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.
Highlights
The tempo, timing and mode of evolution have attracted considerable debate among evolutionary biologists
On the basis of the most comprehensive data set of mitogenomes sampled to date, including eight newly sequenced mitogenomes, this paper aims to improve our understanding of the higher-order phylogeny and classification of Unionidae by the following: (1) testing the monophyly of the poorly known Gonideinae subfamily using both full F- and M- mitogenomes and, for the first time, mitogenomes concatenated; (2) estimating macroevolutionary patterns in freshwater mussels of the Unionidae using, for the first time, a fossil-calibrated mitogenomic approach; (3) estimating the timing of major divergence events and comparing them to those of mitogenome rearrangements; and (4) developing an updated integrative approach to the systematics of Unionidae, on the basis of the mitogenomic results
All eight sequenced haplotypes include the 13 proteincoding genes (PCGs) typically found in metazoan mitochondrial genomes, the sex-specific ORF described for all Unionida mitogenomes with Doubly Uniparental Inheritance (DUI) system (Breton et al 2009, 2011) and 22 transfer RNA and two ribosomal RNA genes (Fig. 1)
Summary
The tempo, timing and mode of evolution have attracted considerable debate among evolutionary biologists. The gene arrangement within mitogenomes is highly conserved, e.g., many vertebrate groups share the same gene order (Pereira 2000). Local homoplastic arrangements have been identified in some invertebrate groups (e.g., Flook and Rowel 1995; Dowton and Austin 1999), complete gene orders generally remain unique and represent signatures with diagnostic value (Basso et al 2017), providing a powerful signal for inferring ancient evolutionary relationships (Boore 2000)
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