Phylogenomic studies have improved understanding of deep metazoan phylogeny and show promise for resolving incongruences among analyses based on limited numbers of loci. One region of the animal tree that has been especially difficult to resolve, even with phylogenomic approaches, is relationships within Lophotrochozoa (the animal clade that includes molluscs, annelids, and flatworms among others). Lack of resolution in phylogenomic analyses could be due to insufficient phylogenetic signal, limitations in taxon and/or gene sampling, or systematic error. Here, we investigated why lophotrochozoan phylogeny has been such a difficult question to answer by identifying and reducing sources of systematic error. We supplemented existing data with 32 new transcriptomes spanning the diversity of Lophotrochozoa and constructed a new set of Lophotrochozoa-specific core orthologs. Of these, 638 orthologous groups (OGs) passed strict screening for paralogy using a tree-based approach. In order to reduce possible sources of systematic error, we calculated branch-length heterogeneity, evolutionary rate, percent missing data, compositional bias, and saturation for each OG and analyzed increasingly stricter subsets of only the most stringent (best) OGs for these five variables. Principal component analysis of the values for each factor examined for each OG revealed that compositional heterogeneity and average patristic distance contributed most to the variance observed along the first principal component while branch-length heterogeneity and, to a lesser extent, saturation contributed most to the variance observed along the second. Missing data did not strongly contribute to either.Additional sensitivity analyses examined effects of removing taxa with heterogeneous branch lengths, large amounts of missing data, and compositional heterogeneity. Although our analyses do at University of Oslo Library on September 26, 2016 http://sysbio.oxfordjournals.org/ Downloaded from 3 not unambiguously resolve lophotrochozoan phylogeny, we advance the field by reducing the list of viable hypotheses. Moreover, our systematic approach for dissection of phylogenomic data can be applied to explore sources of incongruence and poor support in any phylogenomic dataset.Keywords: Trochozoa, Spiralia, Mollusca, Nemertea, Annelida, Brachiopoda, Phoronida, Entoprocta, Platyzoa, Polyzoa, Bryozoa Understanding of deep phylogeny has improved with the application of phylogenomic approaches (e.g., Philippe et al. 2004Philippe et al. , 2005Matus et al. 2006; Delsuc et al. 2006; Dunn et al. 2008; Hejnol et al. 2009; Kocot et al. 2011;Smith et al. 2011;Struck et al. 2011;Zhong et al. 2011a;Ryan et al. 2013;Moroz et al. 2014, Torruella et al. 2015, Whelan et al. 2015.Nonetheless, some regions of the tree of life with short internodes, probably due to rapid diversification, still lack resolution. Relationships within Lophotrochozoa (Halanych et al. 1995) are one such example. Lophotrochozoa is a well-supported clade of invertebrates that includes Anneli...
Ambulacraria, comprising Hemichordata and Echinodermata, is closely related to Chordata, making it integral to understanding chordate origins and polarizing chordate molecular and morphological characters. Unfortunately, relationships within Hemichordata and Echinodermata have remained unresolved, compromising our ability to extrapolate findings from the most closely related molecular and developmental models outside of Chordata (e.g., the acorn worms Saccoglossus kowalevskii and Ptychodera flava and the sea urchin Strongylocentrotus purpuratus). To resolve long-standing phylogenetic issues within Ambulacraria, we sequenced transcriptomes for 14 hemichordates as well as 8 echinoderms and complemented these with existing data for a total of 33 ambulacrarian operational taxonomic units (OTUs). Examination of leaf stability values revealed rhabdopleurid pterobranchs and the enteropneust Stereobalanus canadensis were unstable in placement; therefore, analyses were also run without these taxa. Analyses of 185 genes resulted in reciprocal monophyly of Enteropneusta and Pterobranchia, placed the deep-sea family Torquaratoridae within Ptychoderidae, and confirmed the position of ophiuroid brittle stars as sister to asteroid sea stars (the Asterozoa hypothesis). These results are consistent with earlier perspectives concerning plesiomorphies of Ambulacraria, including pharyngeal gill slits, a single axocoel, and paired hydrocoels and somatocoels. The resolved ambulacrarian phylogeny will help clarify the early evolution of chordate characteristics and has implications for our understanding of major fossil groups, including graptolites and somasteroideans.
BackgroundSymbiotic relationships between microbes and their hosts are widespread and diverse, often providing protection or nutrients, and may be either obligate or facultative. However, the genetic mechanisms allowing organisms to maintain host-symbiont associations at the molecular level are still mostly unknown, and in the case of bacterial-animal associations, most genetic studies have focused on adaptations and mechanisms of the bacterial partner. The gutless tubeworms (Siboglinidae, Annelida) are obligate hosts of chemoautotrophic endosymbionts (except for Osedax which houses heterotrophic Oceanospirillales), which rely on the sulfide-oxidizing symbionts for nutrition and growth. Whereas several siboglinid endosymbiont genomes have been characterized, genomes of hosts and their adaptations to this symbiosis remain unexplored.ResultsHere, we present and characterize adaptations of the cold seep-dwelling tubeworm Lamellibrachia luymesi, one of the longest-lived solitary invertebrates. We sequenced the worm’s ~ 688-Mb haploid genome with an overall completeness of ~ 95% and discovered that L. luymesi lacks many genes essential in amino acid biosynthesis, obligating them to products provided by symbionts. Interestingly, the host is known to carry hydrogen sulfide to thiotrophic endosymbionts using hemoglobin. We also found an expansion of hemoglobin B1 genes, many of which possess a free cysteine residue which is hypothesized to function in sulfide binding. Contrary to previous analyses, the sulfide binding mediated by zinc ions is not conserved across tubeworms. Thus, the sulfide-binding mechanisms in sibgolinids need to be further explored, and B1 globins might play a more important role than previously thought. Our comparative analyses also suggest the Toll-like receptor pathway may be essential for tolerance/sensitivity to symbionts and pathogens. Several genes related to the worm’s unique life history which are known to play important roles in apoptosis, cell proliferation, and aging were also identified. Last, molecular clock analyses based on phylogenomic data suggest modern siboglinid diversity originated in 267 mya (± 70 my) support previous hypotheses indicating a Late Mesozoic or Cenozoic origins of approximately 50–126 mya for vestimentiferans.ConclusionsHere, we elucidate several specific adaptations along various molecular pathways that link phenome to genome to improve understanding of holobiont evolution. Our findings of adaptation in genomic mechanisms to reducing environments likely extend to other chemosynthetic symbiotic systems.
Meiofauna are important components of food webs and for nutrient exchange between the benthos and water column. Recent studies have focused on these communities in the Gulf of Mexico due to potential impacts of the Deepwater Horizon Oil Spill (DWHOS). In particular, intertidal meiofaunal communities from Mobile Bay and Dauphin Island, Alabama, were previously shown to shift from predominately metazoan taxa prior to DWHOS to a fungal-dominated community after the spill. However, knowledge of variability within these communities remains unknown. Herein, we used Illumina high-throughput amplicon sequencing to examine variation throughout a year for the same locations for which the organismal shift was noted. Sediment samples were collected bi-monthly for a year (July 2011-July 2012) from which the meiofaunal community was examined by sequencing the eukaryotic hypervariable V9 region of the 18S rRNA gene. Results showed that the presence of fungal taxa was limited within these communities, suggesting that previously reported acute impacts of the DWHOS on meiofauna were apparently short term. However, these meiofaunal communities show shifts in proportions of metazoan taxa compared to pre-spill samples. Whether this change is due to prolonged impacts of the spill or variation in community composition is unclear. Taxonomic variation within and between sampled locations throughout the study was observed, suggesting potential yearly variation in communities. Continued sampling over a longer timeframe will provide a more complete understanding of seasonality and variation within these communities. Such a baseline is required to assess future anthropogenic impacts.
Deep‐sea tubeworms (Annelida, Siboglinidae) represent dominant species in deep‐sea chemosynthetic communities (e.g. hydrothermal vents and cold methane seeps) and occur in muddy sediments and organic falls. Siboglinids lack a functional digestive tract as adults, and they rely on endosymbiotic bacteria for energy, making them of evolutionary and physiological interest. Despite their importance, inferred evolutionary history of this group has been inconsistent among studies based on different molecular markers. In particular, placement of bone‐eating Osedax worms has been unclear in part because of their distinctive biology, including harbouring heterotrophic bacteria as endosymbionts, displaying extreme sexual dimorphism and exhibiting a distinct body plan. Here, we reconstructed siboglinid evolutionary history using 12 newly sequenced transcriptomes. We parsed data into three data sets that accommodated varying levels of missing data, and we evaluate effects of missing data on phylogenomic inference. Additionally, several multispecies‐coalescent approaches and Bayesian concordance analysis (BCA) were employed to allow for a comparison of results to a supermatrix approach. Every analysis conducted herein strongly supported Osedax being most closely related to the Vestimentifera and Sclerolinum clade, rather than Frenulata, as previously reported. Importantly, unlike previous studies, the alternative hypothesis that frenulates and Osedax are sister groups to one another was explicitly rejected by an approximately unbiased (AU) test. Furthermore, although different methods showed largely congruent results, we found that a supermatrix method using data partitioning with site‐homogenous models potentially outperformed a supermatrix method using the CAT‐GTR model and multispecies‐coalescent approaches when the amount of missing data varies in a data set and when taxa susceptible to LBA are included in the analyses.
Reptiles and other non-mammalian vertebrates have transcriptionally active nucleated red blood cells. If blood transcriptomes can provide quantitative data to address questions relevant to molecular ecology, this could circumvent the need to euthanize animals to assay tissues. This would allow longitudinal sampling of animals' responses to treatments, as well as sampling of protected taxa. We developed and annotated blood transcriptomes from six reptile species. We found on average 25,000 proteins are being transcribed in the blood, and there is a CORE group of 9,282 orthogroups that are found in at least four of six species. In comparison to liver transcriptomes from the same taxa, approximately two-thirds of the orthogroups were found in both blood and liver; and a similar percentage of ecologically relevant gene groups (insulin and insulin-like signaling, electron transport chain, oxidative stress, glucocorticoid receptors) were found transcribed in both blood and liver. As a resource, we provide a user-friendly database of gene ids identified in each blood transcriptome. Although, on average 37% of reads mapped to hemoglobin, importantly, the majority of non-hemoglobin transcripts had sufficient depth (e.g., 97% at ≥10 reads) to be included in differential gene expression analysis. Thus, we demonstrate that RNAseq blood transcriptomes from a very small blood sample (<10 >μl) is a minimally invasive option in non-mammalian vertebrates for quantifying expression of a large number of ecologically relevant genes that would allow longitudinal sampling and sampling of protected populations.
BackgroundDespite extensive study on hemoglobins and hemocyanins, little is known about hemerythrin (Hr) evolutionary history. Four subgroups of Hrs have been documented, including: circulating Hr (cHr), myohemerythrin (myoHr), ovohemerythrin (ovoHr), and neurohemerythrin (nHr). Annelids have the greatest diversity of oxygen carrying proteins among animals and are the only phylum in which all Hr subgroups have been documented. To examine Hr diversity in annelids and to further understand evolution of Hrs, we employed approaches to survey annelid transcriptomes in silico.ResultsSequences of 214 putative Hr genes were identified from 44 annelid species in 40 different families and Bayesian inference revealed two major clades with strong statistical support. Notably, the topology of the Hr gene tree did not mirror the phylogeny of Annelida as presently understood, and we found evidence of extensive Hr gene duplication and loss in annelids. Gene tree topology supported monophyly of cHrs and a myoHr clade that included nHrs sequences, indicating these designations are functional rather than evolutionary.ConclusionsThe presence of several cHrs in early branching taxa suggests that a variety of Hrs were present in the common ancestor of extant annelids. Although our analysis was limited to expressed-coding regions, our findings demonstrate a greater diversity of Hrs among annelids than previously reported.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0933-z) contains supplementary material, which is available to authorized users.
High-quality genomic resources facilitate population-level and species-level comparisons to answer questions about behavioral ecology, morphological and physiological adaptations, as well as the evolution of genomic architecture. Squamate reptiles (lizards and snakes) are particularly diverse in characteristics that have intrigued evolutionary biologists, but high-quality genomic resources for squamates are relatively sparse. Lizards in the genus Sceloporus have a long history as important ecological, evolutionary, and physiological models, making them a valuable target for the development of genomic resources. We present a high-quality chromosome-level reference genome assembly, SceUnd1.0, (utilizing 10X Genomics Chromium, HiC, and PacBio data) and tissue/developmental stage transcriptomes for the Eastern Fence Lizard, Sceloporus undulatus. We performed synteny analysis with other available squamate chromosome-level assemblies to identify broad patterns of chromosome evolution including the fusion of micro- and macrochromosomes in S. undulatus. Using this new S. undulatus genome assembly we conducted reference-based assemblies for 34 other Sceloporus species to improve draft nuclear genomes assemblies from 1% coverage to 43% coverage on average. Across these species, typically >90% of reads mapped for species within 20 million years divergence from S. undulatus, this dropped to 75% reads mapped for species at 35 million years divergence. Finally we use RNAseq and whole genome resequencing data to compare the three assemblies as references, each representing an increased level of sequencing, cost and assembly efforts: Supernova Assembly with data from10X Genomics Chromium library; HiRise Assembly that added data from HiC library; and PBJelly Assembly that added data from PacBio sequencing. We found that the Supernova Assembly contained the full genome and was a suitable reference for RNAseq, but the chromosome-level scaffolds provided by the addition of the HiC data allowed the reference to be used for other whole genome analysis, including synteny and whole genome association mapping analyses. The addition of PacBio data provided negligible gains. Overall, these new genomic resources provide valuable tools for advanced molecular analysis of an organism that has become a model in physiology and evolutionary ecology.
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