A Darwinian Laboratory of Multiple Contact Zones
Authors: Kerstin Johannesson, Alan Le Moan, Samuel Perini, Carl André
Journal: Trends in Ecology & Evolution (2020)

Barriers to gene flow are best studied where divergent populations are in contact, and studies of single-taxon hybrid zones have generated important knowledge about the nature of reproductive barriers.Marine environments, earlier considered to host unstructured species due to high connectivity, offer multispecies contact zones structured by simple physical gradients (e.g., salinity) ideal for comparative studies of divergence and speciation.Overlapping contact zones offer possibilities for comparison of barriers among species of various taxa, life histories, and demographic backgrounds and to test the role of species-specific traits in the formation and function of barriers.Combining genome scans and demographic modelling, barrier regions in the genome can be located and barrier origin traced. With genetic maps, inversions that affect recombination rate (and hence gene flow) can be identified. Barriers to gene flow between divergent populations result in contact (hybrid) zones. Locations where multiple contact zones overlap can be used in comparative studies asking: what mechanisms maintain barriers; what is the origin of the genetic variation involved; and do differences in life history affect the nature of barriers? In a review of 23 marine species' genetic divergence over a postglacial salinity gradient, many showed steep genetic clines supported by divergent selection and/or temporal or spatial segregation. Contacts were primary or secondary and shaped by ancestral variation sometimes involving inversions. The dispersal potential of species seemed less important in shaping clines. Studies of multispecies contact zones will increase our understanding of speciation, but we need to address the taxonomic bias and focus more on postzygotic isolation. Barriers to gene flow between divergent populations result in contact (hybrid) zones. Locations where multiple contact zones overlap can be used in comparative studies asking: what mechanisms maintain barriers; what is the origin of the genetic variation involved; and do differences in life history affect the nature of barriers? In a review of 23 marine species' genetic divergence over a postglacial salinity gradient, many showed steep genetic clines supported by divergent selection and/or temporal or spatial segregation. Contacts were primary or secondary and shaped by ancestral variation sometimes involving inversions. The dispersal potential of species seemed less important in shaping clines. Studies of multispecies contact zones will increase our understanding of speciation, but we need to address the taxonomic bias and focus more on postzygotic isolation. Contact zones (see Glossary) are laboratories for studies of the nature of barriers to gene flow between divergent populations or taxa [1.Barton N.H. Hewitt G.M. Analysis of hybrid zones.Annu. Rev. Ecol. Syst. 1985; 16: 113-148Crossref Scopus (2048) Google Scholar, 2.Hewitt G.M. Hybrid zones, natural laboratories for evolutionary studies.Trends Ecol. Evol. 1988; 3: 158-167Abstract Full Text PDF PubMed Scopus (612) Google Scholar, 3.Abbot R.J. et al.Genomics of hybridization and its evolutionary consequences.Mol. Ecol. 2016; 25: 2325-2332Crossref PubMed Scopus (112) Google Scholar]. Genome-wide sequencing and genetic maps have powered the identification of candidates for barrier loci and investigations of the genomic landscape shaping divergence and speciation [4.Wolf J.B.W. Ellegren H. Making sense of genomic islands of differentiation in light of speciation.Nat. Rev. Genet. 2017; 18: 87-100Crossref PubMed Scopus (212) Google Scholar]. Divergence is usually considered to evolve either in situ as a result of different selection regimes acting on either side of the contact (primary contact) or after secondary contact of populations that have already accumulated differences by selection and/or drift [5.Bierne N. et al.The coupling hypothesis: why genome scans may fail to map local adaptation genes.Mol. Ecol. 2011; 20: 2044-2072Crossref PubMed Scopus (364) Google Scholar, 6.Bierne N. et al.The geography of introgression in a patchy environment and the thorn in the side of ecological speciation.Curr. Zool. 2013; 59: 72-86Crossref Scopus (97) Google Scholar, 7.Ravinet M. et al.Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.J. Evol. Biol. 2017; 30: 1450-1477Crossref PubMed Scopus (225) Google Scholar, 8.Rougemont Q. Bernatchez L. The demographic history of Atlantic salmon (Salmo salar) across its distribution range reconstructed from approximate Bayesian computations.Evolution. 2018; 72: 1261-1277Crossref PubMed Scopus (41) Google Scholar] (Box 1). In both types of contact, identification of the origin and mechanisms of the genetic barriers are central to our understanding of the evolution and maintenance of the divergence [4.Wolf J.B.W. Ellegren H. Making sense of genomic islands of differentiation in light of speciation.Nat. Rev. Genet. 2017; 18: 87-100Crossref PubMed Scopus (212) Google Scholar,7.Ravinet M. et al.Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.J. Evol. Biol. 2017; 30: 1450-1477Crossref PubMed Scopus (225) Google Scholar,9.Faria R. et al.Evolving inversions.Trends Ecol. Evol. 2019; 34: 239-248Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar]. For example, what are the roles of divergent ecological selection, assortative mating (whether due to spatial, temporal, or behavioural isolation), and postzygotic isolation mechanisms caused by intrinsic genetic incompatibilities or extrinsic selection against hybrids?Box 1Primary and Secondary ContactA contact zone originates in one of two ways: (i) secondary contact is formed between two populations that have diverged by genetic drift or selection during a period of isolation prior to contact; whereas (ii) primary contact is formed in situ when a population expands across an environmental transition under divergent selection and gene flow. Genomic patterns resulting from hybridisation will initially be very different between secondary and primary contact zones [7.Ravinet M. et al.Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.J. Evol. Biol. 2017; 30: 1450-1477Crossref PubMed Scopus (225) Google Scholar], and one such difference is the haplotype structure. Secondary contact will produce an introgression pattern characterised by successively smaller 'pieces' of the original background haplotypes with increasing distance from the contact [87.Leitwein M. et al.Using haplotype information for conservation genomics.Trends Ecol. Evol. 2019; 35: 245-258Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar]. This is because repeated recombination during backcrossing breaks apart large introgressed pieces of genomic material (Figure I, 'young' secondary contact). Primary contact, by contrast, will emerge from a common background and hybridisation will occur between haplotypes sharing a common origin. In both secondary and primary zones, ancestral genetic variation (green and brown loci/alleles in Figure I) are likely to play a key role: in secondary zones, ancient adaptive differences will remain important for divergence after contact, while in primary zones ancient polymorphisms can segregate under divergent selection. Over time, new variation (dark blue and red in Figure I), from new mutations or from outside the zones, will establish under selection and contribute to divergence and barriers. Secondary contact can initially form wherever the two earlier isolated populations happen to meet. However, both neutral and selected genetic clines that form at first contact will move until they become trapped in a density trough and/or at a steep environmental shift [1.Barton N.H. Hewitt G.M. Analysis of hybrid zones.Annu. Rev. Ecol. Syst. 1985; 16: 113-148Crossref Scopus (2048) Google Scholar,5.Bierne N. et al.The coupling hypothesis: why genome scans may fail to map local adaptation genes.Mol. Ecol. 2011; 20: 2044-2072Crossref PubMed Scopus (364) Google Scholar]. Primary hybrid zones will evolve at steep environmental shifts. Positions of secondary and primary zones might overlap sometime after establishment [7.Ravinet M. et al.Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.J. Evol. Biol. 2017; 30: 1450-1477Crossref PubMed Scopus (225) Google Scholar], modelling the demographic history using nonadmixed populations outside the contact zone can, however, help to resolve their origin. Also, primary zones might have components of secondary origin; for instance, if primary contact zones form from standing genetic variation that evolved during earlier periods of isolation [85.Van Belleghem S.M. et al.Evolution at two time frames: polymorphisms from an ancient singular divergence event fuel contemporary parallel evolution.PLoS Genet. 2019; 14e1007796Crossref Scopus (44) Google Scholar]. A contact zone originates in one of two ways: (i) secondary contact is formed between two populations that have diverged by genetic drift or selection during a period of isolation prior to contact; whereas (ii) primary contact is formed in situ when a population expands across an environmental transition under divergent selection and gene flow. Genomic patterns resulting from hybridisation will initially be very different between secondary and primary contact zones [7.Ravinet M. et al.Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.J. Evol. Biol. 2017; 30: 1450-1477Crossref PubMed Scopus (225) Google Scholar], and one such difference is the haplotype structure. Secondary contact will produce an introgression pattern characterised by successively smaller 'pieces' of the original background haplotypes with increasing distance from the contact [87.Leitwein M. et al.Using haplotype information for conservation genomics.Trends Ecol. Evol. 2019; 35: 245-258Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar]. This is because repeated recombination during backcrossing breaks apart large introgressed pieces of genomic material (Figure I, 'young' secondary contact). Primary contact, by contrast, will emerge from a common background and hybridisation will occur between haplotypes sharing a common origin. In both secondary and primary zones, ancestral genetic variation (green and brown loci/alleles in Figure I) are likely to play a key role: in secondary zones, ancient adaptive differences will remain important for divergence after contact, while in primary zones ancient polymorphisms can segregate under divergent selection. Over time, new variation (dark blue and red in Figure I), from new mutations or from outside the zones, will establish under selection and contribute to divergence and barriers. Secondary contact can initially form wherever the two earlier isolated populations happen to meet. However, both neutral and selected genetic clines that form at first contact will move until they become trapped in a density trough and/or at a steep environmental shift [1.Barton N.H. Hewitt G.M. Analysis of hybrid zones.Annu. Rev. Ecol. Syst. 1985; 16: 113-148Crossref Scopus (2048) Google Scholar,5.Bierne N. et al.The coupling hypothesis: why genome scans may fail to map local adaptation genes.Mol. Ecol. 2011; 20: 2044-2072Crossref PubMed Scopus (364) Google Scholar]. Primary hybrid zones will evolve at steep environmental shifts. Positions of secondary and primary zones might overlap sometime after establishment [7.Ravinet M. et al.Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.J. Evol. Biol. 2017; 30: 1450-1477Crossref PubMed Scopus (225) Google Scholar], modelling the demographic history using nonadmixed populations outside the contact zone can, however, help to resolve their origin. Also, primary zones might have components of secondary origin; for instance, if primary contact zones form from standing genetic variation that evolved during earlier periods of isolation [85.Van Belleghem S.M. et al.Evolution at two time frames: polymorphisms from an ancient singular divergence event fuel contemporary parallel evolution.PLoS Genet. 2019; 14e1007796Crossref Scopus (44) Google Scholar]. Studies of single contact zones generate important details of mechanisms involved but give less indication of their quantitative importance. Moreover, single-species studies cannot inform us about the role of traits that are invariable within a species (e.g., many life-history traits, large genomic traits). Studies of multispecies contact zones, where the contacts of different species overlap under the same external conditions, allow assessments of the general importance of different patterns of origin, ancestral variation, and genomic architectures in barrier formation. They also enable us to investigate how life-history traits such as dispersal, generation time, and reproductive biology contribute to gene-flow barriers, and the role of prezygotic and postzygotic isolation mechanisms. Multispecies contact zones (sometimes referred to as 'suture zones') are present in both terrestrial [10.Hewitt G.M. Some genetic consequences of ice ages, and their role in divergence and speciation.Biol. J. Linn. Soc. 1996; 58: 247-276Crossref Google Scholar,11.Swenson N.G. Howard D.J. Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America.Am. Nat. 2005; 166: 581-591Crossref PubMed Scopus (312) Google Scholar] and marine [5.Bierne N. et al.The coupling hypothesis: why genome scans may fail to map local adaptation genes.Mol. Ecol. 2011; 20: 2044-2072Crossref PubMed Scopus (364) Google Scholar,12.Johannesson K. André C. Life on the margin - genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea.Mol. Ecol. 2006; 15: 2013-2029Crossref PubMed Scopus (289) Google Scholar, 13.Patarnello T. et al.Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break?.Mol. Ecol. 2007; 16: 4426-4444Crossref PubMed Scopus (424) Google Scholar, 14.DiBattista J.D. et al.When biogeographical provinces collide: hybridization of reef fishes at the crossroads of marine biogeographical provinces in the Arabian Sea.J. Biogeogr. 2015; 42: 1601-1614Crossref Scopus (52) Google Scholar, 15.Ding S. et al.Characterization of hybridization within a secondary contact region of the inshore fish, Bostrychus sinensis, in the East China Sea.Heredity. 2017; 120: 51-62Crossref PubMed Scopus (10) Google Scholar, 16.Stanley R. et al.A climate-associated multispecies cryptic cline in the northwest Atlantic.Sci. Adv. 2018; 4eaaq0929Crossref PubMed Scopus (50) Google Scholar, 17.El Ayari T. et al.The hidden side of a major marine biogeographic boundary: a wide mosaic hybrid zone at the Atlantic–Mediterranean divide reveals the complex interaction between natural and genetic barriers in mussels.Heredity. 2019; 122: 770-784Crossref PubMed Scopus (17) Google Scholar] environments. Compiling recent data from a marine multispecies contact zone at the entrance of the Baltic Sea, we here highlight questions that a comparative approach of such zones can address, to support an increased understanding of the mechanisms involved in divergence and speciation. The transition zone between the marine North Sea (North-East Atlantic) and the brackish Baltic Sea is shaped by a salinity gradient with its steepest part in the Danish Straits (Figure 1, Key Figure). Importantly, low salinity imposes strong physiological stress on most marine organisms and so this gradient impacts heavily on the distribution and adaptation of marine species in this area. After its formation 8000 years ago by the opening of a postglacial freshwater lake into the Atlantic, the Baltic Sea was subsequently colonised by a subset of the marine species living in the North Sea. A few of these established populations along the entire environmental gradient while the majority colonised only the outer part of the gradient [18.Ojaveer H. et al.Status of biodiversity in the Baltic Sea.PLoS One. 2010; 5e12467Crossref PubMed Scopus (207) Google Scholar]. Many of the marine species established in the Baltic Sea show strong plasticity in phenotypic traits [19.Kautsky N. et al.Genotypic and phenotypic differences between Baltic and North Sea populations of Mytilus edulis evaluated through reciprocal transplantations. 1. Growth and morphology.Mar. Ecol. Prog. Ser. 1990; 59: 203-210Crossref Google Scholar, 20.Wood H.L. et al.Physiological plasticity is key to the presence of the isopod Idotea baltica (Pallas) in the Baltic Sea.J. Sea Res. 2014; 85: 255-262Crossref Scopus (9) Google Scholar, 21.Renborg E. et al.Variable salinity tolerance in ascidian larvae is primarily a plastic response to the parental environment.Evol. Ecol. 2014; 28: 561-572Crossref Scopus (21) Google Scholar, 22.Johansson D. et al.Reciprocal transplants support a plasticity-first scenario during colonisation of a large hyposaline basin by a marine macro alga.BMC Ecol. 2017; 1714Crossref PubMed Scopus (11) Google Scholar]; in addition, early genetic studies had already shown examples of strong genetic clines over the salinity gradient [23.Sick K. Haemoglobin polymorphism in fishes.Nature. 1961; 192: 894-896Crossref PubMed Scopus (93) Google Scholar,24.Christiansen F.B. Frydenberg O. Geographical patterns of four polymorphisms in Zoarces viviparus as evidence of selection.Genetics. 1974; 77: 765-770PubMed Google Scholar]. We scanned published studies describing genetic variation in species present over the North Sea–Baltic Sea transition and retrieved useful data for 23 species. These species represent a wide range of taxa (15 fish, five invertebrates, two macroalgae, and one microalga) and a wide range of life histories (Table 1). With only one exception, the recently invaded bay barnacle (Balanus improvisus) [25.Wrange A.L. et al.The story of a hitchhiker: population genetic patterns in the invasive barnacle Balanus (Amphibalanus) improvisus Darwin 1854.PLoS One. 2016; 11e0147082Crossref PubMed Scopus (16) Google Scholar], all species show genetic differentiation over the transition zone. In most species, the separation is between a Baltic Sea and a North Sea population, while in European flounder (Platichthys spp.) there is an additional subdivision inside the Baltic Sea (Figure 1). Importantly, all species form contact zones between divergent populations. Original descriptions indicated that 16 of 22 contact zones roughly overlapped (Figure 1), and after fitting clines to the species with enough data (14 species) this shows that the overlap coincides with the steepest part of the salinity gradient, although some clines are slightly shifted towards lower salinities (Figure 2). In 12 species, the available data allowed a more formal analysis of the presence of genetic clines. This test supports stepped or segmented clines in ten species, while in the isopod Idotea baltica and the Baltic clam [Limecola (Macoma) balthica] divergence tends to be linear rather than stepped (Table 1).Table 1Species with Available Genetic Data from Transect Samples Covering the North Sea–Baltic Sea TransitionSpeciesCommon nameDispersal potentiala'High' denotes several week-long pelagic larvae and/or highly mobile adults giving the species a potential for high gene flow. 'Low' denotes a short pelagic larval (or zygote/spore) stage and sessile or less mobile adults.Genetic databFigure denotes number of SNPs if not specified.FST over zoneOutlier distributionSelection agencyFitted cline modelcThe change in genetic divergence over the salinity gradient was analysed for each taxon separately using three different models, which were then compared with the Akaike information criterion (AIC): a linear model, a stepped cline model [84], and a regression model with segmented relationships (R package 'segmented' [105]), compatible with isolation by distance, stepped clines shaped by one contact, and complex clines shaped by more than one contact, respectively.Type of zoneInferred fromBarrier strength; mechanismdSuggested mechanisms that are not experimentally confirmed are followed by '?'. Note that other mechanisms, not yet investigated, might add to barriers.RefsGadus morhuaAtlantic codHigh1.2 million0.040Three large inversionsSalinity, temperatureToo few dataSecondaryPhylogenyStrong; separate spawning times, local adaptation[42.Berg P.R. et al.Adaptation to low salinity promotes genomic divergence in Atlantic cod (Gadus morhua L.).Genome Biol. Evol. 2015; 7: 1644-1663Crossref PubMed Scopus (111) Google Scholar, 43.Fairweather R. et al.Range-wide genomic data synthesis reveals Transatlantic vicariance and secondary contact in Atlantic cod.Ecol. Evol. 2018; 8: 12140-12152Crossref PubMed Scopus (4) Google Scholar, 44.Weist P. et al.Assessing SNP-markers to study population mixing and ecological adaptation in Baltic cod.PLoS One. 2019; 14e0218127Crossref PubMed Scopus (17) Google Scholar, 45.Nissling A. Westin L. Salinity requirements for successful spawning of Baltic and Belt Sea cod and the potential for cod stock interactions in the Baltic Sea.Mar. Ecol. Prog. Ser. 1997; 152: 261-271Crossref Scopus (108) Google Scholar, 46.Barth J.M.I. et al.Genome architecture enables local adaptation of Atlantic cod despite high connectivity.Mol. Ecol. 2017; 26: 4452-4466Crossref PubMed Scopus (75) Google Scholar, 47.Barth J.M.I. et al.Disentangling structural genomic and behavioral barriers in a sea of connectivity.Mol. Ecol. 2019; 28: 1394-1411Crossref PubMed Scopus (37) Google Scholar, 48.Kirubakaran T.G. et al.Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod.Mol. Ecol. 2016; 25: 2130-2143Crossref PubMed Scopus (109) Google Scholar,69.Andersen O. et al.Haemoglobin polymorphisms affect the oxygen binding properties in Atlantic cod populations.Proc. Biol. Sci. 2009; 276: 833-841Crossref PubMed Scopus (71) Google Scholar]Clupea harengusAtlantic herringHigh6 million0.030Haplotype blocks, one large inversionSalinity, temperatureStepped or segmented clinePrimaryDemographyWeak; local adaptation?[38.Martinez Barrio A. et al.The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing.Elife. 2016; 5e12081Crossref PubMed Scopus (99) Google Scholar,56.Pettersson M.E. et al.A chromosome-level assembly of the Atlantic herring – detection of a supergene and other signals of selection.Genome Res. 2019; 29: 1919-1928Crossref PubMed Scopus (38) Google Scholar,90.Berg F. et al.Genetic factors have a major effect on growth, number of vertebrae and otolith shape in Atlantic herring (Clupea harengus).PLoS One. 2018; 13e0190995Crossref PubMed Scopus (30) Google Scholar]Platichthys flesusEuropean flounderHigh54720.005Few and scatteredSalinity, temperatureSegmented clineSecondaryDemographyWeak; local adaptation?[39.Le Moan A. et al.Beyond parallel evolution: when several species colonize the same environmental gradient.bioRxiv. 2019; (Published online June 6, 2019. https://doi.org/10.1101/662569)Google Scholar,73.Hemmer-Hansen J. et al.Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.).Heredity. 2007; 99: 592-600Crossref PubMed Scopus (130) Google Scholar]P. flesus/Platichthys solemdaliBaltic flounderLow20510.025SalinityToo few dataSecondaryDemographyStrong; separate spawning habitats, local adaptation[51.Momigliano P. et al.Extraordinarily rapid speciation in a marine fish.Proc. Natl. Acad. Sci. U. S. A. 2017; 114: 6074-6079Crossref PubMed Scopus (64) Google Scholar,52.Momigliano P. et al.Platichthys solemdali sp. nov. (Actinopterygii, Pleuronectiformes): a new flounder species from the Baltic Sea.Front. Mar. Sci. 2018; 5: 225Crossref Scopus (22) Google Scholar]Scophthalmus maximusTurbotHigh33480.012Many scatteredSalinityStepped clinePrimaryDemographyModerate; unknown[31.Momigliano P. et al.Biases in demographic modelling affect our understanding of the process of speciation.bioRxiv. 2020; (Published online June 5, 2020. https://doi.org/10.1101/2020.06.03.128298)Google Scholar]Pleuronectus platessaEuropean plaiceHigh66850.013Two inversionsSalinityToo few dataPrimaryDemographyWeak; unknown[39.Le Moan A. et al.Beyond parallel evolution: when several species colonize the same environmental gradient.bioRxiv. 2019; (Published online June 6, 2019. https://doi.org/10.1101/662569)Google Scholar]Limanda limandaCommon dabHigh34680.008ClusteredSalinityStepped clineSecondaryDemographyWeak; unknown[39.Le Moan A. et al.Beyond parallel evolution: when several species colonize the same environmental gradient.bioRxiv. 2019; (Published online June 6, 2019. https://doi.org/10.1101/662569)Google Scholar]Solea soleaCommon soleHigh37140.003Very fewToo few dataPrimaryDemographyVery weak; unknown[40.Diopere E. et al.Seascape genetics of a flatfish reveals local selection under high levels of gene flow.ICES J. Mar. Sci. 2018; 75: 675-689Crossref Scopus (32) Google Scholar,41.Le Moan A. et al.Fine scale population structure linked to neutral divergence in the common sole (Solea solea), a marine fish with high dispersal capacity.bioRxiv. 2019; (Published online June 6, 2019. https://doi.org/10.1101/662619)Google Scholar]Ammodytes tobianusSmall sandeelHigh40390.041Salinity, temperatureSegmented clineStrong; separate spawning times?[91.Christensen A. et al.Sandeel (Ammodytes marinus) larval transport patterns in the North Sea from an individual-based hydrodynamic egg and larval model.Can. J. Fish. Aquat. Sci. 2008; 65: 1498-1511Crossref Scopus (41) Google Scholar,92.Fietz K. et al.Mind the gut: genomic insights to population divergence and gut microbial composition of two marine keystone species.Microbiome. 2018; 682Crossref PubMed Scopus (17) Google Scholar]Hyperoplus lanceolatusGreater sandeelHigh43280.039Salinity, temperatureStepped clineStrong; separate spawning times?[92.Fietz K. et al.Mind the gut: genomic insights to population divergence and gut microbial composition of two marine keystone species.Microbiome. 2018; 682Crossref PubMed Scopus (17) Google Scholar,93.Lynam C.P. et al.Spatial patterns and trends in abundance of larval sandeels in the North Sea: 1950–2005.ICES J. Mar. Sci. 2013; 70: 540-553Crossref Scopus (18) Google Scholar]Symphodus melopsCorkwing wrasseLow50 1300.120Only two spurious outliersStepped or segmented clineSecondaryDemographyStrong; density trough[49.Mattingsdal M. et al.Demographic history, not adaptation, has shaped the strongly differentiated corkwing wrasse populations in Northern Europe.Mol. Ecol. 2020; 29: 160-171Crossref PubMed Scopus (11) Google Scholar]Labrus bergyltaBallan wrasseLow820.027Stepped clineModerate; density trough[50.Seljestad G.W. et al.A cleaner break: genetic divergence between geographic groups and sympatric phenotypes revealed in ballan wrasse (Labrus bergylta).Ecol. Evol. 2020; 10: 6120-6135Crossref PubMed Scopus (6) Google Scholar]Pomatoschistus minutusSandgobyLow22 1900.020DistributedSalinity, turbidityToo few dataSecondaryDemographyModerate; local adaptation[94.Larmuseau M.H.D. et al.To see in different seas: spatial variation in the rhodopsin gene of the sand goby (Pomatoschistus minutus).Mol. Ecol. 2009; 18: 4227-4239Crossref PubMed Scopus (47) Google Scholar,95.Leder E.H. et al.Postglacial establishment of locally adapted fish populations over a steep salinity gradient.J. Evol. Biol. 2020; (Published online June 23, 2020. https://doi.org/10.1111/jeb.13668)Crossref PubMed Scopus (10) Google Scholar]Gasterosterus aculeatusThree-spined sticklebackLow30 0000.015Enriched in regionsSalinity, temperatureToo few dataPrimaryDemographyModerate; local adaptation[67.DeFaveri J. Merilä J. Local adaptation to salinity in the three-spined stickleback?.J. Evol. Biol. 2013; 27: 290-302Crossref PubMed Scopus (47) Google Scholar,96.Guo B. et al.Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks.BMC Biol. 2015; 1319Crossref PubMed Scopus (83) Google Scholar]Salmo salarAtlantic salmonHigh50340.132Too few dataSecondaryDemographyStrong; separate spawning areas[8.Rougemont Q. Bernatchez L. The demographic history of Atlantic salmon (Salmo salar) across its distribution range reconstructed from approximate Bayesian computations.Evolution. 2018; 72: 1261-1277Crossref PubMed Scopus (41) Google Scholar,97.Nilsson J. et al.Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area.Mol. Ecol. 2001; 10: 89-102Crossref PubMed Scopus (128) Google Scholar]Ciona intestinalisVase tunicateLow16530.180SalinityVertical cline (no test)SecondaryDemographyStrong; partly separate spawning times, local adaptation[53.Dybern B.I. The distribution and salinity tolerance of Ciona intestinalis (L.) f. typica with special reference to the waters around southern Scandinavia.Ophelia. 1967; 4: 207-226Crossref Scopus (40) Google Scholar,55.Hudson J. et al.Secondary contacts and genetic admixture between divergent genotypes shape colonisation by an amphiatlantic epibenthic invertebrate.Evol. Appl. 2020; 13: 600-612Crossref PubMed Scopus (12) Google Scholar]Idotea baltica'Isopod'Low33 7740.024SalinityLinear clineWeak; unknown[98.De Wit P. et al.Spatial genetic structure in a crustacean herbivore highlights the need for local considerations in Baltic Sea biodiversity management.Evol. Appl. 2020; 13: 974-990Crossref PubMed Scopus (8) Google Scholar]Balanus improvisusBay barnacleHighmtDNA, four microsatellites0.011No outliersNo clineNo barriers[25.Wrange A.L. et al.The story of a hitchhiker: population genetic patterns in the invasive barnacle Balanus (Amphibalanus) improvisus Darwin 1854.PLoS One. 2016; 11e0147082Crossref PubMed Scopus (16) Google Scholar,99.Wrange A.L. et al.