Genetic, Ecological and Morphological Distinctness of the Blue Mussels Mytilus trossulus Gould and M-edulis L. in the White Sea

Two blue mussel lineages of Pliocene origin, Mytilus edulis (ME) and M. trossulus (MT), co-occur and hybridize in several regions on the shores of the North Atlantic. The two species were distinguished from each other by molecular methods in the 1980s, and a large amount of comparative data on them has been accumulated since that time. However, while ME and MT are now routinely distinguished by various genetic markers, they tend to be overlooked in ecological studies since morphological characters for taxonomic identification have been lacking, and no consistent habitat differences between lineages have been reported. Surveying a recently discovered area of ME and MT co-occurrence in the White Sea and employing a set of allozyme markers for identification, we address the issue whether ME and MT are true biological species with distinct ecological characteristics or just virtual genetic entities with no matching morphological and ecological identities. We find that: (1) in the White Sea, the occurrence of MT is largely concentrated in harbors, in line with observations from other subarctic regions of Europe; (2) mixed populations of ME and MT are always dominated by purebred individuals, animals classified as hybrids constituting only ca. 18%; (3) in terms of shell morphology, 80% of MT bear a distinct uninterrupted dark prismatic strip under the ligament while 97% of ME lack this character; (4) at sites of sympatry MT is more common on algal substrates while ME mostly lives directly on the bottom. This segregation by the substrate may contribute to maintaining reproductive isolation and decreasing competition between taxa. We conclude that while ME and MT are not fully reproductively isolated, they do represent clearly distinguishable biological, ecological and morphological entities in the White Sea. It remains to be documented whether the observed morphological and ecological differences are of a local character, or whether they have simply been overlooked in other contact zones.Peer reviewe

Species identification based on a semi-diagnostic marker : Evaluation of a simple conchological test for distinguishing blue mussels Mytilus edulis L. and M. trossulus Gould

Cryptic and hybridizing species may lack diagnostic taxonomic characters leaving researchers with semi-diagnostic ones. Identification based on such characters is probabilistic, the probability of correct identification depending on the species composition in a mixed population. Here we test the possibilities of applying a semi-diagnostic conchological character for distinguishing two cryptic species of blue mussels, Mytilus edulis and M. trossulus. These ecologically, stratigraphically and economically important molluscs co-occur and hybridize in many areas of the North Atlantic and the neighboring Arctic. Any cues for distinguishing them in sympatry without genotyping would save much research effort. Recently these species have been shown to statistically differ in the White Sea, where a simple character of the shell was used to distinguish two mussel morphotypes. In this paper, we analyzed the associations between morphotypes and species-specific genotypes based on an abundant material from the waters of the Kola Peninsula (White Sea, Barents Sea) and a more limited material from Norway, the Baltic Sea, Scotland and the Gulf of Maine. The performance of the "morphotype test" for species identification was formally evaluated using approaches from evidence-based medicine. Interspecific differences in the morphotype frequencies were ubiquitous and unidirectional, but their scale varied geographically (from 75% in the White Sea to 15% in the Baltic Sea). In addition, salinity-related variation of this character within M. edulis was revealed in the Arctic Barents Sea. For every studied region, we established relationships between the proportions of the morphotypes in the populations as well as between the proportions of the morphotypes in samples and the probabilities of mussels of different morphotypes being M. trossulus and M. edulis. We provide recommendations for the application of the morphotype test to mussels from unstudied contact zones and note that they may apply equally well to other taxa identified by semi-diagnostic traits.Peer reviewe

Spatial Variation in the Frequency of Left-Sided Morph in European Flounder <i>Platichthys flesus</i> (Linnaeus, 1758) from the Marginal Arctic (the White Sea)

The European flounder, Platichthys flesus, is a polymorphic flatfish, which has a large population variation in the proportion of left-sided and right-sided morphs across its geographic range. We compared the frequencies of these morphs in the White Sea (Kandalaksha, Onega, Dvina, and Mezen bays), the region in the northeastern part of species’ range adjacent to the Arctic. The proportion of the two morphs in the populations of White Sea flounders showed high variability and specific regional characteristics. The highest frequency of left-sided individuals was observed in the northwestern (Kandalaksha Bay) and southwestern (Onega Bay) parts of the White Sea. Flounders living in the eastern part of the White Sea (Dvina and Mezen bays) showed a much lower frequency of this trait. No consistent pattern of geographic variation in the proportion of the morphs was found in the geographic range of P. flesus. The lowest frequencies of left-sided individuals were recorded in the flounder populations living at the eastern and western margins of the geographic range. Geographic variation in the proportion of left-sided individuals in flounder populations is likely to be determined by a set of biotic and abiotic factors. Selective influence of the latter, acting through the trophic relationships of this species with other marine organisms, can differ in different parts of flounder’s geographic range

Spatial Variation in the Frequency of Left-Sided Morph in European Flounder Platichthys flesus (Linnaeus, 1758) from the Marginal Arctic (the White Sea)

The European flounder, Platichthys flesus, is a polymorphic flatfish, which has a large population variation in the proportion of left-sided and right-sided morphs across its geographic range. We compared the frequencies of these morphs in the White Sea (Kandalaksha, Onega, Dvina, and Mezen bays), the region in the northeastern part of species&rsquo; range adjacent to the Arctic. The proportion of the two morphs in the populations of White Sea flounders showed high variability and specific regional characteristics. The highest frequency of left-sided individuals was observed in the northwestern (Kandalaksha Bay) and southwestern (Onega Bay) parts of the White Sea. Flounders living in the eastern part of the White Sea (Dvina and Mezen bays) showed a much lower frequency of this trait. No consistent pattern of geographic variation in the proportion of the morphs was found in the geographic range of P. flesus. The lowest frequencies of left-sided individuals were recorded in the flounder populations living at the eastern and western margins of the geographic range. Geographic variation in the proportion of left-sided individuals in flounder populations is likely to be determined by a set of biotic and abiotic factors. Selective influence of the latter, acting through the trophic relationships of this species with other marine organisms, can differ in different parts of flounder&rsquo;s geographic range

Exploring Genetic and Morphological Integrity across Ocean Basins: A Case Study of the Mesopelagic Shrimp <i>Systellaspis debilis</i> (Decapoda: Oplophoridae)

Plankton communities often consist of cosmopolitan species with an extensive gene flow between populations. Nevertheless, populations of some plankton species are genetically structured, owing to various barriers such as ocean currents, hydrological fronts, and continents. Drivers that could explain the genetic structures of most mesopelagic species remain unknown on an ocean-basin scale, and our study aims to analyze the genetic and morphological differences between populations of a cosmopolitan mesopelagic shrimp, Systellaspis debilis, from the Southern and Northern Atlantic Ocean, and the Southwest Indian Ocean. We analyzed the ITS-1 and COI markers of 75 specimens and assessed the genetic integrity and within-species variability of these genes. We also coded 32 morphological characteristics in 73 specimens, analyzed their variability, and assessed the correlation between morphological and genetic characteristics using a Redundancy analysis and Mantel test. Systellaspis debilis was genetically cohesive across the whole Atlantic and Southwest Indian Oceans, which is possibly a result of an intensive gene flow through ecological barriers, the resistance of species to hydrological gradients, a purifying selection of mitochondrial genes, etc. In contrast, we found significant morphological differences between populations from different regions, which mirrors morphological diversification and calls for further genomic approaches in order to understand the basis of these variations and uncover potential local adaptations

Taxonomic composition and morphological features of putative purebred and hybrid mussels in samples of different genetic composition.

<p>PSS on abscissas are plotted against: (A). frequencies of ME (blue symbols), MT (red symbols) and hybrids (green symbols) in samples; (B). ratios between sample means of shell length L of MT and hybrids (red symbols) and ME and hybrids (blue symbols) in samples; (C). frequencies of T-morphotypes among ME (blue symbols), MT (red symbols) and hybrid (green symbols) genetic classes in samples. Polynomial (A) or linear (B, C) functions were fitted to the data. Groups of less than 4 genotypes are not included. Classification of genotypes to ancestry classes in all cases was ISS-based.</p

Distribution of genetic disequilibrium measures in samples of different genetic composition.

<p>PSS, characterizing samples’ genetic composition, are on abscissas, genotypic disequilibrium measures are on ordinate axes: (A). Intra-locus heterozygote deficit <i>F</i>_IS. (B). Average inter-locus correlation <i>R</i>’. Green crosses correspond to empirical samples, orange crosses mark simulated mixed samples. Circles, squares and triangles mark Um, Ry and Ch samples, correspondingly (small symbols correspond to subsamples from different substrates, large symbols to pooled samples). The curves show the maximum disequilibrium in case of physical mixing without interbreeding. Expectations for equilibrium panmictic populations would be close to 0.</p

Genetic composition of mussel samples from Chupa (Ch), Umba (Um) and Ryazhkov (Ry).

<p>Subsamples collected from different substrates (A–algae, B–bottom) are treated separately. <u>Left panel:</u> Frequency distributions of individual T-scores (the sum of T-alleles across the 4 loci). Numbers of individuals are plotted on the abscissas, with T-scores as ordinates. Dark and light bars indicate T- and E-morphotypes, correspondingly. Green lines display the expected distributions under local random mating (dotted lines) and a mixture of parental genotypes without interbreeding (continuous lines). <u>Central panel:</u> Pie charts in the middle illustrate T-frequencies (red sector) vs. E-frequencies (blue sector). The estimated PSS values and the disequilibrium estimates R’ and F_IS are shown. <u>Right panel:</u> ISS distributions. Each symbol represents an individual, ranked along the horizontal axis by ISS. Dark symbols correspond to T-morphotypes, open symbols–to E-morphotypes. The shapes of the symbols reflect an individual T-score: circles– 0–1 (“ME”), triangular– 2–6 (“hybrid”), diamonds– 7–8 (“MT”). Horizontal lines reflect the thresholds chosen to delimit the genotype classes of ME (lower threshold) and MT (upper threshold) on the basis of the analysis of simulated samples (see text, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0152963#pone.0152963.s002" target="_blank">S2 Fig</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0152963#pone.0152963.s003" target="_blank">S3 Fig</a> for details).</p

Map of study area and sampling sites.

<p>(A). Location of the Kandalaksha Bay of the White Sea, and general distribution of three mussel taxa in Europe: ME (<i>Mytilus edulis</i>, blue), MT (<i>M</i>. <i>trossulus</i>, red) and <i>M</i>. <i>galloprovincialis</i> (MG, yellow). Bi- or tri-colored circles indicate zones of sympatry (see references in the text). (B-D) Sampling locations in the White Sea: (B) Kandalaksha Bay. (C) Umba town area. (D) Top of Kandalaksha Bay. Pie diagrams depict estimates of the proportions of ME (blue sector) and MT (red sector) genomes in samples from the genetic dataset (GDS), obtained by STRUCTURE analysis of four-locus genotype data (PSS, see text for details). Data on paired local subsamples collected from the algal and the bottom substrates are shown above and below the algae pictogram, respectively. Black pins indicate sampling sites of the MDS (morphology only). Detailed sampling locality data are in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0152963#pone.0152963.s004" target="_blank">S1 Table</a>. The green lines in part D are isohalines of surface water (after [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0152963#pone.0152963.ref034" target="_blank">34</a>]).</p