Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 10, 342

Molecular Phylogeny of Pearl Oysters and Their Relatives (Mollusca, Bivalvia, Pterioidea)

Affiliations

Molecular Phylogeny of Pearl Oysters and Their Relatives (Mollusca, Bivalvia, Pterioidea)

Ilya Tëmkin. BMC Evol Biol.

Abstract

Background: The superfamily Pterioidea is a morphologically and ecologically diverse lineage of epifaunal marine bivalves distributed throughout the tropical and subtropical continental shelf regions. This group includes commercially important pearl culture species and model organisms used for medical studies of biomineralization. Recent morphological treatment of selected pterioideans and molecular phylogenetic analyses of higher-level relationships in Bivalvia have challenged the traditional view that pterioidean families are monophyletic. This issue is examined here in light of molecular data sets composed of DNA sequences for nuclear and mitochondrial loci, and a published character data set of anatomical and shell morphological characters.

Results: The present study is the first comprehensive species-level analysis of the Pterioidea to produce a well-resolved, robust phylogenetic hypothesis for nearly all extant taxa. The data were analyzed for potential biases due to taxon and character sampling, and idiosyncracies of different molecular evolutionary processes. The congruence and contribution of different partitions were quantified, and the sensitivity of clade stability to alignment parameters was explored.

Conclusions: Four primary conclusions were reached: (1) the results strongly supported the monophyly of the Pterioidea; (2) none of the previously defined families (except for the monotypic Pulvinitidae) were monophyletic; (3) the arrangement of the genera was novel and unanticipated, however strongly supported and robust to changes in alignment parameters; and (4) optimizing key morphological characters onto topologies derived from the analysis of molecular data revealed many instances of homoplasy and uncovered synapomorphies for major nodes. Additionally, a complete species-level sampling of the genus Pinctada provided further insights into the on-going controversy regarding the taxonomic identity of major pearl culture species.

Figures

Figure 1
Figure 1
The summary of recent hypotheses of phylogenetic relationships in the Pterioidea. Numbers in parentheses indicate the number of terminals sampled for each taxon. Abbreviations: Is, Isognomonidae; Ma, Malleidae; ME, minimum evolution; MP, maximum parsimony; ML, maximum likelihood; Pt, Pteriidae; Pu, Pulvinitidae.
Figure 2
Figure 2
A partial view of the most-parsimonious tree based on the analysis of the complete data set and the results of the sensitivity analysis showing the relationships of the outgroups, and the genera Pulvinites, Malleus, and Pteria. The single most-parsimonious topology (L = 6027, CI = 0.56, RI = 0.86) of the complete data set resulting from the combined analysis of the 18S, 28S, 16S, and H3 data under uniform weighting. Numbers at the nodes denoted node numbers; numbers above the branches indicate jackknife/Bremer support values. The results of the sensitivity analysis are summarized below the branches as binary plots with filled shapes denoting clade presence and open shapes denoting clade absence. Circles and squares indicate whether the analyses were performed with or without taking the affine gap costs into account respectively. The tables below describe specific parameter combination used for each analysis listing the costs in the following order: "indel/transversion/transition" or "gap opening/(gap extension)/transition/transversion." Shell icons denote type species.
Figure 3
Figure 3
A partial view of the most-parsimonious tree based on the analysis of the complete data set and the results of the sensitivity analysis showing the relationships of the genera Isognomon, Vulsella, Electroma, Crenatula, and Pinctada. See Figure 2 for legend.
Figure 4
Figure 4
Alternative hypotheses for the pterioidean sister group. Each panel represents a summary topology recovered for the combination(s) of alignment parameters indicated by the sensitivity plots below. See Figure 2 for legend.
Figure 5
Figure 5
Stability trees. Strict (a) and majority-rule (b) consensus trees summarizing cladograms resulting from sensitivity analysis of the complete data set analyzed under 22 alignment parameter combinations (see text for details).
Figure 6
Figure 6
The most-parsimonious tree based on the analysis of the complete data using non-uniform weighting. The single most-parsimonious cladogram (L = 12508, CI = 0.24, RI = 0.52) resulting from the combined analysis of the 18S, 28S, 16S, and H3 data under the cost regime that maximizes homology of both sequence fragments and individual nucleotide positions (2 for substitutions, 3 for gap opening, and 1 for gap extension; [105]).
Figure 7
Figure 7
Partitioned Bremer support (PBrS) analysis. The histogram shows proportional support of each locus for all the nodes (as labeled in Figure 2). The table above the histogram summarizes the PBrS statistics for each locus. Χ, the average Bremer support; Σ, the total Bremer support; %, the percentage of the cumulative Bremer support; %n, percent normalized by the number of parsimony informative characters.
Figure 8
Figure 8
The maximum likelihood tree resulting from the analysis of the complete data set. The ML tree (-logLk = 30253.94) resulting from the combined analysis of the 18S, 28S, 16S, and H3 data. The scale bar indicates the number of substitutions per site. The nodes that disagree between the ML and MP topologies are indicated by arrows.
Figure 9
Figure 9
Parsimony analyses of the reduced data set. All analyses produced single most-parsimonious trees. For molecular-only and simultaneous analyses the combined data for 18S, 28S, 16S, and H3 data were analyzed under equal-costs alignment regime. (a) Morphological data (length = 317, CI = 0.54, RI = 0.56; data from [15]). (b) The molecular data-only tree (1 MPT, length = 3,094, CI = 70.43, RI = 67,40). (c) Combined molecular and morphological data (1 MPT, length = 3,425, CI = 68.85, RI = 66.14). Numbers above branches are jackknife support values. Arrow designates the Pterioidea. Abbreviations: Is, Isognomonidae; Ma, Malleidae; Pt, Pteriidae; Pu, Pulvinitidae.
Figure 10
Figure 10
Parsimony analysis of the complete combined data set. The single most-parsimonious tree (L = 6358, CI = 56, RI = 86) resulting from the parsimony analysis of combined molecular (18S, 28S, 16S, and H3) and morphological data under uniform weighting. Numbers above branches are jackknife support values.

Similar articles

See all similar articles

Cited by 6 PubMed Central articles

See all "Cited by" articles

References

    1. Donkin RA. Beyond price. Pearls and pearl-fishing: origins to the Age of Discoveries. Vol. 224. Philadelphia: American Philosophical Society; 1998.
    1. Landman NH, Mikkelsen PM, Bieler R, Bronson B. Pearls: a natural history. New York: Harry N. Abrams, Inc; 2001.
    1. Strack E. Pearls. Stuttgart: Ruhle-Diebener-Verlag GmbH & Co; 2006.
    1. Southgate PC, Lucas JS. The pearl oyster. Amsterdam, Boston, Heidelberg, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo: Elsevier; 2008.
    1. Burch BL. Pearly shells - part 5: transport by man of commercial pearl shells and their hitch-hikers. Hawaiian Shell News. 1995;43(6):3–6.

Publication types

Substances

LinkOut - more resources

Feedback