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Combined Use of Morphological and Molecular Tools to Resolve Species Mis-Identifications in the Bivalvia The Case of Glycymeris glycymeris and G . pilosa

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ABSTRACT

Morphological and molecular tools were combined to resolve the misidentification between Glycymeris glycymeris and Glycymeris pilosa from Atlantic and Mediterranean populations. The ambiguous literature on the taxonomic status of these species requires this confirmation as a baseline to studies on their ecology and sclerochronology. We used classical and landmark-based morphometric approaches and performed bivariate and multivariate analyses to test for shell character interactions at the individual and population level. Both approaches generated complementary information. The former showed the shell width to length ratio and the valve asymmetry to be the main discriminant characters between Atlantic and Mediterranean populations. Additionally, the external microsculpture of additional and finer secondary ribs in G. glycymeris discriminates it from G. pilosa. Likewise, landmark-based geometric morphometrics revealed a stronger opisthogyrate beak and prosodetic ligament in G. pilosa than G. glycymeris. Our Bayesian and maximum likelihood phylogenetic analyses based on COI and ITS2 genes identified that G. glycymeris and G. pilosa form two separate monophyletic clades with mean interspecific divergence of 11% and 0.9% for COI and ITS2, respectively. The congruent patterns of morphometric analysis together with mitochondrial and nuclear phylogenetic reconstructions indicated the separation of the two coexisting species. The intraspecific divergence occurred during the Eocene and accelerated during the late Pliocene and Pleistocene. Glycymeris pilosa showed a high level of genetic diversity, appearing as a more robust species whose tolerance of environmental conditions allowed its expansion throughout the Mediterranean.

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Plot of the principal components (PCs) based on Procrustes distances (a). Shape changes associated with the PCs are shown as extreme shell shapes representing the positive and negative end of each axis. Percentages of explained variance for each axis are in parentheses. Plot of the canonical variate analysis (CVs) of overall shell shape variation along the first 2 canonical axes (b). Wrapped outline drawings show shape changes associated with variation along first axis. Glycymeris glycymeris (black inverted triangle, UK; grey inverted triangle, France) and Glycymeris pilosa (black circle, Pag; grey circle, Pašman). Percentages of explained variance for each axis are in parentheses.
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pone.0162059.g006: Plot of the principal components (PCs) based on Procrustes distances (a). Shape changes associated with the PCs are shown as extreme shell shapes representing the positive and negative end of each axis. Percentages of explained variance for each axis are in parentheses. Plot of the canonical variate analysis (CVs) of overall shell shape variation along the first 2 canonical axes (b). Wrapped outline drawings show shape changes associated with variation along first axis. Glycymeris glycymeris (black inverted triangle, UK; grey inverted triangle, France) and Glycymeris pilosa (black circle, Pag; grey circle, Pašman). Percentages of explained variance for each axis are in parentheses.

Mentions: Following the landmark-based geometric morphometrics, growth allometry of the Glycymeris sp. was observed and accounted for 14% of the total amount of shape variation. The resulting PCA revealed that the first two components PC 1 and PC 2 (eigenvalues 0.0015 and 0.0010) explained 29.5% and 19.3% of the total variability among the landmarks, on all analyzed specimens (Fig 6). At the primary axis of variation (PC 1), segregation by the species (G. glycymeris vs. G. pilosa) was observed, and it mainly described changes in the umbo region and enlargement of the posterior-ventral axis of the shell. The second PC axis was related to the development of the ligament area and elongation of the anterior region. The shell shape variations among species from different localities were successfully discriminated using CVA (Fig 6). All groups differed significantly between each other as revealed by permutation testing of Procrustes distances. The morphological differentiation measured by Procrustes distance was similarly large between the G. glycymeris from both sampling locations and G. pilosa from Pašman (0.09) or Pag (0.06), respectively. The population distances within species (G. glycymeris from UK vs. France, G. pilosa from Pag vs. Pašman) were similar and considerably smaller (0.05–0.04). The first canonical axis (CV 1) explained the majority of the total variance (75%). Depicting the between species changes along discriminant functions by warped outline drawings revealed that shape was altered most in umbo and upper posterior-anterior region (Fig 6).


Combined Use of Morphological and Molecular Tools to Resolve Species Mis-Identifications in the Bivalvia The Case of Glycymeris glycymeris and G . pilosa
Plot of the principal components (PCs) based on Procrustes distances (a). Shape changes associated with the PCs are shown as extreme shell shapes representing the positive and negative end of each axis. Percentages of explained variance for each axis are in parentheses. Plot of the canonical variate analysis (CVs) of overall shell shape variation along the first 2 canonical axes (b). Wrapped outline drawings show shape changes associated with variation along first axis. Glycymeris glycymeris (black inverted triangle, UK; grey inverted triangle, France) and Glycymeris pilosa (black circle, Pag; grey circle, Pašman). Percentages of explained variance for each axis are in parentheses.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5036790&req=5

pone.0162059.g006: Plot of the principal components (PCs) based on Procrustes distances (a). Shape changes associated with the PCs are shown as extreme shell shapes representing the positive and negative end of each axis. Percentages of explained variance for each axis are in parentheses. Plot of the canonical variate analysis (CVs) of overall shell shape variation along the first 2 canonical axes (b). Wrapped outline drawings show shape changes associated with variation along first axis. Glycymeris glycymeris (black inverted triangle, UK; grey inverted triangle, France) and Glycymeris pilosa (black circle, Pag; grey circle, Pašman). Percentages of explained variance for each axis are in parentheses.
Mentions: Following the landmark-based geometric morphometrics, growth allometry of the Glycymeris sp. was observed and accounted for 14% of the total amount of shape variation. The resulting PCA revealed that the first two components PC 1 and PC 2 (eigenvalues 0.0015 and 0.0010) explained 29.5% and 19.3% of the total variability among the landmarks, on all analyzed specimens (Fig 6). At the primary axis of variation (PC 1), segregation by the species (G. glycymeris vs. G. pilosa) was observed, and it mainly described changes in the umbo region and enlargement of the posterior-ventral axis of the shell. The second PC axis was related to the development of the ligament area and elongation of the anterior region. The shell shape variations among species from different localities were successfully discriminated using CVA (Fig 6). All groups differed significantly between each other as revealed by permutation testing of Procrustes distances. The morphological differentiation measured by Procrustes distance was similarly large between the G. glycymeris from both sampling locations and G. pilosa from Pašman (0.09) or Pag (0.06), respectively. The population distances within species (G. glycymeris from UK vs. France, G. pilosa from Pag vs. Pašman) were similar and considerably smaller (0.05–0.04). The first canonical axis (CV 1) explained the majority of the total variance (75%). Depicting the between species changes along discriminant functions by warped outline drawings revealed that shape was altered most in umbo and upper posterior-anterior region (Fig 6).

View Article: PubMed Central - PubMed

ABSTRACT

Morphological and molecular tools were combined to resolve the misidentification between Glycymeris glycymeris and Glycymeris pilosa from Atlantic and Mediterranean populations. The ambiguous literature on the taxonomic status of these species requires this confirmation as a baseline to studies on their ecology and sclerochronology. We used classical and landmark-based morphometric approaches and performed bivariate and multivariate analyses to test for shell character interactions at the individual and population level. Both approaches generated complementary information. The former showed the shell width to length ratio and the valve asymmetry to be the main discriminant characters between Atlantic and Mediterranean populations. Additionally, the external microsculpture of additional and finer secondary ribs in G. glycymeris discriminates it from G. pilosa. Likewise, landmark-based geometric morphometrics revealed a stronger opisthogyrate beak and prosodetic ligament in G. pilosa than G. glycymeris. Our Bayesian and maximum likelihood phylogenetic analyses based on COI and ITS2 genes identified that G. glycymeris and G. pilosa form two separate monophyletic clades with mean interspecific divergence of 11% and 0.9% for COI and ITS2, respectively. The congruent patterns of morphometric analysis together with mitochondrial and nuclear phylogenetic reconstructions indicated the separation of the two coexisting species. The intraspecific divergence occurred during the Eocene and accelerated during the late Pliocene and Pleistocene. Glycymeris pilosa showed a high level of genetic diversity, appearing as a more robust species whose tolerance of environmental conditions allowed its expansion throughout the Mediterranean.

No MeSH data available.


Related in: MedlinePlus