Rapid microevolution during recent range expansion to harsh environments

Background: Adaptive evolution is one of the crucial mechanisms for organisms to survive and thrive in new environments. Recent studies suggest that adaptive evolution could rapidly occur in species to respond to novel environments or environmental challenges during range expansion. However, for environmental adaptation, many studies successfully detected phenotypic features associated with local environments, but did not provide ample genetic evidence on microevolutionary dynamics. It is therefore crucial to thoroughly investigate the genetic basis of rapid microevolution in response to environmental changes, in particular on what genes and associated variation are responsible for environmental challenges. Here, we genotyped genome-wide gene-associated microsatellites to detect genetic signatures of rapid microevolution of a marine tunicate invader, Ciona robusta, during recent range expansion to the harsh environment in the Red Sea. Results: The Red Sea population was significantly differentiated from the other global populations. The genome-wide scan, as well as multiple analytical methods, successfully identified a set of adaptive genes. Interestingly, the allele frequency largely varied at several adaptive loci in the Red Sea population, and we found significant correlations between allele frequency and local environmental factors at these adaptive loci. Furthermore, a set of genes were annotated to get involved in local temperature and salinity adaptation, and the identified adaptive genes may largely contribute to the invasion success to harsh environments. Conclusions: All the evidence obtained in this study clearly showed that environment-driven selection had left detectable signatures in the genome of Ciona robusta within a few generations. Such a rapid microevolutionary process is largely responsible for the harsh environmental adaptation and therefore contributes to invasion success in different aquatic ecosystems with largely varied environmental factors

Deep Sequencing of Mixed Total DNA without Barcodes Allows Efficient Assembly of Highly Plastic Ascidian Mitochondrial Genomes

Ascidians or sea squirts form a diverse group within chordates, which includes a few thousand members of marine sessile filter-feeding animals. Their mitochondrial genomes are characterized by particularly high evolutionary rates and rampant gene rearrangements. This extreme variability complicates standard polymerase chain reaction (PCR) based techniques for molecular characterization studies, and consequently only a few complete Ascidian mitochondrial genome sequences are available. Using the standard PCR and Sanger sequencing approach, we produced the mitochondrial genome of Ascidiella aspersa only after a great effort. In contrast, we produced five additional mitogenomes (Botrylloides aff. leachii, Halocynthia spinosa, Polycarpa mytiligera, Pyura gangelion, and Rhodosoma turcicum) with a novel strategy, consisting in sequencing the pooled total DNA samples of these five species using one Illumina HiSeq 2000 flow cell lane. Each mitogenome was efficiently assembled in a single contig using de novo transcriptome assembly, as de novo genome assembly generally performed poorly for this task. Each of the new six mitogenomes presents a different and novel gene order, showing that no syntenic block has been conserved at the ordinal level (in Stolidobranchia and in Phlebobranchia). Phylogenetic analyses support the paraphyly of both Ascidiacea and Phlebobranchia, with Thaliacea nested inside Phlebobranchia, although the deepest nodes of the Phlebobranchia–Thaliacea clade are not well resolved. The strategy described here thus provides a cost-effective approach to obtain complete mitogenomes characterized by a highly plastic gene order and a fast nucleotide/amino acid substitution rate

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

<p>Abstract</p> <p>Background</p> <p>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.</p> <p>Results</p> <p>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.</p> <p>Conclusion</p> <p>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.</p

Uspostavljanje popisa morskih invazivnih vrsta u ESENIAS području: sadašnja situacija i buduća očekivanja

In this study we present a list of invasive/potential invasive alien species in the East and South European Network for Invasive Alien Species (ESENIAS) countries with marine borders. The species were classified according to the existing literature and experts’ judgment, as established, casual, invasive and expected. Finally, factsheets were compiled for ten species of high importance based on their expanding/invading character. Of the 160 species comprising the list, 149 were already present in the ESENIAS countries, while eleven were invasive species either present in the Mediterranean or in other European Seas, likely to be recorded in the ESENIAS countries. The majority of the species were of Red Sea/IndoPacific origin (97 species; 60.6%). Italy, Turkey and Greece were the countries with the highest representation of species (159, 152 and 139 species respectively), due to their extended coastline and the number of scholars working on marine invasive species. The highest number of established species was recorded in Turkey (116 species), whereas in Italy and Greece the most numerous species were the “expected” ones (85 and 48 species, respectively). The eastern Adriatic Sea countries (i.e. Albania, Croatia, Montenegro and Slovenia) had generally low numbers of species in this list, many of which are still “expected” to arrive from the neighbouring countries of Greece and Italy. Finally, the most frequently potential pathway was transfer stowaways (ship ballast water: 41 cases; ship hull fouling: 55), whereas unaided spread of Lessepsian immigrants followed (95 cases). This list is intended to serve as an early warning system that through horizon scanning process would assist ESENIAS countries to prioritise invasive alien species, their pathways and the areas of higher likelihood to appear, in order to take management measures.U ovom radu predstavljamo popis invazivnih i potencijalno invazivnih vrsta na istoku i jugu Europske mreže za invazivne vrste (ESENIAS) u zemljama s morskim granicama. Vrste su klasificirane prema postojećoj literaturi i procjeni stručnjaka, pa su tako utvrđene grupe povremenih, invazivnih i očekivanih vrsta. Podaci su dati za deset vrsta čija se važnost temelji na njihovom širenju i invazivnom karakteru. Od 160 vrsta koje sadrži popis, 148 je već bilo prisutno u ESENIAS zemljama, dok je 9 invazivnih vrsta bilo prisutno u Sredozemnom ili u drugim europskim morima, a vjerojatno je da će se zabilježiti i u zemljama udruženim u ESENIAS. Većina vrsta je bile iz Crvenog mora / indopacifičkog podrijetla (97 vrsta, 60,6%). Italija, Turska i Grčka su zemlje s najvišom zastupljenošću vrsta (159, 152 i 139), zbog njihove proširene obale i broja znanstvenika koji rade na morskim invazivnim vrstama. Najveći broj utvrđenih vrsta zabilježen je u Turskoj (116 vrsta), dok su u Italiji i Grčkoj najbrojnije vrste bile “očekivane” (85 i 48 vrsta, respektivno). Istočne zemlje Jadranskog mora (npr. Albanija, Hrvatska, Crna Gora i Slovenija) imale su općenito nizak broj vrsta na ovom popisu, od kojih mnoge još “očekujemo” da pristignu iz susjednih zemalja: Grčke i Italije. Konačno, najčešće su potencijalni putovi bili „transferni putnici“ (balastna voda broda: 41 slučaj, obraštaj brodskog trupa: 55), dok je slijedilo i širenje lesepsijskih migranata (95 slučajeva). Ovaj popis je namijenjen da služi kao sustav ranog upozorenja koji bi kroz proces skeniranja pomogao državama ESENIAS da daju prioritet invazivnim stranim vrstama, njihovim putovima i područjima veće vjerojatnosti pojavljivanja, kako bi se poduzele potrebne mjere upravljanja

Global Diversity of Ascidiacea

The class Ascidiacea presents fundamental opportunities for research in the fields of development, evolution, ecology, natural products and more. This review provides a comprehensive overview of the current knowledge regarding the global biodiversity of the class Ascidiacea, focusing in their taxonomy, main regions of biodiversity, and distribution patterns. Based on analysis of the literature and the species registered in the online World Register of Marine Species, we assembled a list of 2815 described species. The highest number of species and families is found in the order Aplousobranchia. Didemnidae and Styelidae families have the highest number of species with more than 500 within each group. Sixty percent of described species are colonial. Species richness is highest in tropical regions, where colonial species predominate. In higher latitudes solitary species gradually contribute more to the total species richness. We emphasize the strong association between species richness and sampling efforts, and discuss the risks of invasive species. Our inventory is certainly incomplete as the ascidian fauna in many areas around the world is relatively poorly known, and many new species continue to be discovered and described each year

The Magnitude of Global Marine Species Diversity

Background: The question of how many marine species exist is important because it provides a metric for how much we do and do not know about life in the oceans. We have compiled the first register of the marine species of the world and used this baseline to estimate how many more species, partitioned among all major eukaryotic groups, may be discovered. Results: There are ∼226,000 eukaryotic marine species described. More species were described in the past decade (∼20,000) than in any previous one. The number of authors describing new species has been increasing at a faster rate than the number of new species described in the past six decades. We report that there are ∼170,000 synonyms, that 58,000–72,000 species are collected but not yet described, and that 482,000–741,000 more species have yet to be sampled. Molecular methods may add tens of thousands of cryptic species. Thus, there may be 0.7–1.0 million marine species. Past rates of description of new species indicate there may be 0.5 ± 0.2 million marine species. On average 37% (median 31%) of species in over 100 recent field studies around the world might be new to science. Conclusions: Currently, between one-third and two-thirds of marine species may be undescribed, and previous estimates of there being well over one million marine species appear highly unlikely. More species than ever before are being described annually by an increasing number of authors. If the current trend continues, most species will be discovered this century

Ascidian introductions through the Suez Canal: the case study of an Indo-Pacific species

Although marine biological invasions via the Suez Canal have been extensively documented, little is known about the introduction of non-indigenous ascidians (Chordata, Ascidiacea), a group containing particularly aggressive invasive species. Here, we used a multidisciplinary approach to study the introduction of the ascidian Herdmania momus into the Mediterranean Sea. We reviewed its taxonomy and global distribution, and analyzed how genetic variation is partitioned between sides of the Suez Canal. The taxonomic revision showed that H. momus currently has a wide Indo-Pacific distribution. Genetic data indicated two well-differentiated colonization histories across the eastern Mediterranean. Our findings suggest that the range expansion of H. momus has been greatly facilitated by the combined effect of human-mediated transport and the species' ability to adapt to different environments. The integrative approach presented here is critical to attain a holistic understanding of marine biological invasions, especially when studying groups with a poorly resolved taxonomy

Observations on the symbiotic relationship between the caridean shrimp Odontonia sibogae (Bruce, 1972) and its ascidian host Herdmania momus (Savigny, 1816).

Symbiotic relationships between shrimps and other invertebrates are a very common phenomenon in tropical environments. Although the caridean shrimp-ascidian association has been known for many years, the nature of this relationship is still unclear. The current study investigated the association between the caridean shrimp Odontonia sibogae (Bruce, 1972) and solitary ascidians. A combination of field work conducted along the Red Sea coast of Israel and laboratory experiments, conducted during 2015-2016, revealed a clear preference of the shrimps for the ascidian species Herdmania momus (Savigny, 1816), with a low survival ability of the shrimp outside their host's body. The shrimps usually inhabit their host as pairs of male and female or pair of females, but never as pairs of males. Out of the 53 studied females, 51% were observed to bear between 156-1,146 embryos, throughout the course of the year. As these ascidian hosts are known to create large aggregates, we suggest that males may possibly wander among the ascidians occupied by females in order to increase their reproductive success. To date, this is the first study to record the shrimp Dactylonia ascidicola (Borradaile, 1898) inhabiting the ascidian H. momus; and the first study to investigate in depth the ascidian-shrimp association in the Red Sea. It thus provides a platform for future research into the physiological and behavioral adaptations required for such a unique association

Solitary ascidians found on complex settlement plates in the Red Sea and the Mediterranean

We constructed unique settlement plates, each representing six different niches, to assess ascidian niche breadth, and deployed them in similar habitats in the Red Sea and the Mediterranean. Settlement plate design: To estimate and compare habitat niche breadth between species, we designed settlement plates each representing different niches, based on six substrate squares measures 10 x 10 cm as our basic units. The base of the plate was built from stainless steel, and the substrate squares were glued to the base. We used three substrate types within two current /light regimes to allocate six different "niches” to each settlement plate, with total measurement of 30 x 20 cm. The three substrate types were constructed from three materials: cement with sea shells, non-glazed ceramic and recycled plastic. Since substrate is a major factor for fouling species, we selected three materials that differ substantially from each other: plastic is smooth, the non-glazed ceramic is rough but homogenous, and the cement with sea shells is complex and heterogeneous. The two current and light regimes were achieved by placing the plates facing the pillars, and leaving the upper part of the plate open from three directions (from above and from either side) while the lower part remained open from the bottom only and was thus dark and with restricted water flow. We were interested in the relative patterns across species to these niche differences, and hence do not attempt to quantify the exact differences in light and flow between the upper and lower sections. Nevertheless, light measurements confirm the lower side was ~10 time darker than the upper side. We used all possible permutations (36 in total) of substrate type ordering within each current and light regime treatment in constructing the settlement plates. Study sites: The same experimental designs were used in the eastern Mediterranean Sea and northern Red Sea to facilitate direct comparisons. In the Mediterranean, the settlement plates were deployed on three pillars of the Israel Electric Company pier (32°28′ N 34°53 E), and in the Red Sea, on three pillars of the Israeli oil port (29°31′ N 34°56′ E), with minimal distance of 10 meters between pillars. At both sites, the plates were deployed at about 15 meters depth, with the seabed at 20 meters, in order to avoid any bottom effects such as sedimentation. The depth of 15 meters was chosen in order to minimize disturbance to the experiment by the strong winter storms, while still providing sufficient underwater work time when using scuba. As public entrance to both sites is prohibited, the experiment was subjected to minimal human disturbance. Pillars at both sites are located in the open sea (as opposed to closed harbors) and are >30 years old, therefore the fauna found on them represent a climax community. Study design: The experiment lasted one year, from February 2014 to February 2015. For analyses, we combined two types of plates, seasonal and full-year. We deployed 15 full-year plates at each site and these remained undisturbed for the entire year of the experiment. In addition, 10 seasonal plates were replaced every three months, totaling 40 seasonal settlement plates at each site. At the end of each experiment, the settlement plates were removed and taken to the lab for taxonomic identification (using Nikon SMZ18 stereomicroscope and dissection tools). Solitary ascidians were counted and identified to species level where possible (649 out of 658 individuals). In addition, we took monthly underwater photos of all settlement plates. Plates were photographed from the exact same distance and angle using a custom-made tripod. These photos were used in order to identify individuals that were present on the plates during the experiment but did not survive to the point of plate removal, in order to increase sample size for the niche breadth calculations. Unfortunately, only four individuals were added using these photos. We categorized the species found in the Red Sea as Lessepsian (species that are known to establish populations in the Mediterranean) or non-Lessepsian species (species that have not yet been recorded in the Mediterranean, i.e., non-invaders). In the Mediterranean we categorized the species as non-indigenous or indigenous. We included Styela plicata with the indigenous species of the Mediterranean for analysis although it possibly invaded from the Atlantic Ocean (Pineda et al., 2011; Maltagliati et al., 2015) as it is clearly not of tropical origin, unlike the rest of the non-indigenous species, and has been found in the Mediterranean for at least a century (de Barros et al., 2009). Data file structure: plate – id for each settlement plate (reminder: the six different habitats described above are within each plate). site – Mediterranean or Red Sea species type – ‘Lessepsian’ and ‘non Lessepsian’ for the species found on plates in the Red Sea site. ‘indigenous’ and ‘non-indigenous’ for species found on plates in the Mediterranean site. season – ‘spring’, ‘summer’, ‘autumn’, ‘winter’ for the seasonality plates. ‘long term’ for the long term (full year) plates. And ‘added by pictures’ for three records of P. nigra we added in order to increase its sample size for our niche breadth calculations. niche – ‘su’ for shells-up, ‘cu’ for ceramics-up, ‘pu’ for plastic-up, ‘sd’ for shells down etc… substrate – shells, ceramics or plastic light – up – upper part of the plate or down – the lower part of the plate. number of individuals – the actual data – number of individuals foun