Cementing mussels to oysters in the pteriomorphian tree: a phylogenomic approach

Abstract

Mussels (Mytilida) are a group of bivalves with ancient origins and some of the most important commercial shellfish worldwide. Mytilida consists of approximately 400 species found in various littoral and deep-sea environments, and are part of the higher clade Pteriomorphia, but their exact position within the group has been unstable. The multiple adaptive radiations that occurred within Pteriomorphia have rendered phylogenetic classifications difficult and uncertainty remains regarding the relationships among most families. To address this phylogenetic uncertainty, novel transcriptomic data were generated to include all five orders of Pteriomorphia. Our results, derived from complex analyses of large datasets from 41 transcriptomes and evaluating possible pitfalls affecting phylogenetic reconstruction (matrix occupancy, heterogeneity, evolutionary rates, evolutionary models), consistently recover a well-supported phylogeny of Pteriomorphia, with the only exception of the most complete but smallest data matrix (Matrix 3: 51 genes, 90% gene occupancy). Maximum-likelihood and Bayesian mixture model analyses retrieve strong support for: (i) the monophyly of Pteriomorphia, (ii) Mytilida as a sister group to Ostreida, and (iii) Arcida as sister group to all other pteriomorphians. The basal position of Arcida is congruent with its shell microstructure (solely composed of aragonitic crystals), whereas Mytilida and Ostreida display a combination of a calcitic outer layer with an aragonitic inner layer composed of nacre tablets, the latter being secondarily lost in Ostreoidea.

Keywords: Bivalvia; Mollusca; evolutionary rate; genome; phylogenomics; phylogeny.

Figure 1.

(a) Gene occupancy representation per species with maximum occupancy towards the top left. A light cell indicates a non-sampled gene. Mytilus galloprovincialis is the best-represented species, whereas Saccostrea palmula is the worst-represented one. Matrix 1 is represented in red, Matrix 2 in yellow and Matrix 3 in green. (b) Schematic of the 13 matrices generated for the phylogenetic, per cent pairwise identity and compositional heterogeneity analyses. Colour codes are as in (a). (Online version in colour.)

Figure 2.

Phylogenetic hypothesis based on Matrix 2 analysed in PhyML-PCMA (Ln L = −1 132 164.323494) with support values plotted as follows: checked boards in major deep nodes represent nodal support for the different analyses in Matrix 1 (red), Matrix 2 (yellow) and Matrix 3 (green). PhyML-PCMA and ExaML are abbreviated as ML, ExaBayes: EB, PhyloBayes: PB, and RAxML with gene partitions: GP. Filled squares indicate nodal support values higher than 99% BS (ML) and a pp of 0.99 or higher (EB). Grey squares indicate lower nodal support and white squares indicate unrecovered nodes in the specified analysis. Single squares on internal nodes indicate maximum support in all six analyses. Lower nodal support values of internal nodes are reported as follows: Matrix 1 ML/Matrix 1 EB/Matrix 2 ML/Matrix 2 EB/Matrix 2 PB/Matrix 3 ML/Matrix 3 EB/Matrix 3 PB/Matrix 3 GP. Pteriomorphian families are represented in different shades of colour. Top left: supernetwork representation of quartets derived from the individual ML gene trees for Matrix 2. The same colour scheme is applied to all figures. (Online version in colour.)

Figure 3.

Bootstrap resampling frequency for phylogenetic hypotheses (a) monophyly of Pteriomorphia, (b) basal position of Arcida (=monophyly of all other pteriomorphians), (c) monophyly of Limida + Pectinida, (d) Mytilida sister group to Ostreida; inferred from Matrices A–D and Matrix 2, represented in full line (incremental addition of orthogroups in order of per cent pairwise identity, from most to least conserved); Matrices E–J, represented by diamonds (increments of non-additive 50 orthogroups in order of per cent pairwise identity, from most to least conserved). (Online version in colour.)

Figure 4.

Summary tree representing relationships among the superfamilies and orders of Pteriomorphia. Checked boards are coded as in figure 2 and represent nodal support provided by Matrices 1–3. Newell's [47] classification is given for comparison. (Online version in colour.)