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Paralia (Bacillariophyta) stowaways in ship ballast: implications for biogeography and diversity of the genus.

MacGillivary ML, Kaczmarska I - J Biol Res (Thessalon) (2015)

Bottom Line: Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina.Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada.Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Mount Allison University, 63B York Street, Sackville, NB E4L 1G7 Canada.

ABSTRACT

Background: The genus Paralia Heiberg is one of the most recognizable, widely distributed and commonly reported diatoms from contemporary coastal marine environments and ship ballast. Species discovery has historically been made in diatoms through the recognition of morphological discontinuities between specimens, first using light and later electron microscopy. However, recently, morphologically semi-cryptic species of Paralia were delineated using genetic analyses, among mostly tropical and subtropical sites.

Results: Ten morphological characters of the frustules and sequence fragments from the nuclear genome (conserved 18S regions of ribosomal RNA and the variable internal transcribed spacer [ITS]), and from the RuBisCo large subunit (rbcL) gene of the chloroplast genome were examined. Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina. The latter was lecto- and epitypified here because it is most similar to specimens in the type preparation BM1021 representing Smith's concept of the species. Paralia marina and certain genodemes of P. guyana were morphologically cryptic. Only those genodemes of P. guyana that possess prickly separation valves could be morphologically distinguished from P. marina with relative confidence in SEM preparations. All clones established from chains isolated from the ballast sediment of the ships sailing along the Atlantic coast of North America belonged to P. guyana. All DNA sequences of preserved Paralia chains recovered from the three trans-Atlantic voyages (TAVs) samples arriving to eastern Canada from Europe shared 100% identity with P. marina.

Conclusion: First, if the [Formula: see text] = 130592 P. marina cells per ballast tank at the end of the TAVs represents their abundance in ballast tanks of similar crossings and following mid-ocean ballast water exchange, then this diatom, if de-ballasted, exerts a strong and continued propagule pressure on Eastern Canadian coasts. Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada. Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

No MeSH data available.


Related in: MedlinePlus

Hierarchical clustering ofParaliaspecies based on SEM morphometrics. Representative clones were selected based on methods described in the text. The identity and taxonomic affiliation of each clone or sample (in parenthesis) are presented to the right of the cluster diagram. The assigned morpho-cluster and molecular clade (see below) and character state of separation valve face are indicated to the right. Multiscale bootstrap values (AU) are shown as p-values (multiplied by 100) generated from 10000 bootstrap samples; p ≥ 0.95 is considered statistically significant. Distance is equal to 1-correlation so that nodes closer to 0.00 are morphologically more similar. 1 = [10]; 2 = [6]; 3 = P. sulcata s.s., P. ehrmanii and P. obscura have not been genetically defined.
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Fig10: Hierarchical clustering ofParaliaspecies based on SEM morphometrics. Representative clones were selected based on methods described in the text. The identity and taxonomic affiliation of each clone or sample (in parenthesis) are presented to the right of the cluster diagram. The assigned morpho-cluster and molecular clade (see below) and character state of separation valve face are indicated to the right. Multiscale bootstrap values (AU) are shown as p-values (multiplied by 100) generated from 10000 bootstrap samples; p ≥ 0.95 is considered statistically significant. Distance is equal to 1-correlation so that nodes closer to 0.00 are morphologically more similar. 1 = [10]; 2 = [6]; 3 = P. sulcata s.s., P. ehrmanii and P. obscura have not been genetically defined.

Mentions: Eight species, two from this study and six from related species examined earlier [6,10], were analyzed metrically using SEM images using ten metric valve characters also used in recent taxonomic studies of this genus ([6,10,12]; Table 2). This is much more than a routine diatom metric analysis (e.g., valve length, width, striae and areolae) and demonstrated both the wide range of intraspecific morphological variation and the considerable overlap between these taxa. Hierarchical clustering of morphometrically continuous data (i.e., number of rimoportulae in 10 μm, Table 2) rendered approximately unbiased (AU) multiscale bootstrap values and ordered clones into three main clusters, namely, C1, C2 and C3 (Figure 10), represented by two, four and 31 clones respectively. The smallest cluster (p = 0.98), C1, consisted of Miocene P. sulcata s.s. and extant P. fenestrata which both had smooth valve faces on separation valves, but could be distinguished from all other taxa by open, wide, horseshoe-shaped fenestrae. The larger, second cluster, C2 (p = 0.91), included the P. longispina-like species, P. allisonii and P. crawfordii, both of which had triangular marginal spines on the face of separation valves, and one clone from the P. guyana ‘caisn’ genodeme which did not have marginal spines, but had prickles on the separation valve face (Figure 10). Cluster C3 contained four species and all genodemes of P. guyana and may be subdivided into four metrically defined sub-clusters containing a mixture of species and their genodemes. Each of the sub-clusters (C3a-d) had separation valves possessing various non-metric characters (i.e., presence or absence of prickles or spines on the separation valve face). Sub-cluster C3a contained only P. marina (p = 1.00). On the other hand, sub-cluster C3b (p = 1.00) grouped together four taxa with different separation valve face microarchitecture; smooth (Miocene P. obscura, extant P. marina and six clones of the extant ‘smooth’ genodeme of P. guyana), prickly (one clone each of the extant ‘caisn’ and ‘capebreton’ genodemes of P. guyana) and spiny (extant P. ehrmanii). The third sub-cluster, C3c (p = 0.95), contained the three prickly genodemes of P. guyana (three, four and two clones of the ‘caisn’, ‘capebreton’ and ‘servidei’ genodemes, respectively). Sub-cluster C3d grouped together seven clones representing the smooth-faced P. marina (two clones), the ‘smooth’ genodeme of P. guyana (one clone) and the three prickly separation valve-faced P. guyana genodemes (p = 1.00). Neither metric nor discrete characters measured and evaluated consistently segregated taxa from cluster C3 in agreement with their genetic signatures (see below).Figure 10


Paralia (Bacillariophyta) stowaways in ship ballast: implications for biogeography and diversity of the genus.

MacGillivary ML, Kaczmarska I - J Biol Res (Thessalon) (2015)

Hierarchical clustering ofParaliaspecies based on SEM morphometrics. Representative clones were selected based on methods described in the text. The identity and taxonomic affiliation of each clone or sample (in parenthesis) are presented to the right of the cluster diagram. The assigned morpho-cluster and molecular clade (see below) and character state of separation valve face are indicated to the right. Multiscale bootstrap values (AU) are shown as p-values (multiplied by 100) generated from 10000 bootstrap samples; p ≥ 0.95 is considered statistically significant. Distance is equal to 1-correlation so that nodes closer to 0.00 are morphologically more similar. 1 = [10]; 2 = [6]; 3 = P. sulcata s.s., P. ehrmanii and P. obscura have not been genetically defined.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4389653&req=5

Fig10: Hierarchical clustering ofParaliaspecies based on SEM morphometrics. Representative clones were selected based on methods described in the text. The identity and taxonomic affiliation of each clone or sample (in parenthesis) are presented to the right of the cluster diagram. The assigned morpho-cluster and molecular clade (see below) and character state of separation valve face are indicated to the right. Multiscale bootstrap values (AU) are shown as p-values (multiplied by 100) generated from 10000 bootstrap samples; p ≥ 0.95 is considered statistically significant. Distance is equal to 1-correlation so that nodes closer to 0.00 are morphologically more similar. 1 = [10]; 2 = [6]; 3 = P. sulcata s.s., P. ehrmanii and P. obscura have not been genetically defined.
Mentions: Eight species, two from this study and six from related species examined earlier [6,10], were analyzed metrically using SEM images using ten metric valve characters also used in recent taxonomic studies of this genus ([6,10,12]; Table 2). This is much more than a routine diatom metric analysis (e.g., valve length, width, striae and areolae) and demonstrated both the wide range of intraspecific morphological variation and the considerable overlap between these taxa. Hierarchical clustering of morphometrically continuous data (i.e., number of rimoportulae in 10 μm, Table 2) rendered approximately unbiased (AU) multiscale bootstrap values and ordered clones into three main clusters, namely, C1, C2 and C3 (Figure 10), represented by two, four and 31 clones respectively. The smallest cluster (p = 0.98), C1, consisted of Miocene P. sulcata s.s. and extant P. fenestrata which both had smooth valve faces on separation valves, but could be distinguished from all other taxa by open, wide, horseshoe-shaped fenestrae. The larger, second cluster, C2 (p = 0.91), included the P. longispina-like species, P. allisonii and P. crawfordii, both of which had triangular marginal spines on the face of separation valves, and one clone from the P. guyana ‘caisn’ genodeme which did not have marginal spines, but had prickles on the separation valve face (Figure 10). Cluster C3 contained four species and all genodemes of P. guyana and may be subdivided into four metrically defined sub-clusters containing a mixture of species and their genodemes. Each of the sub-clusters (C3a-d) had separation valves possessing various non-metric characters (i.e., presence or absence of prickles or spines on the separation valve face). Sub-cluster C3a contained only P. marina (p = 1.00). On the other hand, sub-cluster C3b (p = 1.00) grouped together four taxa with different separation valve face microarchitecture; smooth (Miocene P. obscura, extant P. marina and six clones of the extant ‘smooth’ genodeme of P. guyana), prickly (one clone each of the extant ‘caisn’ and ‘capebreton’ genodemes of P. guyana) and spiny (extant P. ehrmanii). The third sub-cluster, C3c (p = 0.95), contained the three prickly genodemes of P. guyana (three, four and two clones of the ‘caisn’, ‘capebreton’ and ‘servidei’ genodemes, respectively). Sub-cluster C3d grouped together seven clones representing the smooth-faced P. marina (two clones), the ‘smooth’ genodeme of P. guyana (one clone) and the three prickly separation valve-faced P. guyana genodemes (p = 1.00). Neither metric nor discrete characters measured and evaluated consistently segregated taxa from cluster C3 in agreement with their genetic signatures (see below).Figure 10

Bottom Line: Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina.Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada.Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Mount Allison University, 63B York Street, Sackville, NB E4L 1G7 Canada.

ABSTRACT

Background: The genus Paralia Heiberg is one of the most recognizable, widely distributed and commonly reported diatoms from contemporary coastal marine environments and ship ballast. Species discovery has historically been made in diatoms through the recognition of morphological discontinuities between specimens, first using light and later electron microscopy. However, recently, morphologically semi-cryptic species of Paralia were delineated using genetic analyses, among mostly tropical and subtropical sites.

Results: Ten morphological characters of the frustules and sequence fragments from the nuclear genome (conserved 18S regions of ribosomal RNA and the variable internal transcribed spacer [ITS]), and from the RuBisCo large subunit (rbcL) gene of the chloroplast genome were examined. Frustule morphology did not segregate species, however, comparisons of sequence fragments and ITS2 secondary structures yielded a new species from North American waters, P. guyana (with four genodemes), and another widely-distributed species, P. marina. The latter was lecto- and epitypified here because it is most similar to specimens in the type preparation BM1021 representing Smith's concept of the species. Paralia marina and certain genodemes of P. guyana were morphologically cryptic. Only those genodemes of P. guyana that possess prickly separation valves could be morphologically distinguished from P. marina with relative confidence in SEM preparations. All clones established from chains isolated from the ballast sediment of the ships sailing along the Atlantic coast of North America belonged to P. guyana. All DNA sequences of preserved Paralia chains recovered from the three trans-Atlantic voyages (TAVs) samples arriving to eastern Canada from Europe shared 100% identity with P. marina.

Conclusion: First, if the [Formula: see text] = 130592 P. marina cells per ballast tank at the end of the TAVs represents their abundance in ballast tanks of similar crossings and following mid-ocean ballast water exchange, then this diatom, if de-ballasted, exerts a strong and continued propagule pressure on Eastern Canadian coasts. Despite this, as of 2009, P. marina was found only in Cheticamp, Nova Scotia, Canada. Second, genetic analysis readily segregated cryptic and semi-cryptic taxa of Paralia, highlighting the usefulness of the molecular approach to species recognition, e.g., in programs monitoring alien introductions.

No MeSH data available.


Related in: MedlinePlus