baltic Sea with a Focus on Perch, Pike, and Pikeperch , 2019, Fishes.

[17]  F. Werneck,et al.  Model-based riverscape genetics: disentangling the roles of local and connectivity factors in shaping spatial genetic patterns of two Amazonian turtles with different dispersal abilities , 2019, Evolutionary Ecology.

[18]  A. Forsman,et al.  Contrasting patterns of neutral and functional genetic diversity in stable and disturbed environments , 2018, Ecology and evolution.

[19]  Bernardo J. Clavijo,et al.  Genomic architecture and introgression shape a butterfly radiation , 2018, Science.

[20]  C. Adams,et al.  RADseq and mate choice assays reveal unidirectional gene flow among three lamprey ecotypes despite weak assortative mating: Insights into the formation and stability of multiple ecotypes in sympatry , 2018, Molecular ecology.

[21]  Tiffany J. Chen,et al.  A temporal transcriptome and methylome in human embryonic stem cell-derived cardiomyocytes identifies novel regulators of early cardiac development , 2018, Epigenetics.

[22]  B. Browning,et al.  A one penny imputed genome from next generation reference panels , 2018, bioRxiv.

[23]  H. Wen,et al.  Liver transcriptome analysis reveals extensive transcriptional plasticity during acclimation to low salinity in Cynoglossus semilaevis , 2018, BMC Genomics.

[24]  A. Vainikka,et al.  Comparison of Migratory and Resident Populations of Brown Trout Reveals Candidate Genes for Migration Tendency , 2018, Genome biology and evolution.

[25]  Rémi M. Daigle,et al.  Asymmetric oceanographic processes mediate connectivity and population genetic structure, as revealed by RADseq, in a highly dispersive marine invertebrate (Parastichopus californicus) , 2018, Molecular ecology.

[26]  P. Larsson,et al.  Variation in salinity tolerance between and within anadromous subpopulations of pike (Esox lucius) , 2018, Scientific Reports.

[27]  Bengt Hansson,et al.  Genetic structure of the grey side-gilled sea slug (Pleurobranchaea maculata) in coastal waters of New Zealand , 2017, bioRxiv.

[28]  Josephine R. Paris,et al.  Lost in parameter space: a road map for stacks , 2017 .

[29]  Å. Austin,et al.  A cross-scale trophic cascade from large predatory fish to algae in coastal ecosystems , 2017, Proceedings of the Royal Society B: Biological Sciences.

[30]  S. Dash,et al.  Sticklebacks adapted to divergent osmotic environments show differences in plasticity for kidney morphology and candidate gene expression , 2017, Journal of Experimental Biology.

[31]  A. Norkko,et al.  Extraordinarily rapid speciation in a marine fish , 2017, Proceedings of the National Academy of Sciences.

[32]  J. Olsson,et al.  Temporally stable, weak genetic structuring in brackish water northern pike (Esox lucius) in the Baltic Sea indicates a contrasting divergence pattern relative to freshwater populations , 2017 .

[33]  D. Bekkevold,et al.  Pike (Esox lucius L.) on the edge: consistent individual movement patterns in transitional waters of the western Baltic , 2016, Hydrobiologia.

[34]  Måns Magnusson,et al.  MultiQC: summarize analysis results for multiple tools and samples in a single report , 2016, Bioinform..

[35]  Baocheng Guo,et al.  Population genomic evidence for adaptive differentiation in the Baltic Sea herring , 2016, Molecular ecology.

[36]  P. Larsson,et al.  Causes and consequences of intra-specific variation in vertebral number , 2016, Scientific Reports.

[37]  Chung-Te Chang,et al.  Disentangling the effects of isolation-by-distance and isolation-by-environment on genetic differentiation among Rhododendron lineages in the subgenus Tsutsusi , 2016, Tree Genetics & Genomes.

[38]  P. Larsson,et al.  Testing for Local Adaptation to Spawning Habitat in Sympatric Subpopulations of Pike by Reciprocal Translocation of Embryos , 2016, PloS one.

[39]  G. Evanno,et al.  Seascape and its effect on migratory life‐history strategy influences gene flow among coastal brown trout (Salmo trutta) populations in the English Channel , 2016 .

[40]  G. Luikart,et al.  Harnessing the power of RADseq for ecological and evolutionary genomics , 2016, Nature Reviews Genetics.

[41]  O. Gaggiotti,et al.  A new FST‐based method to uncover local adaptation using environmental variables , 2015 .

[42]  S. Narum,et al.  Population differentiation determined from putative neutral and divergent adaptive genetic markers in Eulachon (Thaleichthys pacificus, Osmeridae), an anadromous Pacific smelt , 2015, Molecular ecology resources.

[43]  S. Cushman,et al.  Isolation by distance, resistance and/or clusters? Lessons learned from a forest‐dwelling carnivore inhabiting a heterogeneous landscape , 2015, Molecular ecology.

[44]  F. Bonhomme,et al.  Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era , 2015, Evolutionary applications.

[45]  T. Cezard,et al.  High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment , 2015, Molecular ecology.

[46]  P. Larsson,et al.  Pike Esox lucius as an emerging model organism for studies in ecology and evolutionary biology: a review , 2015, Journal of fish biology.

[47]  P. Larsson,et al.  Ecology, evolution, and management strategies of northern pike populations in the Baltic Sea , 2015, AMBIO.

[48]  P. Johannessen,et al.  Evolutionary Divergence of Adult Body Size and Juvenile Growth in Sympatric Subpopulations of a Top Predator in Aquatic Ecosystems , 2015, The American Naturalist.

[49]  J. Hemmer-Hansen,et al.  From regionally predictable to locally complex population structure in a freshwater top predator: river systems are not always the unit of connectivity in Northern Pike Esox lucius , 2015 .

[50]  Baocheng Guo,et al.  Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks , 2015, BMC Biology.

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

[52]  N. Stenseth,et al.  Circumpolar phylogeography of the northern pike (Esox lucius) and its relationship to the Amur pike (E. reichertii) , 2014, Frontiers in Zoology.

[53]  B. Koop,et al.  The Genome and Linkage Map of the Northern Pike (Esox lucius): Conserved Synteny Revealed between the Salmonid Sister Group and the Neoteleostei , 2014, PloS one.

[54]  P. Larsson,et al.  Elemental fingerprinting in otoliths reveals natal homing of anadromous Baltic Sea pike (Esox lucius L.) , 2014 .

[55]  M. Stephens,et al.  fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets , 2014, Genetics.

[56]  É. Frichot,et al.  Genome scan methods against more complex models: when and how much should we trust them? , 2014, Molecular ecology.

[57]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[58]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[59]  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.

[60]  A. Forsman.  Effects of genotypic and phenotypic variation on establishment are important for conservation, invasion, and infection biology , 2013, Proceedings of the National Academy of Sciences.

[61]  N. Patterson,et al.  Estimating and interpreting FST: The impact of rare variants , 2013, Genome research.

[62]  R. Butlin,et al.  A systematic review of phenotypic responses to between-population outbreeding , 2013, Environmental Evidence.

[63]  Angel Amores,et al.  Stacks: an analysis tool set for population genomics , 2013, Molecular ecology.

[64]  L. Duret,et al.  Is RAD-seq suitable for phylogenetic inference? An in silico assessment and optimization , 2013, Ecology and evolution.

[65]  E. Bermingham,et al.  On the spatial scale of dispersal in coral reef fishes , 2012, Molecular ecology.

[66]  A. Forsman,et al.  Population‐level consequences of polymorphism, plasticity and randomized phenotype switching: a review of predictions , 2012, Biological reviews of the Cambridge Philosophical Society.

[67]  Dianne H Brunton,et al.  The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song. , 2012, Ecology letters.

[68]  N. Patrik.  What is ecological speciation , 2012 .

[69]  J. Olsson,et al.  Genetic structure of whitefish (Coregonus maraena) in the Baltic Sea , 2012 .

[70]  A. Amores,et al.  Stacks: Building and Genotyping Loci De Novo From Short-Read Sequences , 2011, G3: Genes | Genomes | Genetics.

[71]  J. Olsson,et al.  Genetic population structure of perch Perca fluviatilis along the Swedish coast of the Baltic Sea. , 2011, Journal of fish biology.

[72]  G. Somero,et al.  Transcriptomic responses to salinity stress in invasive and native blue mussels (genus Mytilus) , 2011, Molecular ecology.

[73]  D. Bekkevold,et al.  High salinity tolerance in eggs and fry of a brackish Esox lucius population , 2010 .

[74]  M. Casini,et al.  Recruitment failure of coastal predatory fish in the Baltic Sea coincident with an offshore ecosystem regime shift , 2010 .

[75]  Jonathan K. Pritchard,et al.  Adaptation – not by sweeps alone , 2010, Nature Reviews Genetics.

[76]  J. Ruuhijärvi,et al.  Coastal and freshwater pikeperch (Sander lucioperca) populations differ genetically in the Baltic Sea basin. , 2010, Hereditas.

[77]  P. Larsson,et al.  Assessment of natal origin of pike (Esox lucius) in the Baltic Sea using Sr:Ca in otoliths , 2010, Environmental Biology of Fishes.

[78]  Detlef Weigel,et al.  Genome‐wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies , 2010, Molecular ecology.

[79]  Joseph K. Pickrell,et al.  The Genetics of Human Adaptation: Hard Sweeps, Soft Sweeps, and Polygenic Adaptation , 2010, Current Biology.

[80]  G. Bell.  Fluctuating selection: the perpetual renewal of adaptation in variable environments , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[81]  E. Leskinen,et al.  Potential reasons for the changes in the abundance of pike, Esox lucius, in the western Gulf of Finland, 1939-2007 , 2009 .

[82]  M. Fay,et al.  Genetic diversity and differentiation processes in the ploidy series of Olea europaea L.: a multiscale approach from subspecies to insular populations , 2009, Molecular ecology.

[83]  W. Hutchinson.  The dangers of ignoring stock complexity in fishery management: the case of the North Sea cod , 2008, Biology Letters.

[84]  D. Post,et al.  Intraspecific variation in a predator affects community structure and cascading trophic interactions. , 2008, Ecology.

[85]  Mark Vellend,et al.  Ecological consequences of genetic diversity. , 2008, Ecology letters.

[86]  J. Craig,et al.  A short review of pike ecology , 2008, Hydrobiologia.

[87]  Patrik Nosil,et al.  Heterogeneous Genomic Differentiation Between Walking-Stick Ecotypes: “Isolation by Adaptation” and Multiple Roles for Divergent Selection , 2008, Evolution; international journal of organic evolution.

[88]  R. O’Hara,et al.  Comparative studies of quantitative trait and neutral marker divergence: a meta‐analysis , 2008, Journal of evolutionary biology.

[89]  M. Björklund,et al.  CRYPTIC BARRIERS TO DISPERSAL WITHIN A LAKE ALLOW GENETIC DIFFERENTIATION OF EURASIAN PERCH , 2007, Evolution; international journal of organic evolution.

[90]  Andrew P Hendry,et al.  The speed of ecological speciation. , 2007, Functional ecology.

[91]  N. Melamed-Book,et al.  Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance , 2006, Proceedings of the National Academy of Sciences.

[92]  Philip W. Hedrick,et al.  Genetic Polymorphism in Heterogeneous Environments: The Age of Genomics , 2006 .

[93]  B. Mcrae.  ISOLATION BY RESISTANCE , 2006, Evolution; international journal of organic evolution.

[94]  Felix Gugerli,et al.  Adaptive vs. neutral genetic diversity: implications for landscape genetics , 2006, Landscape Ecology.

[95]  Marti J. Anderson,et al.  Distance‐Based Tests for Homogeneity of Multivariate Dispersions , 2006, Biometrics.

[96]  D. Ebert,et al.  Genetic Diversity and Genetic Differentiation in Daphnia Metapopulations With Subpopulations of Known Age , 2005, Genetics.

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

[98]  A. Kapuscinski,et al.  Spatial genetic structure of northern pike (Esox lucius) in the Baltic Sea , 2005, Molecular ecology.

[99]  A. Hendry,et al.  Population structure attributable to reproductive time: isolation by time and adaptation by time , 2005, Molecular ecology.

[100]  V. Loeschcke,et al.  Microsatellite DNA analysis of northern pike (Esox lucius L.) populations: Insights into the genetic structure and demographic history of a genetically depauperate species , 2004 .

[101]  K. Rowe,et al.  Surviving the ice: Northern refugia and postglacial colonization. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[102]  G. Maes,et al.  Indications for a recent Holarctic expansion of pike based on a preliminary study of mtDNA variation , 2003 .

[103]  R. Petit,et al.  Glacial Refugia: Hotspots But Not Melting Pots of Genetic Diversity , 2003, Science.

[104]  K. Limburg,et al.  Newly discovered reproductive isolation reveals sympatric populations of Esox lucius in the Baltic , 2002 .

[105]  Peter Rothery,et al.  Confidence limits for regression relationships between distance matrices: Estimating gene flow with distance , 2002 .

[106]  R. Frankham,et al.  HOW CLOSELY CORRELATED ARE MOLECULAR AND QUANTITATIVE MEASURES OF GENETIC VARIATION? A META‐ANALYSIS , 2001, Evolution; international journal of organic evolution.

[107]  R. Stephenson.  Stock complexity in fisheries management: a perspective of emerging issues related to population sub-units , 1999 .

[108]  Pierre Legendre,et al.  DISTANCE‐BASED REDUNDANCY ANALYSIS: TESTING MULTISPECIES RESPONSES IN MULTIFACTORIAL ECOLOGICAL EXPERIMENTS , 1999 .

[109]  R. Pierce,et al.  Exploitation of Northern Pike in Seven Small North‐Central Minnesota Lakes , 1995 .

[110]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

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

[112]  D. Post,et al.  The ecological importance of intraspecific variation , 2017, Nature Ecology & Evolution.

[113]  P. Larsson,et al.  Causes and consequences of repeatability, flexibility and individual fine-tuning of migratory timing in pike. , 2016, The Journal of animal ecology.

[114]  Raymond N. Gorley,et al.  PERMANOVA+ for PRIMER. Guide to software and statistical methods , 2008 .

[115]  M. Pieraccini,et al.  Aquatic Conservation: Marine and Freshwater Ecosystems , 2002 .

[116]  K. Muller.  Seasonal anad'romous migration of the pike (Esox lucius L.) in coastal areas of the northern Bothnian sea , 1986 .

[117]  J. Haigh,et al.  The hitch-hiking effect of a favourable gene. , 1974, Genetical research.

[118]  J. Thoday.  Population Genetics , 1956, Nature.

[119]  Edinburgh Research Explorer Population genetics from 1966 to 2016 , 2022 .