Mitochondrial Genome Evolution in Annelida—A Systematic Study on Conservative and Variable Gene Orders and the Factors Influencing its Evolution

The mitochondrial genomes of Bilateria are relatively conserved in their protein-coding, rRNA, and tRNA gene complement, but the order of these genes can range from very conserved to very variable depending on the taxon. The supposedly conserved gene order of Annelida has been used to support the placement of some taxa within Annelida. Recently, authors have cast doubts on the conserved nature of the annelid gene order. Various factors may influence gene order variability including, among others, increased substitution rates, base composition differences, structure of noncoding regions, parasitism, living in extreme habitats, short generation times, and biomineralization. However, these analyses were neither done systematically nor based on well-established reference trees. Several focused on only a few of these factors and biological factors were usually explored ad-hoc without rigorous testing or correlation analyses. Herein, we investigated the variability and evolution of the annelid gene order and the factors that potentially influenced its evolution, using a comprehensive and systematic approach. The analyses were based on 170 genomes, including 33 previously unrepresented species. Our analyses included 706 different molecular properties, 20 life-history and ecological traits, and a reference tree corresponding to recent improvements concerning the annelid tree. The results showed that the gene order with and without tRNAs is generally conserved. However, individual taxa exhibit higher degrees of variability. None of the analyzed life-history and ecological traits explained the observed variability across mitochondrial gene orders. In contrast, the combination and interaction of the best-predicting factors for substitution rate and base composition explained up to 30% of the observed variability. Accordingly, correlation analyses of different molecular properties of the mitochondrial genomes showed an intricate network of direct and indirect correlations between the different molecular factors. Hence, gene order evolution seems to be driven by molecular evolutionary aspects rather than by life history or ecology. On the other hand, variability of the gene order does not predict if a taxon is difficult to place in molecular phylogenetic reconstructions using sequence data or not. We also discuss the molecular properties of annelid mitochondrial genomes considering canonical views on gene evolution and potential reasons why the canonical views do not always fit to the observed patterns without making some adjustments.publishedVersio

Inferring the phylogeny of problematic metazoan taxa using mitogenomic and phylogenomic data

The evolutionary origin and the phylogeny of higher metazoan taxa is still under debate although considerable progress has been made in the past 20 years. Metazoa represents a monophyletic group of highly diverse animals including Bilateria, Cnidaria, Porifera, Ctenophores, and Placozoa. Bilateria comprises the majority of metazoans and consists of three major clades: Deuterostomia, Spiralia (= Lophotrochozoa sensu lato), and Ecdysozoa, whereas the sister group taxa Spiralia and Ecdyzozoa form the monophyletic clade Protostomia. Molecular data have profoundly changed the view of the bilaterian tree of life. One of the main questions concerning bilaterian phylogeny is the on-going debate about the evolution of complexity in Bilateria. It was assumed that the last common ancestor of Deuterostomia, Ecdysozoa and Spiralia had a segmented and coelomate body organization resembling that of an annelid. On the contrary, the traditional view is the evolution of Bilateria from a simple body organization towards more complex forms, assuming that the last common ancestor of Bilateria resembles a platyhelminth-like animal without coelomic cavities and segmentation. To resolve this question, it is necessary to unravel the phylogenetic relationships within Bilateria. By using mitogenomic and phylogenomic data, this thesis had a major contribution to clarify phylogenetic relationships within problematic metazoan taxa: (1) the phylogeny of Deuterostomia, (2) the questionable monophyly of Platyzoa, and first assumptions concerning the phylogeny of Gnathostomulida, Gastrotricha and Polycladida, (3) phylogenetic relationships within annelid taxa, especially Terebelliformia, Diurodrilidae, and Syllidae, with new insights into the evolution of mitochondrial gene order, and (4) new insights into the evolution of annelids, especially the interstitial ones, as well as the colonization of the interstitial realm

Syllidae mitochondrial gene order is unusually variable for Annelida.

Complete mitochondrial genomes of five syllids (Streptosyllis sp., Eusyllis blomstrandi, Myrianida brachycephala, Typosyllis antoni and Typosyllis sp.) have been obtained using Illumina sequencing. Together with two previous studied taxa (Ramisyllis multicaudata and Trypanobia cryptica), the analysed sequences represent most of the main lineages within the family Syllidae (Anoplosyllinae, Eusyllinae, Autolytinae and Syllinae). The genomic features, gene order and phylogenetic relationships are examined. Unusual for annelids, syllid mitochondrial genomes are highly variable in their gene order. Considering genomic features, such as length, skewness, gene content, and codon bias, most similar to the rest of annelids are the genomes of E. blomstrandi and M. brachycephala, while Streptosyllis sp. and the analysed sylline taxa (R. multicaudata, T. cryptica, T. antoni and Typosyllis sp.) are the most dissimilar. Two methionine tRNA's (trnM) have been found in T. antoni and Typosyllis sp. The mt genomes of these latter taxa are the longest with numerous non-coding regions. The 13 protein coding genes, as well as the rRNA's are used to perform phylogenetic analyses that recovered the relationships within the family explored before by previous authors. The gene order in Syllidae shows very different patterns. E. blomstrandi and M. prolifera show a similar pattern to the one found in Pleistoannelida; however this might have changed at least twice within Syllidae: in Streptosyllis sp. and within Syllinae. All analysed Syllinae show different gene orders, thereby illustrating more variability as all other pleistoannelids analysed so far. The information provided herein allows a more accurate reconstruction of the possible evolutionary scenarios in Syllidae

Syllidae mitochondrial gene order is unusually variable for Annelida

Complete mitochondrial genomes of five syllids (Streptosyllis sp., Eusyllis blomstrandi, Myrianida brachycephala, Typosyllis antoni and Typosyllis sp.) have been obtained using Illumina sequencing. Together with two previous studied taxa (Ramisyllis multicaudata and Trypanobia cryptica), the analysed sequences represent most of the main lineages within the family Syllidae (Anoplosyllinae, Eusyllinae, Autolytinae and Syllinae). The genomic features, gene order and phylogenetic relationships are examined. Unusual for annelids, syllid mitochondrial genomes are highly variable in their gene order. Considering genomic features, such as length, skewness, gene content, and codon bias, most similar to the rest of annelids are the genomes of E. blomstrandi and M. brachycephala, while Streptosyllis sp. and the analysed sylline taxa (R. multicaudata, T. cryptica, T. antoni and Typosyllis sp.) are the most dissimilar. Two methionine tRNA's (trnM) have been found in T. antoni and Typosyllis sp. The mt genomes of these latter taxa are the longest with numerous non-coding regions. The 13 protein coding genes, as well as the rRNA's are used to perform phylogenetic analyses that recovered the relationships within the family explored before by previous authors. The gene order in Syllidae shows very different patterns. E. blomstrandi and M. prolifera show a similar pattern to the one found in Pleistoannelida; however this might have changed at least twice within Syllidae: in Streptosyllis sp. and within Syllinae. All analysed Syllinae show different gene orders, thereby illustrating more variability as all other pleistoannelids analysed so far. The information provided herein allows a more accurate reconstruction of the possible evolutionary scenarios in Syllidae.This study is a contribution of the project “Macroevolutionary transitions in Syllidae” CGL2015-63593-P MINECO/FEDER, UE. MTA was supported by the “José Castillejo” fellow by MINECO (Ministerio de Economía y Competitividad, Spanish Government), reference C2008-00006, for a research stay at the University of Leipzig (Germany). CB is supported by a “Ramón y Cajal” fellow by the MINECO, project no RYC-2014-15615. THS acknowledges support by the German Science Foundation (DFG STR-683/6-1, DFG STR-683/6-2 and DFG STR-683/8-1).Peer Reviewe

Data from: The evolution of annelids reveals two adaptive routes to the interstitial realm

Many animals permanently inhabit the marine interstitium, the space between sand grains [ 1, 2 ]. Different evolutionary scenarios may explain the existence of interstitial animals [ 3, 4 ]. These scenarios include (1) that the interstitial realm is the ancestral habitat of bilaterians [ 5, 6 ], (2) that interstitial taxa evolved from larger ancestors by miniaturization, or (3) progenesis [ 3 ]. The first view mirrors the former hypothesis that interstitial annelids, called archiannelids, were at the base of the annelid radiation [ 7 ]. Based on morphological data, however, progenesis is generally favored for interstitial annelids today [ 3, 4, 8 ]. Herein, our phylogenomic approach revealed that interstitial archiannelids are robustly placed into two groups nested within the annelid tree. Evolution of the first group comprising among others Dinophilidae is best explained by progenesis. In contrast, the second group comprising Protodrilida and Polygordiidae appears to have evolved by stepwise miniaturization adapting from coarser to finer sediments. Thus, in addition to progenesis [ 3, 4 ], miniaturization, thought to be too slow for an adaptation to the interstitium [ 3 ], is an important second route allowing adaptation to interstitial environments. Both progenesis and miniaturization should be considered when investigating evolution of interstitial taxa [ 1, 3 ]

Struck2015_CurrentBiology_InterstitialAnnelida

his file contains the concatenated datasets used for phylogenetic analyses in phylip-format in the folder „Datasets“and additional results in the pdf-file „ExtraResults“ with an explanation of the results. The datasets are named in correspondence to the numbers in Table 1 of the manuscript in Current Biology by Struck and co-authors entitled „The evolution of annelids reveals two adaptive routes to the interstitial realm“. The names of the dataset files are as follows: Dataset_1.phy Dataset_2.phy Dataset_3.phy Dataset_4.phy Dataset_5.phy Dataset_6.phy Dataset_7.phy Dataset_8.phy Dataset_9.phy Dataset_10.phy Dataset_11.phy Dataset_12.phy Dataset_13.phy Dataset_14.phy Dataset_15.phy Dataset_16.phy Dataset_17.phy Dataset_18.phy Dataset_19.phy Dataset_20.phy Dataset_21.phy Dataset_22.phy Dataset_23.phy Dataset_24.ph

Data from: Platyzoan paraphyly based on phylogenomic data supports a non-coelomate ancestry of Spiralia

Based on molecular data three major clades have been recognized within Bilateria: Deuterostomia, Ecdysozoa and Spiralia. Within Spiralia, small-sized and simply organized animals such as flatworms, gastrotrichs and gnathostomulids have recently been grouped together as Platyzoa. However, the representation of putative platyzoans was low in the respective molecular phylogenetic studies, in terms of both, taxon number and sequence data. Furthermore, increased substitution rates in platyzoan taxa raised the possibility that monophyletic Platyzoa represents an artefact due to long-branch attraction. In order to overcome such problems, we employed a phylogenomic approach, thereby substantially increasing i) the number of sampled species within Platyzoa and ii) species-specific sequence coverage in datasets of up to 82,162 amino acid positions. Using established and new measures (long-branch score) we disentangled phylogenetic signal from misleading effects such as long-branch attraction. In doing so, our phylogenomic analyses did not recover a monophyletic origin of platyzoan taxa that, instead, appeared paraphyletic with respect to the other spiralians. Platyhelminthes and Gastrotricha formed a monophylum, which we name Rouphozoa. To the exclusion of Gnathifera, Rouphozoa and all other spiralians represent a monophyletic group, which we name Platytrochozoa. Platyzoan paraphyly suggests that the last common ancestor of Spiralia was a simple-bodied organism lacking coelomic cavities, segmentation and complex brain structures, and that more complex animals such as annelids evolved from such a simply organized ancestor. This conclusion contradicts alternative evolutionary scenarios proposing an annelid-like ancestor of Bilateria and Spiralia and several independent events of secondary reduction