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Tunicate bulb size variation in monocots explained by temperature and phenology

Plants bulbs are modified shoot systems comprised of short internodes with apical bud(s) surrounded by layers of leaf bases. Bulb diameters can vary greatly, with overall bulb size playing a role in flower formation as well as resource allocation. Despite the importance of bulb size to the overall fitness of an individual, evolutionary and ecological aspects of this trait have been almost completely neglected. Examining over 2500 herbarium vouchers for 115 selected species, we analyzed monocot tunicate bulb size within a phylogenetic context in order to investigate its evolutionary significance. We recorded two bulb diameter optima and observed that as bulb size increases taxa inhabit warmer areas with less temperature seasonality. Furthermore, we found that hysteranthous taxa, a habit where leaves emerge separately from flowers, exhibit overall larger bulbs potentially due to reliance upon belowground stored resources to flower rather than on current environmental inputs. This work highlights the importance of including the belowground portion of plants into ecological and evolutionary studies in order to gain a more complete understanding of the evolution of plant forms and functions.

Data from: An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models

BACKGROUND: Tunicates have been recently revealed to be the closest living relatives of vertebrates. Yet, with more than 2500 described species, details of their evolutionary history are still obscure. From a molecular point of view, tunicate phylogenetic relationships have been mostly studied based on analyses of 18S rRNA sequences, which indicate several major clades at odds with the traditional class-level arrangements. Nonetheless, substantial uncertainty remains about the phylogenetic relationships and taxonomic status of key groups such as the Aplousobranchia, Appendicularia, and Thaliacea. RESULTS: Thirty new complete 18S rRNA sequences were acquired from previously unsampled tunicate species, with special focus on groups presenting high evolutionary rate. The updated 18S rRNA dataset has been aligned with respect to the constraint on homology imposed by the rRNA secondary structure. A probabilistic framework of phylogenetic reconstruction was adopted to accommodate the particular evolutionary dynamics of this ribosomal marker. Detailed Bayesian analyses were conducted under the non-parametric CAT mixture model accounting for site-specific heterogeneity of the evolutionary process, and under RNA-specific doublet models accommodating the occurrence of compensatory substitutions in stem regions. Our results support the division of tunicates into three major clades: 1) Phlebobranchia + Thaliacea + Aplousobranchia, 2) Appendicularia, and 3) Stolidobranchia, but the position of Appendicularia could not be firmly resolved. Our study additionally reveals that most Aplousobranchia evolve at extremely high rates involving changes in secondary structure of their 18S rRNA, with the exception of the family Clavelinidae, which appears to be slowly evolving. This extreme rate heterogeneity precluded resolving with certainty the exact phylogenetic placement of Aplousobranchia. Finally, the best fitting secondary-structure and CAT-mixture models suggest a sister-group relationship between Salpida and Pyrosomatida within Thaliacea. CONCLUSION: An updated phylogenetic framework for tunicates is provided based on phylogenetic analyses using the most realistic evolutionary models currently available for ribosomal molecules and an unprecedented taxonomic sampling. Detailed analyses of the 18S rRNA gene allowed a clear definition of the major tunicate groups and revealed contrasting evolutionary dynamics among major lineages. The resolving power of this gene nevertheless appears limited within the clades composed of Phlebobranchia + Thaliacea + Aplousobranchia and Pyuridae + Styelidae, which were delineated as spots of low resolution. These limitations underline the need to develop new nuclear markers in order to further resolve the phylogeny of this keystone group in chordate evolution.

Data from: Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate

Genomes of animals as different as sponges and humans show conservation of global architecture. Here we show that multiple genomic features including transposon diversity, developmental gene repertoire, physical gene order, and intron-exon organization are shattered in the tunicate Oikopleura, belonging to the sister group of vertebrates and retaining chordate morphology. Ancestral architecture of animal genomes can be deeply modified and may therefore be largely nonadaptive. This rapidly evolving animal lineage thus offers unique perspectives on the level of genome plasticity. It also illuminates issues as fundamental as the mechanisms of intron gain.

Data from: Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny

BACKGROUND: Tunicates represent a key metazoan group as the sister-group of vertebrates within chordates. The six complete mitochondrial genomes available so far for tunicates have revealed distinctive features. Extensive gene rearrangements and particularly high evolutionary rates have been evidenced with regard to other chordates. This peculiar evolutionary dynamics has hampered the reconstruction of tunicate phylogenetic relationships within chordates based on mitogenomic data. RESULTS: In order to further understand the atypical evolutionary dynamics of the mitochondrial genome of tunicates, we determined the complete sequence of the solitary ascidian Herdmania momus. This genome from a stolidobranch ascidian presents the typical tunicate gene content with 13 protein-coding genes, 2 rRNAs and 24 tRNAs which are all encoded on the same strand. However, it also presents a novel gene arrangement, highlighting the extreme plasticity of gene order observed in tunicate mitochondrial genomes. Probabilistic phylogenetic inferences were conducted on the concatenation of the 13 mitochondrial protein-coding genes from representatives of major metazoan phyla. We show that whereas standard homogeneous amino acid models support an artefactual sister position of tunicates relative to all other bilaterians, the CAT and CAT+BP site- and time-heterogeneous mixture models place tunicates as the sister-group of vertebrates within monophyletic chordates. Moreover, the reference phylogeny indicates that tunicate mitochondrial genomes have experienced a drastic acceleration in their evolutionary rate that equally affects protein-coding and ribosomal-RNA genes. CONCLUSION: This is the first mitogenomic study supporting the new chordate phylogeny revealed by recent phylogenomic analyses. It illustrates the beneficial effects of an increased taxon sampling coupled with the use of more realistic amino acid substitution models for the reconstruction of animal phylogeny.

Data from: Tunicates and not cephalochordates are the closest living relatives of vertebrates

Tunicates or urochordates (appendicularians, salps and sea squirts), cephalochordates (lancelets) and vertebrates (including lamprey and hagfish) constitute the three extant groups of chordate animals. Traditionally, cephalochordates are considered as the closest living relatives of vertebrates, with tunicates representing the earliest chordate lineage. This view is mainly justified by overall morphological similarities and an apparently increased complexity in cephalochordates and vertebrates relative to tunicates. Despite their critical importance for understanding the origins of vertebrates, phylogenetic studies of chordate relationships have provided equivocal results. Taking advantage of the genome sequencing of the appendicularian Oikopleura dioica, we assembled a phylogenomic data set of 146 nuclear genes (33,800 unambiguously aligned amino acids) from 14 deuterostomes and 24 other slowly evolving species as an outgroup. Here we show that phylogenetic analyses of this data set provide compelling evidence that tunicates, and not cephalochordates, represent the closest living relatives of vertebrates. Chordate monophyly remains uncertain because cephalochordates, albeit with a non-significant statistical support, surprisingly grouped with echinoderms, a hypothesis that needs to be tested with additional data. This new phylogenetic scheme prompts a reappraisal of both morphological and palaeontological data and has important implications for the interpretation of developmental and genomic studies in which tunicates and cephalochordates are used as model animals.

Data from: Accelerated evolutionary rate of housekeeping genes in tunicates

Phylogenomics has recently revealed that tunicates represent the sister-group of vertebrates in the newly defined clade Olfactores. However, phylogenomic and comparative genomic studies have also suggested that tunicates are characterized by an elevated rate of molecular evolution and a high degree of genomic divergence. Despite the recurrent interest in the group, the picture of tunicate peculiar evolutionary dynamics is still fragmentary, as it mainly lies in studies focusing on only a few model species. In order to expand the available genomic data for the group, we used the high-throughput 454 technology to sequence the partial transcriptome of a previously unsampled tunicate, Microcosmus squamiger. This allowed us to get further insights into tunicate-accelerated evolution through a comparative analysis based on pertinent phylogenetic markers, i.e., a core of 35 housekeeping genes conserved across bilaterians. Our results showed that tunicates evolved on average about two times faster than the other chordates, yet the degree of this acceleration varied extensively upon genes and upon lineages. Appendicularia and Aplousobranchia were detected as the most divergent groups which were also characterized by highly heterogeneous substitution rates across genes. Finally, an estimation of the d (N)/d (S) ratio in three pairs of closely related taxa within Olfactores did not reveal strong differences between the tunicate and vertebrate lineages suggesting that for this set of housekeeping genes, the accelerated evolution of tunicates is plausibly due to an elevated mutation rate rather than to particular selective effects.

opennotspecifiedDec 2013View details →

FIGURE 2. A, B in Ascidia subterranea sp. nov. (Phlebobranchia: Ascidiidae), a new tunicate belonging to the A. sydneiensis Stimpson, 1855 group, found as burrow associate of Axiopsis serratifrons A. Milne-Edwards, 1873 (Decapoda: Axiidae) on Derawan Island, Indonesia

FIGURE 2. A, B Ascidia subterranea sp. nov. (MNHN P5 ASC.A 416/2), tunic removed seen from the left (A) and right (B) side respectively. C, D Corresponding drawings to the photographs in A and B. an—anus, as—atrial siphon, gd—gonadal ducts, ht(?)—enlarged blood vessel, probably the heart, in—intestine, mb—muscle belt, ov—ovary, re—rectum, sto—stomach

opennotspecifiedDec 2013View details →

FIGURE 1. A in Ascidia subterranea sp. nov. (Phlebobranchia: Ascidiidae), a new tunicate belonging to the A. sydneiensis Stimpson, 1855 group, found as burrow associate of Axiopsis serratifrons A. Milne-Edwards, 1873 (Decapoda: Axiidae) on Derawan Island, Indonesia

FIGURE 1. A Opening of the burrow of Axiopsis serratifrons, with anterior end of the shrimp visible, surrounded by the narrow leafed morph of Halodule uninervis. B Tunic papillae (tpa) of Ascidia subterranea sp. nov. (MNHN P5 ASC.A 416/2). C Schematic representation of the habitat of Ascidia subterranea sp. nov., showing the position of the living tunicate on the burrow roof. Also shown are the pair of shrimps, and associated bivalves, gastropods and polychaetes. Three alternative (all of them speculative) positions for the siphon are depicted.

opennotspecifiedDec 2017View details →

FIGURE 2. Fimbrora calsubia. A, branchial tissue stained with haemalum. B, body without tunic showing the atrial aperture. Scale bars 1 in Deep-sea ascidians from Papua New Guinea

FIGURE 2. Fimbrora calsubia. A, branchial tissue stained with haemalum. B, body without tunic showing the atrial aperture. Scale bars 1cm.

FIGURE 4 in Pelagic tunicates (Appendicularia and Thaliacea) of Sri Lanka: two first records with an annotated checklist

FIGURE 4. Schematic diagrams of Sri Lankan pelagic tunicates, showing the general morphology of their families (A–H): the lateral view of mature individuals of Fritillariidae (A) and Oikopleuridae (B); gonozooid (C) and degenerated oozooid / nurse (D) of Doliolidae; dorsal view of a solitary zooid (E) and aggregate zooid (F) of Salpidae; a blastozooid (G) and sagittal section of a colony (H) of Pyrosomatidae. Adapted from Claus (1883), Esnal (1981), Barnes et al. (1993) and Sri Lankan specimens. Note: The tails of appendicularian diagrams have been rotated through 90º for clarity.

FIGURE 3 in Pelagic tunicates (Appendicularia and Thaliacea) of Sri Lanka: two first records with an annotated checklist

FIGURE 3. Re-reported salp, Pegea confoederata, to Sri Lanka in "Waya-jel-Survey" in preserved form (A–D): a colony of zooids (A); embryo (B); aggregate zooid (C); solitary zooid (D). E—endostyle; G—gill; N—nucleus; S—stolon. Scales: B = 5 mm; C & D = 8 mm; A = 20 mm.

FIGURE 2 in Pelagic tunicates (Appendicularia and Thaliacea) of Sri Lanka: two first records with an annotated checklist

FIGURE 2. Firstly reported pelagic tunicates to Sri Lanka in "Waya-jel-Survey" (A–F): a live colony of Pyrostremma spinosum near to the sea surface (A & B), and an illustration of its blastozooid (C); Thalia sibogae solitary zooid in preserved form (D), ventral view of medioventral projections (E), and an illustration of its posterior part (F). a—anus; ap—atrial palp; dmp— dorsal medioventral projection; e—endostyle; es—excurrent/buccal siphon; g—ganglion; is—incurrent/atrial siphon; lp—lateral projection; n—nucleus; o—ovary; pb—pharyngeal basket; pp—posterior projection; sl—stolon; sm—stomach; t—testis; vmp—ventral medioventral projection. Scales: E = 0.5 mm; C, D, F = 1 mm; A & B = 0.4 m. Images A & B by Franco Banfi from off Mirissa, Sri Lanka

FIGURE 1 in Pelagic tunicates (Appendicularia and Thaliacea) of Sri Lanka: two first records with an annotated checklist

FIGURE 1. Sampling localities of pelagic tunicates within the three regions of Sri Lankan Exclusive Economic Zone (EEZ) denoted by BBR (Bay of Bengal Region), LSR (Laccadive Sea Region) and IOR (Indian Ocean Region). Source of the map: Maritime Boundaries Geodatabase, Flanders Marine Institute (https://www.marineregions.org/). Remarks of each sampling station (St.) indicated by open circles are in Table 1

FIGURE 7 in A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

FIGURE 7. Results of plate assay (A) and zymographic analysis (B) for cellulase activity of Polydora tunicola sp. nov. Haloes (A: destained areas) and destained bands (B: arrowheads) indicate the cellulose decomposition (exhibition of cellulase activity). PC = positive control (crystalline style of a brackish water clam Corbicula japonica), NC = negative control.

FIGURE 6 in A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

FIGURE 6. Maximum likelihood tree inferred from concatenated sequences of nuclear 18S and 28S and mitochondrial 16S rRNA gene sequences of Polydora species obtained in this study and from DDBJ/EMBL/GenBank database (Table 1). The gene sequences obtained in this study are highlighted in boldface. SH-aLRT/approximate Bayes support/ultrafast bootstrap support values of ≥80%/≥0.95/≥95%, respectively, are given beside the respective nodes. Nodes with red circles indicate triple high support values of SH-aLRT ≥ 80, approximate Bayes support ≥ 0.95, and ultrafast bootstrap support ≥ 95. The scale bar represents the number of substitutions per site. Sequences of Dipolydora species are used for outgroup rooting. The symbols at the left of the species names indicate the lifestyle based on the available information (Table 1).

FIGURE 5 in A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

FIGURE 5. Micro-CT images of the host ascidian. A: three-dimensional (3D) reconstructed image of three U-shaped burrows of Polydora tunicola sp. nov. B: two-dimensional reconstructed images of three U-shaped burrows of Polydora tunicola sp. nov. extracted from tomographic data. Arrowheads of figures A and B indicate the apertures of the burrows. C–E: Cross-sectional image of the host. Arrowheads indicate the boreholes of Polydora tunicola sp. nov. in the ascidian tunic. Scale bars = 10 mm.

FIGURE 4 in A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

FIGURE 4. Polydora tunicola sp. nov. A: palps and mud tubes of Polydora tunicola sp. nov. protruding from their burrows in the tunics of the sessile ascidian Polycarpa cf. cryptocarpa kroboja. B: closeup of palps and mud tubes of Polydora tunicola sp. nov. C, D: tubes of Polydora tunicola sp. nov. concentrated on near siphons of the ascidians. E: juvenile of Polydora tunicola sp. nov. (arrowhead) constructing a mucous tube on the siphons of the ascidians but not yet bore into the tunic. F: cross-section of a host ascidian showing many pairs of boreholes filled with mud tubes (arrowheads) of Polydora tunicola sp. nov. in the host tunic. Photo by O. Hoshino (A–E) and H. Abe (F).

FIGURE 1 in A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

FIGURE 1. Maps showing sampling locations of Polydora tunicola sp. nov. A: Japan. B: Izu-Oshima Island and its vicinity.

FIGURE 2 in A novel symbiotic relationship between ascidians and a new tunic-boring polychaete (Annelida: Spionidae: Polydora)

FIGURE 2. Polydora tunicola sp. nov. Light micrographs showing the morphology of preserved specimens (holotype: NSMTPol H-855). A: entire body. B: anterior end, dorsal view. C: anterior end, lateral view. D: posterior end, lateral view. E: posterior end, dorsal view. F: posterior end, ventral view. Scale bars: (A) = 5 mm; (B–C) = 1 mm; (D–F) = 500 μm.