Molecular paleobiological insights into the origin of the Brachiopoda

Abstract

Most studies of brachiopod evolution have been based on their extensive fossil record, but molecular techniques, due to their independence from the rock record, can offer new insights into the evolution of a clade. Previous molecular phylogenetic hypotheses of brachiopod interrelationships place phoronids within the brachiopods as the sister group to the inarticulates, whereas morphological considerations suggest that Brachiopoda is a monophyletic group. Here, these hypotheses were tested with a molecular phylogenetic analysis of seven nuclear housekeeping genes combined with three ribosomal genes. The combined analysis finds brachiopods to be monophyletic, but with relatively weak support, and the craniid as the sister taxon of all other brachiopods. Phylogenetic-signal dissection suggests that the weak support is caused by the instability of the craniid, which is attracted to the phoronids. Analysis of slowly evolving sites results in a robustly supported monophyletic Brachiopoda and Inarticulata (Linguliformea+Craniiformea), which is regarded as the most likely topology for brachiopod interrelationships. The monophyly of Brachiopoda was further tested with microRNA-based phylogenetics, which are small, noncoding RNA genes whose presence and absence can be used to infer phylogenetic relationships. Two novel microRNAs were characterized supporting the monophyly of brachiopods. Congruence of the traditional molecular phylogenetic analysis, microRNAs, and morphological cladograms suggest that Brachiopoda is monophyletic with Phoronida as its likely sister group. Molecular clock analysis suggests that extant phoronids have a Paleozoic divergence despite their conservative morphology, and that the early brachiopod fossil record is robust, and is not affected by taphonomic factors relating to the late-Precambrian/early-Cambrian phosphogenic event.

The Evolution of Brachiopoda

“…It also has obvious implications for hypotheses about the evolution of the bivalved shell in brachiopods (Section 5.4). Later analyses have recovered the more traditional view that brachiopods and phoronids could be sister clades (Giribet et al 2000, Sperling et al 2011. Ongoing research (E.A.…”

“…Many researchers subsequently sequenced additional species, attempting to test the conclusions of Field and colleagues and establish an ever more robust and defensible phylogeny of all animals. These studies included at least one, sometimes two or three, brachiopod species, in part because of their mosaic of features, articulated so clearly by Hyman (Giribet et al 2000, Paps et al 2009, Sperling et al 2011. From these and other studies, the Lophotrochozoa (Halanych et al 1995) molluscs, annelids, bryozoans, phoronids, and brachiopods, deriving its name from morphological features of the lophophore and trochophore larvae.…”

“…Determining patterns of divergence among ancient lineages became popular initially on the basis of comparisons of sequences of 18S rRNA, and later with additional genes and improved analytical techniques. The molecular systematic approach is now the standard for investigating phylogenetic relationships among extant taxa (Sperling et al 2011, Cohen 2013, Giribet 2015. Most recently, next-generation sequencing techniques have allowed this field to take another major leap forward with technology that enables the rapid and relatively inexpensive reconstruction of evolutionary relationships among massive numbers of taxa using phylogenomic data (e.g., Hejnol et al 2009, Nesnidal et al 2013, Luo et al 2015.…”

A critical appraisal of the use of microRNA data in phylogenetics

“…Typically in these studies, the phylogeny is first estimated from some other source of data, and then the correspondence of the inferred tree to select miRNA families is discussed (e.g., refs. [23][24][25][26][27]]. …”

Bichir microRNA repertoire suggests a ray-finned fish affinity of Polypteriforme

“…miRNA sequences, which have been successfully applied to many metazoan phylogenetic studies Heimberg et al, 2010;Sperling et al, 2010;Campbell et al, 2011;Philippe et al, 2011;Rota-Stabelli et al, 2011;Sperling et al, 2011;Wiegmann et al, 2011;Helm et al, 2012;Lyson et al, 2012;Pisani et al, 2012;Fromm et al, 2013;Peterson et al, 2013;Tarver et al, 2013), have five properties making them among the most reliable phylogenetic markers: (i) identification of novel miRNAs does not necessarily require fully sequenced genome sequence, (ii) new lineage-specific miRNA families are continually added to metazoan genomes through time which makes them ideal as phylogenetic markers, (iii) low levels of secondary miRNA loss, (iv) rarity of substitutions to the mature miRNA sequence, and (v) almost impossible scenario of convergent evolution of miRNAs Tarver et al, 2013). Therefore, miRNAs should provide an alternative and valuable evidence for the evolutionary position of Polypteriformes.…”