Mesozoic mitogenome rearrangements and freshwater mussel (Bivalvia: Unionoidea) macroevolution

Abstract

Using a new fossil-calibrated mitogenome-based approach, we identified macroevolutionary shifts in mitochondrial gene order among the freshwater mussels (Unionoidea). We show that the early Mesozoic divergence of the two Unionoidea clades, Margaritiferidae and Unionidae, was accompanied by a synchronous split in the gene arrangement in the female mitogenome (i.e., gene orders MF1 and UF1). Our results suggest that this macroevolutionary jump was completed within a relatively short time interval (95% HPD 201-226 Ma) that coincided with the Triassic-Jurassic mass extinction. Both gene orders have persisted within these clades for ~200 Ma. The monophyly of the so-called "problematic" Gonideinae taxa was supported by all the inferred phylogenies in this study using, for the first time, the M- and F-type mitogenomes either singly or combined. Within Gonideinae, two additional splits in the gene order (UF1 to UF2, UF2 to UF3) occurred in the Mesozoic and have persisted for ~150 and ~100 Ma, respectively. Finally, the mitogenomic results suggest ancient connections between freshwater basins of East Asia and Europe near the Cretaceous-Paleogene boundary, probably via a continuous paleo-river system or along the Tethys coastal line, which are well supported by at least three independent but almost synchronous divergence events.

Fig. 1

Gene maps of the F- and M-type mitochondrial genomes of Chamberlainia hainesiana, Microcondylaea bonellii, Pilsbryoconcha exilis and Monodontina vondembuschiana. Genes positioned inside the circle are encoded on the heavy strand, and genes outside the circle are encoded on the light strand. Color codes: Small and large ribosomal RNAs (red), transfer RNAs (purple), FORF F-specific open reading frame (yellow), MORF M-specific open reading frame (yellow), PCGs genes (green)

Fig. 2

Diagrams of the four distinct gene orders known in Unionidae to date. In the F-type, three gene orders are depicted: UF1, UF2 and UF3. In the male M-type lineage, the only Unionidae gene arrangement is shown: M-type 1 (UM1). Blue boxes highlight gene rearrangement region from UF1 to UF2 (Box A) and from UF2 to UF3 (Box B). Small and large ribosomal RNAs and transfer RNAs are depicted by one letter of the amino acid code; Arrow colour codes, follow Fig. 1

Fig. 3

Phylogenetic (BI-NUC) tree of Unionida estimated from 14 concatenated individual mtDNA gene sequences (12 protein-coding and 2 rRNA genes). Values for branch support are represented in the following order: (1) Bayesian posterior probabilities (PP) for BI-NUC tree, (2) Bayesian PP for BI-AA tree, (3) ML bootstrap support (BS) values for ML-NUC and (4) ML BS values for ML-AA tree. Maximum support values (PP = 1, BS = 100) are represented by asterisks. Gonideinae subfamily and tribes are highlighted. For details see text. GenBank codes in Table 1

Fig. 4

Phylogenetic (BI-NUC) tree of Unionida estimated from 28 concatenated individual mtDNA gene sequences (24 protein-coding and 4 rRNA genes) of the first combined Female+Male concatenated data set. Maximum branch support values (BI-NUC/BI-AA PP = 1; ML-NUC/ML-AA BS = 100) are represented by asterisks, while # represents the only non-supported branch by ML-AA tree. Gonideinae subfamily and tribes are highlighted. GenBank codes in Table 1

Fig. 5

Unionidae F-haplotype phylogenetic sub-tree (BI-NUC) used to infer the most parsimonious putative ancestral gene orders and gene rearrangements, mapped as MF1, UF1, UF2 and UF3 (see text for details). Margaritiferidae and all subfamily nodes were collapsed for visual purposes

Fig. 6

Time-calibrated mitogenomic phylogeny, an example of three-level classification scheme (subfamilies, tribes and subtribes) and evolution of the mitochondrial gene order in the Unionoidea. Fossil-calibrated ultrametric chronogram of the Unionoidea calculated under a lognormal relaxed clock model and a Yule process speciation implemented in BEAST and obtained for the complete mitogenome data set. The outgroup sample is not shown. Bars indicate 95% confidence intervals of the estimated divergence times between lineages (Ma). Black numbers near nodes are mean ages (Ma). Color labels indicate the mitochondrial gene order (MF1, UF1, UF2, and UF3). Red asterisks indicate fossil calibrations (Supplementary Table 1). Stratigraphic chart according to the International Commission on Stratigraphy, 2015

Fig. 7

Historical biogeography of the Unionidae. This combined scenario has been inferred from three different statistical modeling approaches (S-DIVA, DEC and S-DEC) based on the time-calibrated mitogenomic phylogeny (Fig. 6). Pie charts near nodes indicate probabilities of certain ancestral areas. Color circles on the tip nodes indicate the range of each species. Color labels indicate the mitochondrial gene order (UF1, UF2, and UF3)