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Geographical isolation, habitat variation and trophic specialization have contributed to a large extent to the astonishing diversity of cichlid fishes in the Great East African lakes. Because parasite communities often vary across space and environments, parasites can accompany and potentially enhance cichlid species diversification. However, host dispersal may reduce opportunities for parasite-driven evolution by homogenizing parasite communities and allele frequencies of immunity genes. To test for the relationships between parasite community variation, host dispersal and parasite-induced host evolution, we studied two sympatric cichlid species with contrasting dispersal capacities along the shores of southern Lake Tanganyika. Whereas the philopatric Tropheus moorii evolved into several genetically differentiated colour morphs, Simochromis diagramma is phenotypically rather uniform across its distribution range and shows only weak population structure. Populations of both species were infected with divergent parasite communities and harbour differentiated variant pools of an important set of immune genes, the major histocompatibility complex (MHC). The overall extent of geographical variation of parasites and MHC genes was similar between host species. This indicates that immunogenetic divergence among populations of Lake Tanganyika cichlids can occur even in species that are strongly dispersing. However, because this also includes species that are phenotypically uniform, parasite-induced evolution may not represent a key factor underlying species diversification in this system., (© 2016 John Wiley & Sons Ltd.)

Unravelling the factors shaping the genetic structure of mobile marine species is challenging due to the high potential for gene flow. However, genetic inference can be greatly enhanced by increasing the genomic, geographical or environmental resolution of population genetic studies. Here, we investigated the population structure of turbot (Scophthalmus maximus) by screening 17 random and gene-linked markers in 999 individuals at 290 geographical locations throughout the northeast Atlantic Ocean. A seascape genetics approach with the inclusion of high-resolution oceanographical data was used to quantify the association of genetic variation with spatial, temporal and environmental parameters. Neutral loci identified three subgroups: an Atlantic group, a Baltic Sea group and one on the Irish Shelf. The inclusion of loci putatively under selection suggested an additional break in the North Sea, subdividing southern from northern Atlantic individuals. Environmental and spatial seascape variables correlated marginally with neutral genetic variation, but explained significant proportions (respectively, 8.7% and 10.3%) of adaptive genetic variation. Environmental variables associated with outlier allele frequencies included salinity, temperature, bottom shear stress, dissolved oxygen concentration and depth of the pycnocline. Furthermore, levels of explained adaptive genetic variation differed markedly between basins (3% vs. 12% in the North and Baltic Sea, respectively). We suggest that stable environmental selection pressure contributes to relatively strong local adaptation in the Baltic Sea. Our seascape genetic approach using a large number of sampling locations and associated oceanographical data proved useful for the identification of population units as the basis of management decisions., (© 2013 John Wiley & Sons Ltd.)

Genes with major phenotypic effects facilitate quantifying the contribution of genetic vs. plastic effects to adaptive divergence. A classical example is Ectodysplasin (Eda), the major gene controlling lateral plate phenotype in three-spined stickleback. Completely plated marine stickleback populations evolved repeatedly towards low-plated freshwater populations, representing a prime example of parallel evolution by natural selection. However, many populations remain polymorphic for lateral plate number. Possible explanations for this polymorphism include relaxation of selection, disruptive selection or a balance between divergent selection and gene flow. We investigated 15 polymorphic stickleback populations from brackish and freshwater habitats in coastal North-western Europe. At each site, we tracked changes in allele frequency at the Eda gene between subadults in fall, adults in spring and juveniles in summer. Eda genotypes were also compared for body size and reproductive investment. We observed a fitness advantage for the Eda allele for the low morph in freshwater and for the allele for the complete morph in brackish water. Despite these results, the differentiation at the Eda gene was poorly correlated with habitat characteristics. Neutral population structure was the best predictor of spatial variation in lateral plate number, suggestive of a substantial effect of gene flow. A meta-analysis revealed that the signature of selection at Eda was weak compared to similar studies in stickleback. We conclude that a balance between divergent selection and gene flow can maintain stickleback populations polymorphic for lateral plate number and that ecologically relevant genes may not always contribute much to local adaptation, even when targeted by selection., (© 2013 John Wiley & Sons Ltd.)

Quantifying the contribution of the various processes that influence population genetic structure is important, but difficult. One of the reasons is that no single measure appropriately quantifies all aspects of genetic structure. An increasing number of studies is analysing population structure using the statistic D, which measures genetic differentiation, next to G(ST) , which quantifies the standardized variance in allele frequencies among populations. Few studies have evaluated which statistic is most appropriate in particular situations. In this study, we evaluated which index is more suitable in quantifying postglacial divergence between three-spined stickleback (Gasterosteus aculeatus) populations from Western Europe. Population structure on this short timescale (10 000 generations) is probably shaped by colonization history, followed by migration and drift. Using microsatellite markers and anticipating that D and G(ST) might have different capacities to reveal these processes, we evaluated population structure at two levels: (i) between lowland and upland populations, aiming to infer historical processes; and (ii) among upland populations, aiming to quantify contemporary processes. In the first case, only D revealed clear clusters of populations, putatively indicative of population ancestry. In the second case, only G(ST) was indicative for the balance between migration and drift. Simulations of colonization and subsequent divergence in a hierarchical stepping stone model confirmed this discrepancy, which becomes particularly strong for markers with moderate to high mutation rates. We conclude that on short timescales, and across strong clines in population size and connectivity, D is useful to infer colonization history, whereas G(ST) is sensitive to more recent demographic events., (© 2012 Blackwell Publishing Ltd.)

Heavy fishing and other anthropogenic influences can have profound impact on a species' resilience to harvesting. Besides the decrease in the census and effective population size, strong declines in mature adults and recruiting individuals may lead to almost irreversible genetic changes in life-history traits. Here, we investigated the evolution of genetic diversity and effective population size in the heavily exploited sole (Solea solea), through the analysis of historical DNA from a collection of 1379 sole otoliths dating back from 1957. Despite documented shifts in life-history traits, neutral genetic diversity inferred from 11 microsatellite markers showed a remarkable stability over a period of 50 years of heavy fishing. Using simulations and corrections for fisheries induced demographic variation, both single-sample estimates and temporal estimates of effective population size (N(e) ) were always higher than 1000, suggesting that despite the severe census size decrease over a 50-year period of harvesting, genetic drift is probably not strong enough to significantly decrease the neutral diversity of this species in the North Sea. However, the inferred ratio of effective population size to the census size (N(e) /N(c) ) appears very small (10(-5) ), suggesting that overall only a low proportion of adults contribute to the next generation. The high N(e) level together with the low N(e) /N(c) ratio is probably caused by a combination of an equalized reproductive output of younger cohorts, a decrease in generation time and a large variance in reproductive success typical for marine species. Because strong evolutionary changes in age and size at first maturation have been observed for sole, changes in adaptive genetic variation should be further monitored to detect the evolutionary consequences of human-induced selection., (© 2011 Blackwell Publishing Ltd.)

An excellent model to elucidate the mechanisms and importance of evolution in the marine environment is the spectral tuning mechanism of the visual pigment in vertebrates. In the sand goby Pomatoschistus minutus (Teleostei; Gobiidae), a distribution-wide study showed that spatial variation at the rhodopsin gene (RH1) matches the characteristics of specific light environments. This match suggests that populations are locally adapted to selective light regimes targeting the RH1 gene. If so, then the direction of selection should depend on the regional spatial and temporal stability of the light conditions. We tested this prediction by comparing goby populations from two regions: the Baltic Sea, characterized by divergent, but temporally stable light conditions, and the North Sea, characterized by locally heterogeneous and temporally variable light conditions. RH1 sequences of 491 Pomatoschistus minutus individuals from 15 locations were analysed. We found that variation at the RH1 gene in the Baltic populations showed signatures of diversifying selection, whereas the RH1 gene in the North Sea showed signatures of stabilizing selection. These different modes of selection are consistent with the regional light conditions and hence support our predictions, but may also be influenced by migration between the open sea and more turbid estuarine environments. An interesting observation is that within one gene, synonymous and non-synonymous SNPs show a totally different pattern between populations. Population differentiation based on non-synonymous SNPs of the RH1 gene correlated with spectral variation of the local environment of the sand goby populations. In contrast, the differentiation based on synonymous SNPs of RH1 reflects more the neutral historical pattern of the species.

Aquatic organisms living in a range of photic environments require specific mechanisms to tune their visual pigments. Maximum absorbance (lambda(max)) of retinal rods in populations of the marine demersal sand goby, (Pomatoschistus minutus; Gobiidae, Teleostei) correlates with the local optic environment. It has been shown that this is not regulated through a physiological response by exchanging the rhodopsin chromophore. To test for evolutionary adaptation, the sequence of the rhodopsin (RH1) gene was analysed in 165 Pomatoschistus minutus individuals from seven populations across its distribution range. Analysis showed a high level of intraspecific polymorphism at the RH1 gene, including nonsynonymous mutations on amino acids, known as spectral tuning sites. Population differentiation at these sites was in agreement with the observed differentiation in lambda(max) values. Analyses of d(N)/d(S) substitution rate ratios and likelihood ratio tests under site-specific models detected a significant signal of positive Darwinian selection on the RH1 gene. A strong discrepancy in differentiation was noticed between RH1 gene variation and the presumably neutral microsatellites and mitochondrial data. Samples did not cluster according to geographical or historical proximity with regards to RH1, but according to the general photic conditions of the habitat environment of the sand goby. This study highlights the usefulness of sensory genes, like rhodopsin, for studying the characteristics of local adaptation in marine nonmodel organisms.

In Belgium, the Pelophylax esculentus complex has recently been subjected to multiple introductions of non-native water frogs, increasing the occurrence of hybridisation events. In the present study, we tested the reliability of morphometric and recently developed microsatellite tools to identify introgression and to determine the origin of exotic Belgian water frogs. By analysing 150 individuals of each taxon of the P. esculentus complex and an additional 60 specimens of the introduced P. cf. bedriagae, we show that neither of the currently available tools appears to have sufficient power to reliably distinguish all Belgian water frog species. We therefore aimed at increasing the discriminatory power of a microsatellite identification tool by developing a new marker panel with additional microsatellite loci. By adding only two new microsatellite loci (RlCA5 and RlCA1b20), all taxa of the P. esculentus complex could be distinguished from each other with high confidence. Three more loci (Res3, Res5 and Res17) provided a powerful discrimination of the exotic species.

In Western Europe, many pond owners introduce amphibians for ornamental purposes. Although indigenous amphibians are legally protected in most European countries, retailers are circumventing national and international legislation by selling exotic nonprotected sibling species. We investigated to what extent non-native species of the European water frog complex (genus Pelophylax) have become established in Belgium, using morphological, mitochondrial and nuclear genetic markers. A survey of 87 sampling sites showed the presence of non-native water frogs at 47 locations, mostly Marsh frogs (Pelophylax ridibundus). Surprisingly, at least 19% of all these locations also harboured individuals with mitochondrial haplotypes characteristic of Anatolian water frogs (Pelophylax cf. bedriagae). Nuclear genotyping indicated widespread hybridization and introgression between P. ridibundus and P. cf. bedriagae. In addition, water frogs of Turkish origin obtained through a licensed retailer, also contained P. ridibundus and P. cf. bedriagae, with identical haplotypes to the wild Belgian populations. Although P. ridibundus might have invaded Belgium by natural range expansion from neighbouring countries, our results suggest that its invasion was at least partly enhanced by commercial trade, with origins as far as the Middle East. Also the invasion and rapid spread of Anatolian lineages, masked by their high morphological similarity to P. ridibundus, is likely the result of unregulated commercial trade. We expect that Anatolian frogs will further invade the exotic as well as the native range of P. ridibundus and other Pelophylax species elsewhere in Western and Central Europe, with risks of large-scale hybridization and introgression.

The geological history of the Mediterranean Sea, its hydrography and connection with the Atlantic Ocean have been well documented. Despite a wealth of historical and oceanographic data, the Atlantic-Mediterranean transition remains controversial at the biological level as there are discordant results regarding the biogeographical separation between the Atlantic and Mediterranean biota. The opening of the Strait of Gibraltar at the end of the Messinian Salinity Crisis (some 5.33 million years ago), removed the land barrier that impeded the marine biota allowing it to disperse freely into the Mediterranean Sea. However, present day genetic patterns suggest a limitation to gene flow for some marine species, preventing population admixture. In the last few years, a large number of studies have challenged the hypothesis of the Strait of Gibraltar representing a phylogeographical break. A review of more than 70 papers reveals no obvious relationship between either dispersal ability or life history, and observed patterns of partial or complete genetic isolation between Atlantic and Mediterranean populations. We re-analysed a selection of this large body of data (20 studies in total) in order to provide a homogeneous and coherent view on the generality of the phylogeographical patterns and the presence of a phylogeographical barrier. This offered the opportunity to summarize the state of the art on this matter and reach some general conclusions on the evolutionary history across the Atlantic-Mediterranean range. Geographically, some species in the transition zone showed step changes of allele frequencies associated with the Almeria-Oran Front rather than with the Strait of Gibraltar itself. A major part of the data describe evolutionary events well within the time frame of the Quaternary age as very few taxa pre-date closure of the Tethys Sea. Results point to a combined signature of vicariance, palaeoclimate fluctuation and life-history traits on the Atlantic-Mediterranean phylogeographical patterns. Principal component analysis failed to show any particular association between biological traits and genetic variables. It would argue that organismal determinism may play a far less significant role than marine biogeographers have generally believed.

Three measures of divergence, estimated at nine putatively neutral microsatellite markers, 14 quantitative traits, and seven quantitative trait loci (QTL) were compared in eight populations of the three-spined stickleback (Gasterosteus aculeatus L.) living in the Scheldt river basin (Belgium). Lowland estuarine and polder populations were polymorphic for the number of lateral plates, whereas upland freshwater populations were low-plated. The number of short gill rakers and the length of dorsal and pelvic spines gradually declined along a coastal-inland gradient. Plate number, short gill rakers and spine length showed moderate to strong signals of divergent selection between lowland and upland populations in comparison between P(ST) (a phenotypic alternative for Q(ST)) and neutral F(ST). However, such comparisons rely on the unrealistic assumption that phenotypic variance equals additive genetic variance, and that nonadditive genetic effects and environmental effects can be minimized. In order to verify this assumption and to confirm the phenotypic signals of divergence, we tested for divergent selection at the underlying QTL. For plate number, strong genetic evidence for divergent selection between lowland and upland populations was obtained based on an intron marker of the Eda gene, of which the genotype was highly congruent with plate morph. Genetic evidence for divergent selection on short gill rakers was limited to some population pairs where F(ST) at only one of two QTL was detected as an outlier, although F(ST) at both loci correlated significantly with P(ST). No genetic confirmation was obtained for divergent selection on dorsal spine length, as no outlier F(ST)s were detected at dorsal spine QTL, and no significant correlations with P(ST) were observed.

Life history traits of highly vagile marine species, such as adult reproductive success and larval dispersal, are strongly determined by oceanographic and climatic forces. Nevertheless, marine organisms may show restricted dispersal in time and space. Patterns of isolation by distance (IBD) have been repeatedly observed in marine species. If spawning time is a function of geographical location, temporal and spatial isolation, can easily be confounded or misinterpreted. In this study, we aimed at discriminating between various forces shaping the genetic composition of recruiting juveniles of the European eel (Anguilla anguilla L.). By controlling for geographical variation, we assessed temporal variation and tested for possible isolation by time (IBT) between recruitment waves within and between years. Using 12 polymorphic allozyme and six variable microsatellite loci, we show that genetic differentiation was low (F(ST) = 0.01-0.002) and significant between temporal samples. Regression analysis between genetic and temporal distance, was consistent with a subtle interannual pattern of IBT. Our data suggest that the population dynamics of the European eel may be governed by a double pattern of temporal variance in genetic composition: (i) a broad-scale IBT of spawning cohorts, possibly as a consequence of the large migration loop in anguillids and strong variance in annual adult reproductive contribution; and (ii) a smaller-scale variance in reproductive success (genetic patchiness) within cohorts among seasonally separated spawning groups, most likely originating from fluctuating oceanic and climatic forces. The consistency of both mechanisms remains to be verified with fine-scale analyses of both spawning/migrating aged adults and their offspring to confirm the stochastic/deterministic nature of the IBT pattern in eel.

Climatic oscillations during the Pleistocene epoch had a dramatic impact on the distribution of biota in the northern hemisphere. In order to trace glacial refugia and postglacial colonization routes on a global scale, we studied mitochondrial DNA sequence variation in a freshwater fish (burbot, Lota lota; Teleostei, Gadidae) with a circumpolar distribution. The subdivision of burbot in the subspecies Lota lota lota (Eurasia and Alaska) and Lota lota maculosa (North America, south of the Great Slave Lake) was reflected in two distinct mitochondrial lineages (average genetic distance is 2.08%). The lota form was characterized by 30 closely related haplotypes and a large part of its range (from Central Europe to Beringia) was characterized by two widespread ancestral haplotypes, implying that transcontinental exchange/migration was possible for cold-adapted freshwater taxa in recent evolutionary time. However, the derived mitochondrial variants observed in peripheral populations point to a recent separation from the core group and postglacial recolonization from distinct refugia. Beringia served as refuge from where L. l. lota dispersed southward into North America after the last glacial maximum. Genetic variation in the maculosa form consisted of three mitochondrial clades, which were linked to at least three southern refugia in North America. Two mitochondrial clades east of the Continental Divide (Mississippian and Missourian clades) had a distinct geographical distribution in the southern refuge zones but intergraded in the previously glaciated area. The third clade (Pacific) was exclusively found west of the Continental Divide.

The anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system allows for inferring the role of adaptation in speciation with a high level of accuracy because the freshwater ecotype has evolved multiple times from a uniform anadromous ancestor. A cause for concern is that independent evolution among drainages is not guaranteed in areas with a poorly resolved glacial history. This is the case for the west European great rivers, whose downstream valleys flanked the southern limit of the late Pleistocene ice sheet. We tested for independent and postglacial colonization of these valleys hypothesizing that the relationships among anadromous and freshwater sticklebacks correspond to a raceme structure. We compared the reduction in plate number accompanying this colonization to the genetic differentiation using 13 allozyme and five microsatellite loci in 350 individuals. Overall microsatellite differentiation (F(ST) = 0.147) was twice as large as allozyme differentiation (F(ST) = 0.066). Although habitat-specific gene flow may mask the ancestral relationships among both ecotypes, levels of microsatellite differentiation supported the hypothesis of raceme-like divergence, reflecting independent colonizations rather than the presence of two distinct evolutionary clades. Under an infinite alleles model and in the absence of gene flow, the observed freshwater divergence might be reached after 440 (microsatellites) to 4500 (allozymes) generations. Hence, the anadromous-freshwater stickleback system most likely diverged postglacially. We conclude that the reduction in plate number in two freshwater basins probably occurred independently, and that its considerable variation among populations is not in agreement with the time since divergence.

The phylogeographical patterns of a small marine fish, the common goby, Pomatoschistus microps, were assessed at 12 sites along the northeastern Atlantic coasts and the western Mediterranean Sea. A combination of two genetic markers was employed: cellulose acetate allozyme electrophoresis (CAGE) and sequence analysis of a 289 bp fragment of the mitochondrial locus cytochrome b. Both markers were congruent in revealing significant differences between samples (global FST = 0.247 for the allozymes and PhiST = 0.437 for the mitochondrial DNA data) and a pattern of isolation-by-distance. Phylogeographical analyses yielded a shallow branching structure with four groups. Three of those were confined to the Atlantic basin and showed a star-like pattern. The fourth group contained a central haplotype occurring at the edges of the species' distribution, accompanied by a few more rare variants, which were restricted to the Mediterranean Sea. A genetic break was observed around the British Isles, with distinct haplotypes dominating at either side of the English Channel. A significantly negative correlation between the degree of genetic diversity and latitude was recorded both for mitochondrial DNA (mtDNA) and allozymes in the Atlantic basin. Gene flow analysis suggested that recolonization of the North Sea and the coasts of western Scotland and Ireland may have taken place from a glacial refugium in the Southern Bight of the North Sea. These results are discussed in the perspective of possible postglacial migration routes of marine fish along the northeastern Atlantic coasts.

The distribution of genetic diversity at 10 highly polymorphic microsatellite loci within the European freshwater fish, Cottus gobio, L. was examined. The sampling range comprised a large geographical scale including lineages known to be highly divergent at both mitochondrial DNA (mtDNA) and allozymes. An analysis of genetic variability within populations showed that expected heterozygosity and allelic richness could be explained largely by current effective population sizes. Evidence was found, however, that historical processes predating the last major glaciation affected allelic richness. In addition to confirming the large-scale patterns from earlier studies, the microsatellite data revealed new insights into recent processes by analysing genetic structure within ancient lineages defined by mtDNA data. Stepwise mutation model (SMM) and nonSMM-based methods demonstrated a clear genetic structuring within the Northwestern European lineage comprising populations from Britain and Belgium, and within the Central European lineage populations from the rivers Danube, Elbe and Main. Supported by an analysis of genetic variability within populations these results showed that the bullhead populations most probably persisted throughout the last major glaciation within the British Isles and within the drainages of the rivers Elbe and Main. Such observations provide the first genetic evidence for a glacial refugium in such close proximity to the European glacial margins.