Comparative phylogeography and population genetic structure of three widespread mollusc species in the Mediterranean and near Atlantic

Although several studies have evaluated the genetic structure and phylogeographic patterns in many species of marine invertebrates, a general model that applies to all of them remains elusive. For example, some species present an admixture of populations with high gene flow, whereas others exhibit more complex patterns characterized by small‐scale unstructured genetic heterogeneity, even at a local scale. These differences are thought to be due to clear biological aspects such as direct versus indirect development, or the presence of lecithotrophic versus planktotrophic larvae, but few studies compare animals with similar distributions and life modes. Here, we explore the phylogeographic and genetic structure patterns in two chiton (Chiton olivaceus and Lepidopleurus cajetanus) and one abalone (Haliotis tuberculata) species co‐occurring in the same habitat. Samples were obtained from shallow rocky bottoms along the Iberian Peninsula (Atlantic and Mediterranean coasts), Italy, Croatia and Greece, and the mitochondrial markers COI and 16S rRNA gene were sequenced. Our data show evidence of admixture and population expansion in C. olivaceus and H. tuberculata, whereas L. cajetanus exhibited a ‘chaotic patchiness’ pattern defined by a high genetic variability with locality‐exclusive haplotypes, high genetic divergence, and a lack of geographic structure. Shared haplotypes were sampled in both coasts of Iberia (for H. tuberculata) and in the Western and Eastern Mediterranean (for C. olivaceus), potentially indicating high dispersal ability and a recent expansion. The processes underlying the fine‐scale structuring in L. cajetanus remain a mystery. These results are especially interesting because the reproductive mode of the two chitons is similar but differs from that of the abalone, with a veliger larva, while instead the genetic structure of C. olivaceus and H. tuberculata are similar, thus contrasting with predictions based on the life history of the three molluscs and showing that the genetic patterns of marine species may be shaped by many factors, including historical ones.     

Evaluating the genetic effects of the invasive Ocenebra inornata on the native oyster drill Ocenebra erinacea

Studies focusing on the effect of invasive species on the genetic diversity of native marine invertebrates remain scant. Here we report diversity among French populations of the intertidal gastropod Ocenebra erinacea (Linnaeus, 1758) sampled in the presence and absence of the invasive Ocenebra inornata (Recluz, 1851). Between 1999 and 2004, a total of 352 individuals of O. erinacea was collected from 15 sites (five of which had the invasive present) and was genotyped at the mitochondrial locus Cytochrome Oxidase 1 (cox1). No statistical difference was observed between polymorphism levels recorded within native populations exposed to the invasive, compared with populations sampled in the absence of O. inornata. No sign of native population decline was detected in response to the invader. While significant shifts in native O. erinacea population sizes have previously been reported in the literature, genetic effects may take longer to accumulate, or may be undetectable without a larger panel of genetic markers. By contrast, large genetic distances and significant population differentiation were recorded between Atlantic and Mediterranean O. erinacea samples, suggesting that these populations have distinct evolutionary histories. Comparison of genetic divergence within the closely related genus Nucella suggests that the Atlantic populations of O. erinacea and those from Thau Lagoon in the Mediterranean may belong to different species or subspecies.     

The first use of Fulton's K for assessing and comparing the conditions of inter‐tidal fish populations

Fulton's K condition factor was applied, for the first time, to inter‐tidal specimens of the shanny (Lipophrys pholis) and long‐spined scorpion fish (Taurulus bubalis) from two English rocky shore and two Welsh rocky shore sites during summer 2010 and winter 2011. As both species contribute to the diet of commercial species such as cod (Gadus morhua) and near‐threatened species such as the European otter (Lutra lutra), their condition may affect that of these predators. Fulton's K found that inter‐tidal Welsh fish maintained a ‘good’ condition between seasons, whereas the inter‐tidal English fish were in a poorer condition during winter. Although condition also changed amongst the sites on each coast, further studies are needed into fish morphologies, environmental parameters, prey availabilities and abundances, and fish specimen sex and maturities.     

Genetic seascape of the threatened Caribbean elkhorn coral,Acropora palmata,on the Puerto Rico Shelf

It has been proposed that the elkhorn coral Acropora palmata is genetically separated into two distinct provinces in the Caribbean, an eastern and a western population admixing in Western Puerto Rico and around the Mona Passage. In this study, the genetic structure of A. palmata sampled at 11 Puerto Rican localities and localities from Curaçao, the Bahamas and Guadeloupe were examined. Analyses using five microsatellite markers showed that 75% of sampled colonies had unique genotypes, the rest being clone mates. Genetic diversity among genets was high (H_E = 0.761) and consistent across localities (0.685–0.844). F_ST ranged from ?0.011 to 0.047, supporting low but significant genetic differentiation between localities within the previously reported eastern and western genetic provinces. Plots of genetic per geographic distances and significant Mantel tests supported isolation‐by‐distance (IBD) within Puerto Rico. Analysis with the software STRUCTURE favored a scenario with weak differentiation between two populations, assigning Eastern Puerto Rican locations (Fajardo and Culebra), Guadeloupe and Curaçao to the Caribbean eastern population and Western Puerto Rican locations (west of Vega Baja and Ponce), Mona and the Bahamas to the Caribbean western population. Vieques and San Juan area harbored admixed profiles. Standardized F_ST per 1000 km unit further supported higher differentiation between localities belonging to different STRUCTURE populations, with IBD being stronger within Puerto Rico than on larger regional scales. This stronger genetic transition seems to separate localities between putative eastern and western provinces in the Eastern Puerto Rican region, but not around the Mona Passage.     

Inter‐ and intra‐colonial genotypic diversity in hermatypic hydrozoans of the family Milleporidae

Genetic diversity is the basis for adaptation and therefore of primary scientific interest, especially in species that are threatened by anthropogenic challenges, e.g. climate change and/or pollution. Coral reefs are among the most threatened but also the most diverse ecosystems and have therefore been studied quite extensively. So far, most investigations have focused on scleractinian corals while the equally important reef builders, the hydrozoans, have been less considered. Here we provide the first study of genotypic variability as well as intra‐colonial genetic variability, the co‐occurrence of more than one genotype within a single colony, in Milleporidae based on microsatellites. We analysed two geographically distinct populations from the Millepora dichotoma complex, one from the Red Sea and one from the Great Barrier Reef. Additionally, a population of Millepora platyphylla was analysed from French Polynesia. We compared microsatellite multilocus genotypes and cytochrome c oxidase subunit I haplotypes for each of the three field sites to detect levels of genotypic diversity at the intra‐ and inter‐specific levels. Furthermore, we examined all species for the occurrence of intra‐colonial genetic variability, a recently described mechanism in scleractinian corals that might enhance the adaptive potential of sessile organisms. We found both species and all field sites to be genotypically variable. Twelve mitochondrial haplotypes and 27 multilocus microsatellite genotypes were identified. In addition, intra‐colonial genetic variability was detected in the M. dichotoma complex from the Great Barrier Reef as well as in M. platyphylla from French Polynesia. All of the intra‐colonial genetically variable colonies consisted of one main genotype and a second divergent genotype caused by somatic mutations (mosaicism). Our study proves that Milleporidae are genetically variable and that the phenomenon of intra‐colonial genetic variability also occurs in this important reef‐building family.     

Ocean currents determine functional connectivity in an Antarctic deep‐sea shrimp

The coherency among larval stages of marine taxa, ocean currents and population connectivity is still subject to discussion. A common view is that organisms with pelagic larval stages have higher dispersal abilities and therefore show a relatively homogeneous population genetic structure. Contrary to this, local genetic differentiation is assumed for many benthic direct developers. Specific larval or adult migratory behavior and hydrographic effects may significantly influence distribution patterns, rather than passive drifting abilities alone. The Southern Ocean is an ideal environment to test for the effects of ocean currents on population connectivity as it is characterized by several well‐defined and strong isolating current systems. In this study we studied the genetic structure of the decapod deep‐sea shrimp Nematocarcinus lanceopes, which has planktotrophic larval stages. We analysed 194 individuals from different sample localities around the Antarctic continent using nine microsatellite markers. Consistent with a previous study based on mitochondrial DNA markers, primarily weak genetic patterns among N. lanceopes populations around the continent were found. Using ocean resistance modeling approaches we were able to show that subtle genetic differences among populations are more likely explained by ocean currents rather than by geographic distance for the Atlantic Sector of the Southern Ocean.     

The genetic structure of the exotic ascidian Styela plicata (Tunicata) from Italian ports,with a re‐appraisal of its worldwide genetic pattern

The pleated ascidian Styela plicata (Lesueur, 1823) is a solitary species commonly found in ports and marinas around the world. It has been recorded in the Mediterranean region since the mid‐19th century. In the present work, the species’ genetic diversity was analysed, employing a 613‐bp portion of the mitochondrial cytochrome c oxidase subunit I (COI) gene from 149 individuals collected in 14 ports along Italian coasts at spatial scales ranging from 1 to approximately 2200 km. Haplotype and nucleotide diversity values were h = 0–0.933 (total h = 0.789) and π = 0–0.145 (total π = 0.0094), respectively. A general southward trend of increasing within‐population genetic diversity was observed. Analysis of molecular variance revealed significant genetic structuring but no significant differences were detected among basins, and no isolation by distance was found. Our data were integrated with the COI sequences available from previous studies and re‐analysed in order to investigate the possible routes of introduction of this ascidian into the Mediterranean Sea. The presence of the two COI haplogroups detected in previous molecular investigations on S. plicata at intercontinental spatial scale was confirmed in the Mediterranean Sea. The results revealed multiple introductions of S. plicata, although some locations appear to have experienced rapid expansion from few founding individuals with reduced genetic diversity. However, continuous introductions would confound the pattern deriving from single founder events and make it difficult to estimate the time needed for gene diffusion into established populations. This mixing of effects creates difficulties in understanding the past and current dynamics of this introduction, and managing this alien invasive ascidian whose genetic structure is continuously shuffled by vessel‐mediated transport.     

Sexual traits plasticity of the potentially invasive limpet Bostrycapulus odites (Gastropoda: Calyptraeidae) within its natural distribution in South America

The slipper limpet Bostrycapulus odites has recently been reported as an introduced species on the Spanish Mediterranean coast. Another species in the family Calyptraeidae, Crepidula fornicata, is a problematic invasive species in the Northeast Atlantic, which makes the closely related Bostrycapulus introduction a matter of concern. Information on the biology of B. odites in its natural environment can facilitate predictions on where the species could find favourable conditions for settlement and expansion. Size and sex were recorded for individuals in four populations over 2600 km of the Southwestern Atlantic shoreline, in Argentina and Brazil, covering the whole native latitudinal range of this widely distributed species. Animals were collected by hand in the intertidal or by SCUBA in subtidal locations; specimens were examined to determine shell length, sex, and the presence and number of brooded egg capsules in females. Mean shell length for the whole population did not differ significantly among populations. However, this species experiences sequential hermaphroditism (protandrism), and the size at sexual maturity (minimum male size) increased significantly with latitude. The fecundity of females at all sites increased with size, and the number of brooded egg capsules as well as the average size of capsules was larger in bigger individual females; however, mean fecundity varied among sites independent of mean female body size. This limpet species modifies its reproductive traits with local conditions, and sexual characters develop earlier in more temperate localities.     

Molecular evidence for Myripristis jacobus and Scarus taeniopterus new to Bay of Bengal: Sporadic appearance or preliminary colonization?

Individual specimens of Myripristis jacobus Cuvier, 1829 and Scarus taeniopterus Lesson, 1829 were collected from Gopalpur‐on‐sea, Odisha coast, Bay of Bengal. Both the fish samples were assigned species level tags using the conventional taxonomic methods. The capture of both the fish species is of particular interest in that they were new to the Bay of Bengal. Molecular analysis using the mitochondrial cytochrome oxidase subunit I (COI) gene showed high confidence sequence similarity in species identification. The resultant phylogenetic relationships strongly support the monophyly of both the genus with congruent clustering of both the species according to their morphological identification. In addition, the time tree produced is in complete agreement with the recent studies. These studies conclusively prove that both the species might have been originated during the middle to the late Miocene period. Furthermore, both fish species are typical inhabitants of stigmatized coral reefs, confined to the reef regions. These fish species perhaps migrated to the Bengal Bay from the Andaman and Nicobar Islands reef regions because of climatic changes.     

First record of an odontaspidid shark in New Zealand waters

Photographs and a preserved head are identified as Odontaspis herbsti Whitley, 1950, an Australian sand shark growing to about 3 m long and similar to the Mediterranean O. ferox Risso, but differing in having a uniform grey body without black markings on the back or sides. No living odontaspidids have previously been reported from New Zealand. Six specimens were trawled in 119–165 m off Table Cape, Hawke Bay, in October‐November 1972. Californian and. East Atlantic (Madeira) specimens are treated as conspecific with O. herbsti. It is suggested that O. herbsti is normally an inhabitant of the continental slope, and that the present records are of a few individuals that have strayed on to the shelf.     

Determining the correct identity of South African Marthasterias (Echinodermata: Asteroidea)

Marthasterias glacialis are found in the cool-temperate waters of the north-eastern Atlantic Ocean, in the subtropical waters of the Mediterranean Sea and along the south-western tip of Africa. The South African Marthasterias population includes two morphotypes, a smooth, spineless rarispina form and a spiny africana form, that have been described as separate species, subspecies, or forma by various authors over the past century. To test whether these two morphotypes represent separate species, and whether either, or both, are conspecific with the North-East Atlantic species, 78 Marthasterias were collected from the Cape Peninsula of South Africa. Morphological comparisons between individuals of the two forms showed no significant clustering of samples, indicating that there is no morphological separation of the two South African forms into distinct groupings. The africana and rarispina forms were also shown to be genetically indistinguishable, using a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene and the nuclear internal transcribed spacer 1 (ITS1). In addition, the COI sequences were also compared to those from European specimens, and phylogenetic reconstruction and intra- and interspecific levels of divergence suggested that the South African specimens form a single group that is genetically distinct from the European M. glacialis. Although the allopatric distribution, high genetic divergence (more than 3% for the COI fragment) and morphological differences suggest that the South African form should be raised to species status under the name Marthasterias africana, further work must assess an independent genetic marker (nuclear) to support raising the COI clade to species level. True M. glacialis have a spine-armament pattern of a series of three or more regular spine rows down the length of each arm, whereas M. africana are either covered in many irregularly spaced spines, or have an extraordinarily bare surface with only two spine rows per arm. Marthasterias africana may also have an actinal spine simulating the presence of a third inferomarginal spine. This work tentatively resolves the taxonomic dispute, elucidates the separation and amalgamation of the two African forms and suggests a single, uniquely South African Marthasterias species that might be distinct from the north Atlantic M. glacialis, although further analyses to test reproductive isolation between the North-East Atlantic and South African forms are required.     

West versus East Mediterranean Sea: origin and genetic differentiation of the sea cucumber Holothuria polii

We studied the genetic structure of the sea cucumber Holothuria (Roweothuria) polii (Delle Chiaje 1823) by analysing the mitochondrial DNA variation in two fragments of cytochrome oxidase I (COI) and 16S genes. Individuals were collected in seven locations along the Mediterranean Sea, which cover a wide range of the species distribution. We found high haplotype diversity for COI and moderate diversity for 16S, and low nucleotide diversity for both genes. Our results for the COI gene showed many recent and exclusive haplotypes with few mutational changes, suggesting recent or ongoing population expansion. The Western and Eastern Mediterranean populations exhibited slight but significant genetic differentiation (COI gene) with higher genetic diversity in the East. The most ancient haplotype was not present in the westernmost sampling location (SE Spain). The oldest expansion time was observed in Turkey, corresponding to mid‐Pleistocene. Turkey had also the highest genetic diversity (number of total and exclusive haplotypes, polymorphisms, haplotype and nucleotide diversity). This suggests that this region could be the origin of the subsequent colonizations through the Mediterranean Sea, a hypothesis that should be assessed with nuclear markers in future research.     

Disentangling exploitation of the intertidal grazer Phorcus sauciatus (Gastropoda: Trochidae) in an oceanic archipelago: Implications for conservation

Harvesting of intertidal grazers such as topshells is known to affect negatively the exploited populations by altering population structure and decreasing abundance. Phorcus sauciatus has a wide geographic distribution in the North‐eastern Atlantic Ocean and is subject to increasing levels of harvesting pressure due to the expansion of human population on coastal areas. The effect of proximity to human settlements and coastal accessibility on the size structure and abundance of P. sauciatus populations was examined in Madeira archipelago. Mean size, proportion of reproductive individuals, and abundance of this species were generally smaller in areas closer to human settlements and in more accessible coastal areas. Marine protected areas returned the highest mean sizes evidencing their effectiveness in preserving the size structure of this species. The results highlight the necessity to regulate the harvest of P. sauciatus in Madeira archipelago, as well as the implementation of management measures aiming at the sustainable exploitation and conservation of this species, exploited in this region since the early 15th century.     

High connectivity between sea lough populations of a planktonic larval disperser with the adjacent open coast

Several previous studies have reported high levels of genetic differentiation between populations inside European Marine Reserves and their adjacent coastlines for a direct‐developing species. These studies suggest that sea loughs may not represent the most suitable sites for inclusion into Marine Protected Area (MPA) or Marine Reserve networks as they are not well connected to other populations. However, many marine species have pelagic larvae, and the connectivity of populations of such species inside sea loughs with non‐lough populations remains unknown. Here, I investigated the levels of gene flow between populations of the acorn barnacle Semibalanas balanoides inside and outside Strangford Lough, Northern Ireland; this species has a long‐lived pelagic larvae (4–6 weeks). There were no significant differences in the levels of genetic diversity between sea lough and non‐lough populations and no evidence for genetic differentiation between any of the populations examined; the populations appear well mixed and well connected, in contrast to what has been reported for a previous direct‐developing species.     

Cryptic diversity and phylogeography of the island‐associated barnacle Chthamalus moro in Asia

Pleistocene glaciations were among the important historic events that shaped the population structures of marine organisms. Genetic studies of different marine fauna and flora have demonstrated the effect of Pleistocene glaciations on taxa that reside in marginal seas. However, how marine island species responded to Pleistocene glaciations remains relatively unstudied, especially in Asia. Genetic analyses based on the island‐associated barnacle Chthamalus moro collected from 14 sites in Asia reveal that C. moro comprises three distinct lineages, with COI divergence ranging from 3.9 to 8.3%. Population genetic analyses on respective lineages reveal signs of demographic expansion within the Pleistocene epoch at different times. The Ogasawara lineage, which has a more oceanic distribution, expanded the earliest, followed by the population expansion of the Ryukyu and Southern lineages that inhabit islands closer to the continent. The data suggest that the inhabitants of outer islands may have been less affected by Pleistocene glaciations than those that reside closer to the continent, as the former were able to maintain a large, stable, effective population size throughout the late Pleistocene.     

Chromosomal population structuring in carangids (Perciformes) between the north-eastern and south-eastern coasts of Brazil

The family Carangidae comprises 151 species, of which only 19 have been so far karyotyped, including a few representatives from the Western Atlantic Ocean. This study compared the cytogenetic features of three Atlantic carangids, Chloroscombrus chrysurus, Trachinotus goodei and T. falcatus, from north-eastern Brazilian coast, with previously obtained cytogenetic data from southern populations. All species presented 2n = 48 chromosomes. Chloroscombrus chrysurus showed a conserved karyotypic macrostructure (2n = 48a, FN = 48) whereas T. goodei (2m + 2sm + 44a; FN = 52) and T. falcatus (2n = 10m/sm + 38a; FN = 58) presented more diversified karyotypes. Data showed that the samples of C. chrysurus from the north-eastern and south-eastern regions did not differ cytogenetically. However, the frequency or position of ribosomal sites (Ag-NOR/18S rDNA) were effective in discriminating the populations of Trachinotus between these coastal regions. The distinct chromosomal patterns suggest a historical genetic fractionating of the Trachinotus populations along the Brazilian coast.     

High connectivity and directional gene flow in European Atlantic and Mediterranean populations of Ciona intestinalis sp. A

Understanding the factors that cause population divergence has long been of interest to marine biologists in their attempts to interpret the effect of human‐mediated vectors. Broadcast‐spawning species with limited dispersal capability are excellent candidates to measure the present‐day patterns of genetic diversity. The tunicate Ciona intestinalis (Ascidiacea) is comprised of a complex of morphologically cryptic species that form vigorous aggregates in eutrophic habitats (harbors, gulfs and lagoons) where they can compete with the epibenthic community and cause biofouling problems. This study investigated biogeographic variability and migration patterns of C. intestinalis sp. A along Northeast Atlantic and Mediterranean coasts using microsatellite markers. Data presented here on 371 specimens collected from 17 populations reveal high genetic polymorphism, but with a deficit of heterozygote deficiency. Absence of evidence for isolation by distance suggests that the genetic patterns do not reflect the geographic distribution of sampled populations. Substantial gene flow and artificial potential for dispersal boost high levels of within‐population genetic variability and prevent genetic differentiation within and between seas. A predominant eastward migration pattern was revealed by the data set, with very limited opportunity for C. intestinalis sp. A to travel westward. This directional movement indicates that other properties (e.g. habitat quality, genetic traits, mating system, life cycle) may cause adaptive divergence at a large biogeographic scale.     

A facies of Kophobelemnon (Cnidaria,Octocorallia) from Santa Maria di Leuca coral province (Mediterranean Sea)

During a research cruise carried out in April 2010, aimed at updating the knowledge on the biodiversity of the Santa Maria di Leuca (SML) cold‐water coral province (Mediterranean Sea), a facies of the sea pen Kophobelemnon stelliferum (Muller, 1776) was found on mud‐dominated bottoms. This finding represents a new species and a new habitat record from the SML coral province as well as a new bathyal facies in the whole Central Mediterranean Sea. The colonies were collected using an epi‐benthic sledge, at depths between 400 and 470 m. A significant positive relationship between polyp number and colony length was detected. Density of the colonies ranged from 0.003 to 0.038 N·m^?2. Differences and affinities between Mediterranean and Atlantic occurrences of K. stelliferum are discussed.     

Size‐frequency distributions of Joania cordata and Argyrotheca cuneata (Brachiopoda: Megathyrididae) from the Central Tyrrhenian Sea

Size‐frequency distributions can support reliable inferences concerning population dynamics of brachiopods, but only a few data are available so far. In this study, length and width frequency distributions of dead specimens of the Recent brachiopods Joania cordata and Argyrotheca cuneata from the Marine Protected Area ‘Secche di Tor Paterno’, Central Tyrrhenian Sea, Italy (41°35′ N, 12°20′ E), are reported in order to add new data about size‐frequency distributions of brachiopods. The studied specimens came from death assemblages in the coralligenous substrate, in the Posidonia oceanica meadows, and in the sand channels. The observed patterns vary from left‐skewed (J. cordata) to right‐skewed (A. cuneata), indicating respectively a low and high mortality of smaller individuals. Significant differences between the coralligenous substrate and the P. oceanica meadow were observed for both species, revealing a variation among different habitats. All length and width distributions are clearly polymodal, but the biological meaning of the peaks is difficult to interpret, as the two species seem to have a 2‐year life span. A biometric analysis of shell sizes revealed that length and width are the most variable parameters during the growth of the animal.