Molecular Evidence for Lessepsian Invasion of Soritids (Larger Symbiont Bearing Benthic Foraminifera)

The Mediterranean Sea is considered as one of the hotspots of marine bioinvasions, largely due to the influx of tropical species migrating through the Suez Canal, so-called Lessepsian migrants. Several cases of Lessepsian migration have been documented recently, however, little is known about the ecological characteristics of the migrating species and their aptitude to colonize the new areas. This study focused on Red Sea soritids, larger symbiont-bearing benthic foraminifera (LBF) that are indicative of tropical and subtropical environments and were recently found in the Israeli coast of the Eastern Mediterranean. We combined molecular phylogenetic analyses of soritids and their algal symbionts as well as network analysis of Sorites orbiculus Forskål to compare populations from the Gulf of Elat (northern Red Sea) and from a known hotspot in Shikmona (northern Israel) that consists of a single population of S. orbiculus. Our phylogenetic analyses show that all specimens found in Shikmona are genetically identical to a population of S. orbiculus living on a similar shallow water pebbles habitat in the Gulf of Elat. Our analyses also show that the symbionts found in Shikmona and Elat soritids belong to the Symbiodinium clade F5, which is common in the Red Sea and also present in the Indian Ocean and Caribbean Sea. Our study therefore provides the first genetic and ecological evidences that indicate that modern population of soritids found on the Mediterranean coast of Israel is probably Lessepsian, and is less likely the descendant of a native ancient Mediterranean species.     

Why is the mediterranean more readily colonized than the Red Sea,by organisms using the Suez Canal as a passageway?

Summary Since the opening of the Suez Canal, more than 120 Red Sea species colonized the eastern Mediterranean, whereas less than 10 Mediterranean species colonized the Red Sea. For most of the species involved in this colonization, the mode of dispersal from the source to the colonized area is through free-drifting propagules. In order to examine whether the current regime of the Suez Canal may be involved in this assymetry in colonization, a mathematical hydraulic model that forecasts the direction and velocity of water currents through the year, along the length of the Canal, was utilized. The movements of free-floating propagules that occur at either entrance of the Canal, was simulated on a computer, and it was found that the completion of a Mediterranean-bound passage of Red Sea propagules is far faster and much more likely than a completion of a Red Sea-bound passage of Mediterranean propagules.Paper No. 7 in the series Colonization of the Eastern Mediterranean by Red Sea species immigrating through the Suez Canal     

rDNA analysis of the Red Sea seagrass,Halophila, reveals vicariant evolutionary diversification

The effects of opening the Suez Canal as a connection between the Red Sea and the Mediterranean Sea were reported for a number of marine species. However, the evolutionary origin of the seagrasses in the Red Sea and the linking population genetics of seagrasses between the Arabian Sea, the Gulf of Aden, the Red Sea and the Mediterranean Sea have not yet been investigated in detail. The invasion of Halophila stipulacea Asch. from the Red Sea into the Mediterranean Sea after the opening of the Suez Canal was already recorded. We hypothesize that Halophila ovalis populations in the Red Sea developed through long-term historical processes such as vicariant evolutionary diversification. Seagrass samples were collected along the Egyptian coastline of the Red Sea and analysed by the molecular marker ITS. The sequences were compared with published ITS sequences from seagrasses collected in the whole area of interest. In this study, we reveal the linking population genetics, phylogeography and phylogenetics of two dominant seagrass species, Halophila stipulacea and Halophila ovalis, among species collected in the Red Sea and worldwide. The results indicate that the Red Sea Halophila ovalis populations do not group to Halophila ovalis worldwide, and Halophila major, Halophila ovalis collected worldwide and Halophila ovalis collected at the Red Sea are sister clades. Hence, vicariant evolutionary diversification for Halophila ovalis may occur in the Red Sea.     

Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus)

Since the opening of the Suez Canal in the 19th century, a growing number of teleosts species have become permanently established in the eastern Mediterranean. As environmental parameters in the Mediterranean are very different from those in the Red Sea, there is an opportunity to evaluate the gene flow associated with the acclimatisation of these species to their new environment. Initial colonisation may have been restricted to individuals with marginal genotypes compared to populations of the Red Sea, eventually better adapted to the Mediterranean environment. Alternatively, colonisation may have occurred without major genetic differentiation, due to a large flux of immigrants and a continuous gene flow from the populations of origin. Using different molecular genetic techniques (mitochondrial DNA, Exon-Primed Intron-Crossing PCR amplification (EPIC) and Inter-Simple Sequence Repeats (ISSRs), patterns of genetic differentiation on both sides of the Suez isthmus were tested on two Lessepsian rabbitfish species (Siganus rivulatus and Siganus luridus). The absence of genetic differentiation between Mediterranean and Red Sea populations in both species showed that a great number of migrants participated to the colonisation of the Mediterranean, excluding any bottleneck event. This colonisation success suggests large eco-physiological plasticity in S. rivulatus and S. luridus that allowed them to thrive in the new environment.     

Red to Mediterranean Sea bioinvasion: natural drift through the Suez Canal,or anthropogenic transport?

The biota of the eastern basin of the Mediterranean Sea has experienced dramatic changes in the last decades, in part as a result of the massive invasion of Red Sea species. The mechanism generally hypothesized for the 'Red-to-Med' invasion is that of natural dispersal through the Suez Canal. To date, however, this hypothesis has not been tested. This study examines the mode of invasion, using as a model the mussel Brachidontes pharaonis, an acclaimed 'Lessepsian migrant' that thrives along the eastern Mediterranean coast. Our findings reveal two distinct lineages of haplotypes, and five possible explanations are discussed for this observation. We show that the genetic exchange among the Mediterranean, Gulf of Suez and the northern Red Sea is sufficiently large to counteract the build up of sequential genetic structure. Nevertheless, these basins are rich in unique haplotypes of unknown origin. We propose that it is historic secondary contact, an ongoing anthropogenic transport or both processes, that participate in driving the population dynamics of B. pharaonis in the Mediterranean and northern Red Sea.     

The rDNA ITS Region in the Lessepsian Marine Angiosperm <Emphasis Type="BoldItalic">Halophila stipulacea</Emphasis> (Forssk.) Aschers. (Hydrocharitaceae): Intragenomic Variability and Putative Pseudogenic Sequences

Halophila stipulacea is a dioecious marine angiosperm, widely distributed along the western coasts of the Indian Ocean and the Red Sea. This species is thought to be a Lessepsian immigrant that entered the Mediterranean Sea from the Red Sea after the opening of the Suez Canal (1869). Previous studies have revealed both high phenotypic and genetic variability in Halophila stipulacea populations from the western Mediterranean basin. In order to test the hypothesis of a Lessepsian introduction, we compare genetic polymorphism between putative native (Red Sea) and introduced (Mediterranean) populations through rDNA ITS region (ITS1-5.8S-ITS2) sequence analysis. A high degree of intraindividual variability of ITS sequences was found. Most of the intragenomic polymorphism was due to pseudogenic sequences, present in almost all individuals. Features of ITS functional sequences and pseudogenes are described. Possible causes for the lack of homogenization of ITS paralogues within individuals are discussed.     

Marine molluscs from the Iztuzu beach near Dalyan (Mediterranean coast of Turkey)

Abstract

A total of l84 species of marine molluscs has been identified from shells collected on the beach of Iztuzu near Dalyan (Mu?la province, Turkey). Of these, 16 species of gastropod and 4 species of bivalvia are new For the extreme Eastern Mediterranean. Only three species of Lessepsian migrants (from the Red Sea via the Suez canal) have been found.     

Genetic differentiation among populations of Minona ileanae (Platyhelminthes: Proseriata) from the Red Sea and the Suez Canal

The phenomenon of Lessepsian migration has stimulated the interest of biologists ever since the opening of the Suez Canal in 1869, concerning, in particular, the possible effects of migrants on Mediterranean autochthonous communities. So far, most attention has been devoted to macrofaunal taxa - yet, the nature of the sandy shores of the Canal may constitute an ideal habitat for many interstitial taxa. However, studies on these organisms, and especially on “inconspicuous” taxa, such as the microturbellaria, are almost completely lacking. A recent sampling campaign along the shores of the Suez Canal, aimed at studying the composition and distribution of free-living Platyhelminthes in the area, potential invaders of the Mediterranean Sea, revealed the occurrence of the interstitial species Minona ileanae (Neoophora: Proseriata), first described on specimens collected in the Gulf of Eilat-Aqaba (Red Sea). The presence of a significant population of this species in the Suez area, a possible source of colonizers of the Canal, allowed comparison between its genetic pattern and those obtained from three populations collected in the Canal. Their genetic structure was surveyed by means of ISSR (Inter-Simple Sequence Repeat) molecular markers. UPGMA cluster analysis based on the matrix of interindividual dissimilarity (1-relatedness) and the assignment test revealed sharp genetic divergence among the four samples with a highly significant F_ST value (0.155, P < 0.001). The significant genetic differentiation may be related to a post-1869 colonisation of the Canal with swift genetic divergence, due to either different pressure selection of the habitats and/or the short life cycle of M. ileanae, or, more convincingly, to an early migration to the Isthmus in pre-Lessepsian periods, during i) the Last Interglacial Optimum, ii) the Holocene Climatic Optimum, or iii) across the artificial waterways built by the ancient Egyptians from the 13th century B.C. onwards. The remarkable tolerance shown in laboratory of the species to salinity values ranging from as low as 10‰ to 80‰ supports the possibility that M. ileanae may have survived in the water bodies of the Isthmus in pre-Lessepsian times.     

Molecular analysis of the recently described lizardfish Saurida lessepsianus (Synodontidae) from the Red Sea and the Mediterranean,with remarks on its phylogeny and genetic bottleneck effect

The opening of the Suez Canal in 1869 led to a massive influx of Red Sea species that invaded the Mediterranean; this was termed ‘Lessepsian migration'. Among these species was a species of lizardfish, identified by some authors as Saurida undosquamis and by others as S. macrolepis. Recently, the Red Sea and the Mediterranean populations were described according to external characteristics as a unique taxon, Saurida lessepsianus. Our molecular study confirms this finding and determines that all previous records of S. undosquamis and S. macrolepis in the Red Sea and the Mediterranean are misidentifications of S. lessepsianus. The Mediterranean population of S. lessepsianus exhibits a lower genetic variability than that of the Red Sea population, suggesting a bottleneck effect.     

First record of the bluespotted cornetfish from the Mediterranean Sea

Three specimens of the Indo-Pacific Bluespotted cornetfish Fistularia commersonii are recorded for the first time from the Mediterranean. The presence of this species in the Mediterranean is due to migration from the Red Sea via the Suez Canal.     

Seagrasses in the Zeit Bay area and at Ras Ghârib (Egyptian Red Sea coast)

The distribution and ecology of seagrasses along parts of the Egyptian Red Sea coasts have been investigated. Five of the 10 species ever reported from the Red Sea have been found in this area, i.e. Halodule uninervis (Forssk.) Aschers., Thalassodendron ciliatum (Forssk.) den Hartog, Halophila stipulacea (Forssk.) Aschers., Halophila ovalis (R. Br.) Hook. f. and Halophila ovata Gaud. H. ovata is recorded here for the first time for the west coast of the Red Sea. The finding of Halophila decipiens Ostenfeld represents a new record to the Red Sea; this species has been found at a depth of 30 m, near Ras Ghârib in the Gulf of Suez.     

First confirmed record of Lagocephalus sceleratus(Gmelin, 1789) in the Mediterranean Sea

One specimen of the Indo‐Pacific silverstripe blaasop Lagocephalus sceleratus (Gmelin, 1789)(Tetraodontidae) is recorded from the Aegean coast of Turkey and is confirmed for the Mediterranean. Dispersal of the species to the Mediterranean is due to migration from the Red Sea via the Suez Canal.     

Opisthobranch molluscs of the Sudanese Red Sea

Eighteen opisthobranch species are described and illustrated from the Sudanese Red Sea, including seven new species, one new subspecies and three species for which this is the first Red Sea record. Eleven bullomorphs, four pleurobranchomorphs, four sacoglossans and four phyllidiid mudibranchs are now known from the Red Sea. There appears to be a high percentage of endemic species in the Red Sea. This is what one might expect, in view of the conditions of near isolation, low temperatures and high salinity that prevailed in this sea 13000 23000 years ago. Of the groups discussed in this paper, one Red Sea species has invaded the Mediterranean Sea, and one Mediterranean species has invaded the Red Sea, since the opening of the Suez Canal in 1867. Many Red Sea species are very colourful, in comparison to Mediterranean ones. This could perhaps be because Red Sea waters are cleaner, thereby favouring the evolution of greater precision in colour markings.     

Opisthobranch molluscs of the Sudanese Red Sea

Eighteen opisthobranch species are described and illustrated from the Sudanese Red Sea, including seven new species, one new subspecies and three species for which this is the first Red Sea record. Eleven bullomorphs, four pleurobranchomorphs, four sacoglossans and four phyllidiid mudibranchs are now known from the Red Sea.
There appears to be a high percentage of endemic species in the Red Sea. This is what one might expect, in view of the conditions of near isolation, low temperatures and high salinity that prevailed in this sea 13000 23000 years ago.
Of the groups discussed in this paper, one Red Sea species has invaded the Mediterranean Sea, and one Mediterranean species has invaded the Red Sea, since the opening of the Suez Canal in 1867.
Many Red Sea species are very colourful, in comparison to Mediterranean ones. This could perhaps be because Red Sea waters are cleaner, thereby favouring the evolution of greater precision in colour markings.     

The Japanese threadfin bream Nemipterus japonicus, a new Indo‐Pacific fish in the Mediterranean Sea

A specimen of the Japanese threadfin bream Nemipterus japonicus was recorded for the first time from the Mediterranean Sea. The presence of this Indo‐Pacific fish in the Mediterranean is evidently due to migration from the Red Sea via the Suez Canal.     

First record of Apogon queketti Gilchrist (Osteichthyes: Apogonidae) in the Mediterranean Sea

The spotfin cardinalfish Apogon queketti is recorded for the first time in the north-eastern Mediterranean Sea (Iskenderun Bay, Turkey). Two specimens of this species, 111 and 102 mm total length were caught by a commercial trawler at depths of 55 and 60 m on 14 October 2004 and 23 April 2005, respectively. The occurrence of this species in the Mediterranean Sea is the result of migration from the Red Sea via the Suez Canal.     

The Arabian scad Trachurus indicus, a new Indo-Pacific species in the Mediterranean Sea

The Arabian scad Trachurus indicus is recorded for the first time from the Mediterranean Sea (Iskenderun Bay, Turkey). The presence of this Indo-Pacific fish in the Mediterranean Sea is probably because of migration from the Red Sea via the Suez Canal.     

Long-term changes in population genetic features of a rapidly expanding marine invader: implication for invasion success

Large blooms of Rhopilema nomadica, a highly venomous rhizostamatid scyphozoan species introduced to the Mediterranean through the Suez Canal, have become ubiquitous in the summer and winter months along the Israeli coasts since the mid-1980s. This species has since spread across the eastern Mediterranean and was sighted as far west as Tunisia and Sardinia. For the past 12 years, we have studied changes in the mitochondrial COI haplotypes diversity of R. nomadica to investigate small scale fluctuactions of genetic diversity and to reveal possible genetic structuring of the fast spreading invader in the Eastern Mediterranean. The 1091 COI sequences analysed, revealed a highly diverse population displaying 89 haplotypes, 46 of which appeared as singletons, low frequency haplotypes. All the specimens analysed throughout the period belong to a single unstructured population. Though lacking data from the source population in the Red Sea, the high within-population diversity and the high diversity of COI haplotypes support the hypothesis of multiple introductions events, or an open corridor with a continuous influx of propagules. Tajima’s D and Fu’s Fst negative values and the increased numbers of COI singletons from early to late sampling periods, have verified that the Israeli population is characterized by a rapid expanding population. Further research is needed for the evaluation of COI diversity and patterns in R. nomadica populations across the eastern Mediterranean Sea and Red Sea, as well as any correlation of the high variability between COI locus and phenotypic diversity.

     

Comparative genetics of scyphozoan species reveals the geological history and contemporary processes of the Mediterranean Sea

Jellyfish are useful genetic indicators for aquatic ecosystems as they have limited mobility and are highly exposed to the water column. By using comparative genomics and the molecular clock (timetree) of Rhizostoma pulmo, we revealed a divergence point between the East and West Mediterranean Sea (MS) populations that occurred 4.59 million years ago (mya). It is suggested that the two distinct ecological environments we know today were formed at this time. We propose that before this divergence, the highly mixed Atlantic and Mediterranean waters led to the wide dispersal of different species including R. pulmo. At 4.59 mya, the Western and Eastern MS were formed, indicating the possibility of a dramatic environmental event. For the first time, we find that for the jellyfish we examined, the division of the MS in east and west is not at the Straits of Sicily as generally thought, but significantly to the east. Using genomics of the Aurelia species, we examined contemporary anthropogenic impacts with a focus on migration of scyphozoa across the Suez Canal (Lessepsian migration). Aurelia sp. is among the few scyphozoa we find in both the MS and the Red Sea, but our DNA analysis revealed that the Red Sea Aurelia sp. did not migrate or mix with MS species. Phyllorhiza punctata results showed that this species was only recently introduced to the MS as a result of anthropogenic transportation activity, such as ballast water discharge, and revealed a migration vector from Australia to the MS. Our findings demonstrate that jellyfish genomes can be used as a phylogeographic molecular tool to trace past events across large temporal scales and reveal invasive species introduction due to human activity.