Denser mitogenomic sampling improves resolution of the phylogeny of the superfamily Trochoidea (Gastropoda: Vetigastropoda)

Abstract

The great morphological and ecological diversity within the superfamily Trochoidea s.l. (Gastropoda: Vetigastropoda) has in the past hindered the reconstruction of a robust phylogeny for the group based on morphology. Moreover, previous molecular phylogenies disagreed on the monophyly and internal relationships of Trochoidea s.l., as well as on its relative phylogenetic position within Vetigastropoda. In order to further resolve the trochoidean and vetigastropod phylogenetic trees, we considerably increased the representation of trochoidean families for which no previous mitochondrial (mt) genomes were available: the complete mt genome of Cittarium pica (Tegulidae) and the nearly complete mt genomes of Tectus virgatus (Tegulidae), Gibbula umbilicaris (Trochidae), and Margarites vorticiferus (Margaritidae) were sequenced. In addition, the nucleotide sequences of all protein coding and rRNA genes of Clanculus margaritarius (Trochidae) and of Calliostoma zizyphinum (Calliostomatidae) were derived from transcriptomic sequence data. The reconstructed phylogenetic trees using probabilistic methods and Neomphalina as outgroup recovered with maximal support a Trochoidea sensu Hickman & McLean, 1990 clade that included superfamilies Angarioidea and Phasianelloidea deeply nested within superfamily Trochoidea sensu Williams (2012). The families Trochidae and Calliostomatidae were the sister group to the remaining trochoidean lineages. Of these, the family Margaritidae was sister to a clade including Phasianelloidea + Angarioidea and Turbinidae + Tegulidae, this latter family being paraphyletic (Cittarium and Tectus need to be assigned to a new family). Gene order within newly determined mt genomes was very stable (with only few rearrangements restricted to tRNA genes) and conformed to the vetigastropod and gastropod consensus genome organizations.

A phylogenomic framework for Vetigastropoda (Mollusca)

“…Because of the minute size of scissurelloids and the deep sea environments inhabited by the two latter superfamilies, these taxa have been some of the hardest to sample in molecular phylogenies (but see Kano 2008). Lepetelloidea in particular is absent in most studies, but has been recovered as the sister group to Patellogastropoda, which was nested in Vetigastropoda, in a seven-gene phylogeny ( Seguenzioidea (here represented by Chilodontaidae) has been recovered with Haliotoidea in several mitogenome and nuclear studies (Aktipis and Giribet 2011;Lee et al 2016;Uribe et al 2016Uribe et al , 2017 and more broadly with Haliotoidea, Scissurelloidea and Lepetodriloidea in other phylogenies (Kano 2008;Williams et al 2008). Here this superfamily is the sister group to all vetigastropods except pleurotomariids (Figure 1.2).…”

“…Some key studies, though with few markers, presented densely sampled phylogenies, helping place not only the most diverse groups, but also minute and hard-to-collect taxa (Aktipis and Giribet 2011;Kano 2008;Williams et al 2008). Finally, a recent burst of publications based on mitochondrial genomes have targeted deep vetigastropod relationships, albeit with limited taxon sampling (Lee et al 2016;Uribe et al 2016Uribe et al , 2017Wort et al 2017).…”

“…haliotids, fissurellids, scissurellids) and to the asymmetric trochids (Ponder and Lindberg 1997;Salvini-Plawen 1980;Sasaki 1998). Trochoidea, the most diverse superfamily of vetigastropods, has also received considerable attention, with many dedicated studies (Uribe et al 2017;Williams 2012;Williams et al 2010Williams et al , 2008Williams and Ozawa 2006). Phasianellidae and Angariidae, once considered subfamilies of Turbinidae, have later been elevated to family and even superfamily status, being recovered as early divergences in the tree (Williams et al 2008;Williams and Ozawa 2006).…”

“…Phasianellidae and Angariidae, once considered subfamilies of Turbinidae, have later been elevated to family and even superfamily status, being recovered as early divergences in the tree (Williams et al 2008;Williams and Ozawa 2006). More recently, however, they have been consistently recovered within the superfamily Trochoidea with mitochondrial genomes and a small sample of vetigastropod transcriptomes (Lee et al 2016;Uribe et al 2016Uribe et al , 2017Zapata et al 2014).…”

“…This issue is accentuated by insufficient taxon sampling of vetigastropods and outgroups. Particularly problematic taxa that have been placed in very different positions depending on the study, and that seem to be more affected by LBA, are Fissurellidae, Haliotidae, Lepetelloidea and Lepetodriloidea (Aktipis and Giribet 2011;Lee et al 2016;Uribe et al 2016Uribe et al , 2017Williams et al 2008). Familial relationships within Trochoidea have been redefined recently with relatively good support, but pending the inclusion of several missing families (Uribe et al 2017).…”