Cryptic speciation and genetic structure of widely distributed brittle stars (Ophiuroidea) in Europe

Pérez‐Portela, R., Almada, V. & Turon, X. (2012). Cryptic speciation and genetic structure of widely distributed brittle stars (Ophiuroidea) in Europe. —Zoologica Scripta, 00, 000–000. The development of molecular techniques has led to the detection of numerous cases of cryptic speciation within widely distributed marine invertebrate species and important taxonomic revisions in all the major marine taxa. In this study, we analysed a controversial marine species complex in the genus Ophiothrix, a widespread taxon in European waters traditionally assigned to two nominal species, Ophiothrix fragilis and O. quinquemaculata. These species are important components of the rocky shores and deep marine benthos along the North Atlantic and Mediterranean littoral. Their status (including variants of both species) has remained contentious due to overlapping variability in morphological characters. In this study, we analysed the genetic and morphological differences of Ophiothrix lineages along the Atlantic and Mediterranean coasts. We also assessed population genetic structure in the Atlantic and Mediterranean basins by sequencing two mitochondrial genes, the 16S rRNA gene and COI gene, of 221 specimens from 13 locations. Phylogenetic analyses demonstrated the existence of two genetically distinct lineages, attributable to two different species although unrelated to previous taxonomic distinctions. Morphological differences could also be detected between these lineages. Samples from the Northeast Atlantic and one from the deep Mediterranean grouped within Lineage I, whereas Lineage II pooled together the southern Atlantic and rocky shallow Mediterranean samples. In the northern region of the Iberian Peninsula and at a deep locality in the Mediterranean, both lineages overlap. Speciation processes likely happened during the Mio–Pliocene transition (about 4.8–7.5 million years ago), when marine‐level oscillations led to the blockage of major marine corridors in Europe and promoted genetic isolation by vicariance. Secondary contact between lineages following sea‐level increases and recolonization during the refilling of the Mediterranean after the Miocene salinity crisis could explain the present‐day distribution of genetic variability. No barriers to gene flow along the Atlanto‐Mediterranean area were detected for Lineage II, and the lack of genetic structure could be caused by a mixture of several factors, such as wide dispersal potential, recent demographic expansion and large population size.     

Deep phylogeographic structure may indicate cryptic species within the Sparid genus Spondyliosoma

Two geographically nonoverlapping species are currently described within the sparid genus Spondyliosoma: Spondyliosoma cantharus (Black Seabream) occurring across Mediterranean and eastern Atlantic waters from NW Europe to Angola and S. emarginatum (Steentjie) considered endemic to southern Africa. To address prominent knowledge gaps this study investigated range-wide phylogeographic structure across both species. Mitochondrial DNA sequences revealed deep phylogeographic structuring with four regionally partitioned reciprocally monophyletic clades, a Mediterranean clade and three more closely related Atlantic clades [NE Atlantic, Angola and South Africa (corresponding to S. emarginatum)]. Divergence and distribution of the lineages reflects survival in, and expansion from, disjunct glacial refuge areas. Cytonuclear differentiation of S. emarginatum supports its validity as a distinct species endemic to South African waters. However, the results also indicate that S. cantharus may be a cryptic species complex wherein the various regional lineages represent established/incipient species. A robust multilocus genetic assessment combining morphological data and detailing interactions among lineages is needed to determine the full diversity within Spondyliosoma and the most adequate biological and taxonomic status.     

DNA barcoding reveals cryptic diversity in marine hydroids (Cnidaria, Hydrozoa) from coastal and deep-sea environments

Fifty-six sequences of the mitochondrial 16S RNA gene were generated for hydroids, belonging to six nominal families — Eudendriidae, Lafoeidae, Haleciidae, Sertulariidae, Plumulariidae and Aglaopheniidae — collected from bathyal environments of the Gulf of Cadiz (22 haplotypes), Greenland (1 haplotype), Azores (1 haplotype), the shallow waters of the UK (17 haplotypes) and Portugal (2 haplotypes). When combined and analysed with 68 additional sequences published in GenBank, corresponding to 63 nominal species of these families (nine species in common between the GenBank sequences and those presented by the authors), cryptic species were detected (e.g. two species of Nemertesia and other of Lafoea ), as well as apparent cases of conspecificity (e.g. Nemertesia antennina and N. perrieri and Aglaophenia octodonta , A. pluma and A. tubiformis ). Other taxonomic inconsistencies were found in the data including cases where species from different genera clustered together (e.g. Sertularia cupressina , Thuiaria thuja , Abietinaria abietina and Ab. filicula ). The mitochondrial 16S rRNA proved to be a useful DNA 'barcode' gene for hydroids, not only allowing discrimination of species, but also in some cases of populations, genera and families, and their intra- or interphylogenetic associations. Although still under-represented in public data bases, the 16S rRNA gene is starting to be used frequently in the study of hydroids. These data provide powerful complementary evidence for advancing our understanding of hydrozoan systematics.     

Cryptic habitats and cryptic diversity: unexpected patterns of connectivity and phylogeographical breaks in a Mediterranean endemic marine cave mysid

The marine cave‐dwelling mysid Hemimysis margalefi is distributed over the whole Mediterranean Sea, which contrasts with the poor dispersal capabilities of this brooding species. In addition, underwater marine caves are a highly fragmented habitat which further promotes strong genetic structuring, therefore providing highly informative data on the levels of marine population connectivity across biogeographical regions. This study investigates how habitat and geography have shaped the connectivity network of this poor disperser over the entire Mediterranean Sea through the use of several mitochondrial and nuclear markers. Five deeply divergent lineages were observed among H. margalefi populations resulting from deep phylogeographical breaks, some dating back to the Oligo‐Miocene. Whether looking at the intralineage or interlineage levels, H. margalefi populations present a high genetic diversity and population structuring. This study suggests that the five distinct lineages observed in H. margalefi actually correspond to as many separate cryptic taxa. The nominal species, H. margalefi sensu stricto, corresponds to the westernmost lineage here surveyed from the Alboran Sea to southeastern Italy. Typical genetic breaks such as the Almeria‐Oran Front or the Siculo‐Tunisian Strait do not appear to be influential on the studied loci in H. margalefi sensu stricto. Instead, population structuring appears more complex and subtle than usually found for model species with a pelagic dispersal phase. The remaining four cryptic taxa are all found in the eastern basin, but incomplete lineage sorting is suspected and speciation might still be in process. Present‐day population structure of the different H. margalefi cryptic species appears to result from past vicariance events started in the Oligo‐Miocene and maintained by present‐day coastal topography, water circulation and habitat fragmentation.     

Grateloupia turuturu (Halymeniaceae,Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora

Grateloupia doryphora (Montagne) Howe, originally described from Peru, has repeatedly been reported as an invasive species in Atlantic and Mediterranean waters. Various attempts to explain this species' route of introduction have been unsatisfactory. New evidence from comparative rbcL sequence analysis and morphology suggests that this adventive species in the NE and NW Atlantic corresponds with G. turuturu Yamada, originally described from Japan. This provenance follows a well-recognized trend of invasive marine organisms that have colonized the Atlantic Ocean and Mediterranean Sea from Pacific NE Asia.     

Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters

Colossendeis megalonyx Hoek, 1881 is a widespread and abundant pycnogonid in the Southern Ocean which has also been reported from the South Atlantic and South Pacific Oceans. Its strictly benthic lifestyle is expected to promote genetic differentiation among populations and ultimately facilitate speciation. On the other hand, the reported eurybathy and unknown larval stages of this species may allow Colossendeis megalonyx to maintain genetic continuity between isolated shallow-water habitats by active dispersal through the deep sea or by passive rafting on floating substrates. Thus, it remains unknown whether and to which extent geographically separated populations of Colossendeis megalonyx maintain gene flow in the Southern Ocean. We sampled 96 specimens of Colossendeis megalonyx from three stations in the Atlantic Sector of the Southern Ocean and one station from the South American continental shelf (Burdwood Bank). The genetic structure of nominal Colossendeis megalonyx as well as its phylogenetic position within the genus Colossendeis were assessed using a fragment of the cytochrome c oxidase subunit 1 gene. Our data strongly support that nominal Colossendeis megalonyx consists of at least five cryptic and one pseudocryptic mitochondrial lineages, four of which appear to be geographically restricted. Two lineages occurred at locations separated by more than 1,000 km in the Antarctic, thus indicating high levels of gene flow or recent colonization. No haplotype sharing across the Polar Frontal Zone was observed. Our results strongly suggest that cryptic speciation occurred within the genus Colossendeis. The wide biogeographic distribution range of Colossendeis megalonyx and perhaps that of other Antarctic pycnogonids should therefore be regarded with caution.     

Divergent sympatric lineages of the Atlantic and Indian Ocean crinoid Tropiometra carinata

The shallow water comatulid crinoid Tropiometra carinata is native to both the Atlantic and Indian Oceans, a distribution anomalous among shallow water crinoids and many other broadcast spawning species. Given this species' short pelagic larval duration, the findings of previous work that suggest that the Benguela upwelling is a significant barrier to gene flow in broadcast spawning species, and T. carinata's unexpected geographic distribution, we predicted that the crinoids presently recognized as T. carinata consisted of a species complex. To test this prediction, we sequenced a portion of the mitochondrial cytochrome oxidase 1 gene from 30 individuals of T. carinata collected from Brazil, the Mozambique Channel, Madagascar, and Reunion Island. We found that nucleotide divergence ranged 0.02–3.10% among haplotypes. Moreover, while a Bayesian phylogenetic tree indicated that there were two substantially divergent genetic lineages, there was no evidence to support that T. carinata is comprised of a species complex due to isolation‐by‐distance. Surprisingly, both lineages were found in sympatry in both the Atlantic and Indian Oceans. Likewise, a 95% parsimony haplotype network revealed that identical haplotypes are found in both oceans, suggesting that a species complex may indeed exist, just not one caused by geographic isolation. We discuss possible explanations for this unexpected genetic structure, such as natural dispersal or human‐mediated movement, and how the genetic structure found here is relevant to other marine organisms and to cryptic speciation.     

A three‐way contact zone between forms of Patella rustica (Mollusca: Patellidae) in the central Mediterranean Sea

Previous studies have reported the occurrence of three differentiated mtDNA lineages within Patella rustica in the Mediterranean Sea. Two hypotheses have been proposed to explain these observations: (1) the maintenance of ancestral polymorphism within a single species; (2) the occurrence of cryptic species not identified previously. To distinguish between these hypotheses, we screened the genetic variability at nine allozyme loci, an intron from the α‐amylase gene and a mitochondrial gene for 187 individuals of P. rustica sampled from seven Mediterranean localities. Eight additional localities were screened for the last two markers to place the differentiated lineages in a clear geographic context. Our results demonstrate that the three mtDNA lineages correspond to three distinct nuclear genotype clusters and provide further details on their distribution: the cluster corresponding to the mtDNA lineage from the Atlantic and western Mediterranean extends as far as the south coast of Italy, whereas the remaining two clusters occur in sympatry in the eastern Mediterranean. One of the eastern Mediterranean clusters is highly differentiated and seems to be reproductively isolated from the codistributed form; we therefore suggest that it corresponds to a new species. The remaining two clusters are less differentiated and form a contact zone across south Italian shores. This three‐way contact zone constitutes an interesting model for the study of speciation in the marine realm. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 154–169.     

Unexpected mosaic distribution of two hybridizing sibling lineages in the teleplanically dispersing snail Stramonita haemastoma suggests unusual postglacial redistribution or cryptic invasion

Molecular approaches have proven efficient to identify cryptic lineages within single taxonomic entities. Sometimes these cryptic lineages maybe previously unreported or unknown invasive taxa. The genetic structure of the marine gastropod Stramonita haemastoma has been examined in the Western Mediterranean and North‐Eastern Atlantic populations with mtDNA COI sequences and three newly developed microsatellite markers. We identified two cryptic lineages, differentially fixed for alternative mtDNA COI haplogroups and significantly differentiated at microsatellite loci. The mosaic distribution of the two lineages is unusual for a warm‐temperate marine invertebrate with a teleplanic larval stage. The Atlantic lineage was unexpectedly observed as a patch enclosed in the north of the Western Mediterranean Sea between eastern Spain and the French Riviera, and the Mediterranean lineage was found in Macronesian Islands. Although cyto‐nuclear disequilibrium is globally maintained, asymmetric introgression occurs in the Spanish region where the two lineages co‐occur in a hybrid zone. A first interpretation of our results is mito‐nuclear discordance in a stable postglacial hybrid zone. Under this hypothesis, though, the location of genetic discontinuities would be unusual among planktonic dispersers. An alternative interpretation is that the Atlantic lineage, also found in Senegal and Venezuela, has been introduced by human activities in the Mediterranean area and is introgressing Mediterranean genes during its propagation, as theoretically expected. This second hypothesis would add an additional example to the growing list of cryptic marine invasions revealed by molecular studies.     

Multiple transisthmian divergences,extensive cryptic diversity,occasional long‐distance dispersal,and biogeographic patterns in a marine coastal isopod with an amphi‐American distribution

Excirolana braziliensis is a coastal intertidal isopod with a broad distribution spanning the Atlantic and Pacific tropical and temperate coasts of the American continent. Two separate regional studies (one in Panama and one in Chile) revealed the presence of highly genetically divergent lineages, implying that this taxon constitutes a cryptic species complex. The relationships among the lineages found in these two different regions and in the rest of the distribution, however, remain unknown. To better understand the phylogeographic patterns of E. braziliensis, we conducted phylogenetic analyses of specimens from much of its entire range. We obtained DNA sequences for fragments of four mitochondrial genes (16S rDNA, 12S rDNA, COI, and Cytb) and also used publicly available sequences. We conducted maximum likelihood and Bayesian phylogenetic reconstruction methods. Phylogeographic patterns revealed the following: (1) new highly divergent lineages of E. braziliensis; (2) three instances of Atlantic–Pacific divergences, some of which appear to predate the closure of the Isthmus of Panama; (3) the distributional limit of highly divergent lineages found in Brazil coincides with the boundary between two major marine coastal provinces; (4) evidence of recent long‐distance dispersal in the Caribbean; and (5) populations in the Gulf of California have closer affinities with lineages further south in the Pacific, which contrasts with the closer affinity with the Caribbean reported for other intertidal organisms. The high levels of cryptic diversity detected also bring about challenges for the conservation of this isopod and its fragile environment, the sandy shores. Our findings underscore the importance of comprehensive geographic sampling for phylogeographic and taxonomical studies of broadly distributed putative species harboring extensive cryptic diversity.     

A molecular phylogenetic appraisal of the systematics of the Aglaopheniidae (Cnidaria: Hydrozoa,Leptothecata) from the north‐east Atlantic and west Mediterranean

The hydrozoan family Aglaopheniidae (Cnidaria) is widespread worldwide and contains some of the most easily recognizable hydroids because of their large colony size and characteristic microscopic structure. The systematics of the group has, however, been controversial and dedicated molecular analyses are lacking. We therefore analysed existing and new 16S rRNA sequences of Aglaopheniidae, in a total of 98 16S sequences corresponding to 25 putative species (25 nominal and three undescribed) from seven genera. The monophyly of the subfamilies Gymnangiinae and Aglaopheniinae, and tribes Aglaopheniini and Cladocarpini were not verified with 16S sequence data. The genera Gymnangium and Aglaophenia can only be considered valid if both Gymnangium gracicaule and Aglaophenia latecarinata are removed from their respective genera. The phenotypically similar Cladocarpus and Streptocaulus are probably monophyletic and clearly distinct genetically. The genus Lytocarpia may be polyphyletic. The nominal species Aglaophenia pluma, Aglaophenia tubiformis, and Aglaophenia octodonta are probably conspecific, as are also the species Aglaophenia acacia and Aglaophenia elongata. The 16S data revealed the existence of two potentially unnamed species of Aglaophenia respectively from the Azores and Madeira. The phylogeographical structure of the taxa with the greatest representation of haplotypes from the north‐east Atlantic and Mediterranean, revealed the influence of Mediterranean waters in Madeira and the Azores, and gene flow between deep waters of the Mediterranean and Atlantic. The last glaciations in Europe may have caused genetic bottlenecks but also high intraspecific haplotype diversity. Finally, Macrorhynchia philippina was detected in samples from Madeira and possibly represents an invasive species. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164 , 717–727.     

A complex species complex: The controversial role of ecology and biogeography in the evolutionary history of Syllis gracilis Grube, 1840 (Annelida,Syllidae)

The cryptic diversity in the polychaete Syllis gracilis Grube, 1840, in the Mediterranean Sea was examined with an integrative morpho-molecular approach. Individuals of S. gracilis were collected at eleven Mediterranean localities to provide an insight into the role of brackish environments in inducing cryptic speciation. The examination of morphological features combined with a molecular genetic analysis based on a partial sequence of the 16S rRNA gene highlighted discrepancies between morphological and molecular diversity. Morphological data allowed to identify a morphotype with short appendages occurring in coralline algae communities and another one with long appendages observed in brackish-water environments and Sabellaria reefs. Multivariate analyses showed that sampling localities were the greatest source of morphological divergence, suggesting that phenotypic plasticity may play a role in local adaptations of S. gracilis populations. Molecular data showed the occurrence of four divergent lineages not corresponding to morphological clusters. Different species delimitation tests gave conflicting results, retrieving, however, at least four separated entities. Some lineages occurred in sympatry and were equally distributed in marine and brackish-water environments, excluding a biogeographic or ecological explanation of the observed pattern and suggesting instead ancient separation between lineages and secondary contact. The co-occurrence of different lineages hindered the identification of the lineage corresponding to S. gracilis sensu stricto. The discrepancy between morphological and molecular diversity suggests that different environmental and biogeographic features may interact in a complex and unpredictable way in shaping diversity patterns. An integrative approach is needed to provide a satisfactory insight on evolutionary processes in marine invertebrates.     

Polymorphism in a common Atlantic reef coral (Montastraea cavernosa) and its long-term evolutionary implications

Recent advances in morphometrics and genetics have led to the discovery of numerous cryptic species in coral reef ecosystems. A prime example is the Montastraea annularis scleractinian coral species complex, in which morphological, genetic, and reproductive data concur on species boundaries, allowing evaluation of long-term patterns of speciation and evolutionary innovation. Here we test for cryptic species in the Atlantic species, Montastraea cavernosa, long recognized as polymorphic. Our modern samples consist of 94 colonies collected at four locations (Belize, Panamá, Puerto Rico in the Caribbean; S?o Tomé in the Eastern Atlantic). Our fossil samples consist of 78 colonies from the Plio-Pleistocene of Costa Rica and Panamá. Landmark morphometric data were collected on thin sections of 46 modern and 78 fossil colonies. Mahalanobis distances between colonies were calculated using Bookstein coordinates, revealing two modern and four fossil morphotypes. The remaining 48 of the 94 modern colonies were assigned to morphotype using discriminant analysis of calical measurements. Cross-tabulation and multiple comparisons tests show no significant morphological differences among geographic locations or water depths. Patterns of variation within and among fossil morphotypes are similar to modern morphotypes. DNA sequence data were collected for two polymorphic nuclear loci (β-tub1 and β-tub2) on all 94 modern colonies. Haplotype networks show that both genes consist of two clades, but morphotypes are not associated with genetic clades. Genotype frequencies and two-locus genotype assignments indicate genetic exchange across clades, and ϕst values show no genetic differentiation between morphotypes at different locations. Taken together, our morphological and genetic results do not provide evidence for cryptic species in M. cavernosa, but indicate instead that this species has an unusually high degree of polymorphism over a wide geographic area and persisting for >25 million years (myr).     

Phylogeography of the common ragworm Hediste diversicolor (Polychaeta: Nereididae) reveals cryptic diversity and multiple colonization events across its distribution

Previous studies on the common ragworm Hediste diversicolor (Polychaeta: Nereididae) revealed a marked genetic fragmentation across its distribution and the occurrence of sibling taxa in the Baltic Sea. These results suggested that the phylogeographic patterns of H. diversicolor could reflect interactions between cryptic differentiation and multiple colonization events. This study aims to describe the large-scale genetic structuring of H. diversicolor and to trace the phylogeographic origins of the genetic types described in the Baltic Sea. Samples of H. diversicolor (2 <  n  < 28) were collected at 16 locations across the NE Atlantic coasts of Europe and Morocco and in the Mediterranean, Black and Caspian Seas and sequenced at two mitochondrial gene fragments (COI and cyt b , 345 and 290 bp, respectively). Bayesian analyses revealed deep phylogeographic splits yielding three main clades corresponding to populations (i) from the NE Atlantic coasts (from Germany to Morocco) and from part of the Western Mediterranean, (ii) from the Mediterranean Sea, and (iii) from the Black and Caspian Seas. These clades are further divided in well-supported subclades including populations from different regions of NE Atlantic and Mediterranean (i.e. Portugal/Morocco, Western Mediterranean, Adriatic Sea). The Baltic Sea comprises three sympatric lineages sharing a common evolutionary history with populations from NE Atlantic, Western Mediterranean and Black/Caspian Seas, respectively. Hence, the current patterns of genetic structuring of H. diversicolor appear as the result of allopatric isolation, multiple colonization events and possible adaptation to local environmental conditions.     

Reappraisal and range extension of non-indigenous Mysidae (Crustacea, Mysida) in continental and coastal waters of eastern France

A survey of species belonging to the family Mysidae, conducted in June 2007 in fresh- to brackish waters of eastern France, revealed a recent range extension of the invasive Ponto-Caspian species Hemimysis anomala to the Moselle, Saône, and Rhône rivers. In the estuary of the Grand Rhône it reached for the first time the Mediterranean coast. The network of navigation canals in NE France was likely a key element of its north to south pathway starting from the Rhine River. Important range extensions were also noted for Limnomysis benedeni in this network and in the Moselle River. The euryhaline species Neomysis integer, endemic in coastal waters of the NE Atlantic, was found in the Rhône delta, thus confirming previous very rare records in the 1930–1950s from the Mediterranean coast of France. Invasion mechanisms and pathways, expansion potential, and establishment conditions of the species are discussed.     

Three‐dimensional post‐glacial expansion and diversification of an exploited oceanic fish

Vertical divergence in marine organisms is being increasingly documented, yet much remains to be carried out to understand the role of depth in the context of phylogeographic reconstruction and the identification of management units. An ideal study system to address this issue is the beaked redfish, Sebastes mentella – one of four species of ‘redfish’ occurring in the North Atlantic – which is known for a widely distributed ‘shallow‐pelagic’ oceanic type inhabiting waters between 250 and 550 m, and a more localized ‘deep‐pelagic’ population dwelling between 550 and 800 m, in the oceanic habitat of the Irminger Sea. Here, we investigate the extent of population structure in relation to both depth and geographic spread of oceanic beaked redfish throughout most of its distribution range. By sequencing the mitochondrial control region of 261 redfish collected over a decadal interval, and combining 160 rhodopsin coding nuclear sequences and previously genotyped microsatellite data, we map the existence of two strongly divergent evolutionary lineages with significantly different distribution patterns and historical demography, and whose genetic variance is mostly explained by depth. Combined genetic data, analysed via independent approaches, are consistent with a Late Pleistocene lineage split, where segregation by depth probably resulted from the interplay of climatic and oceanographic processes with life history and behavioural traits. The ongoing process of diversification in North Atlantic S. mentella may serve as an ‘hourglass’ to understand speciation and adaptive radiation in Sebastes and in other marine taxa distributed across a depth gradient.     

Benthic hydroids (Cnidaria: Hydrozoa) from the Spanish Antarctic expedition Bentart 95

A total of 61 species of hydroids, belonging to 13 families and 23 genera, were found during the Spanish Antarctic expedition Bentart 95 with the RV Hespérides. Ten of the species were identified only to generic level. The dominance of the subclass Leptothecatae, with 57 species, was remarkable. The remaining four species belong to the subclass Anthoathecatae. By far the most diverse family was the Sertulariidae, with 25 species (41%), followed by Haleciidae with nine species (15%) and Kirchenpaueriidae with six (10%). The family Plumulariidae, represented by one species of Nemertesia, is recorded for the first time from Antarctic waters. Eudendrium scotti, Perarella clavata and Symplectoscyphus hero are each recorded for the second time. Symplectoscyphus with 11 species was the dominant genus. Almost 60% of the species diversity is concentrated in just a little more than the 20% of genera. Nearly 70% of the species are endemic to Antarctic waters and 90% of them are restricted to Antarctic or Antarctic/sub-Antarctic waters.     

Phylogeography and population genetics of the cryptic bonnethead shark Sphyrna aff. tiburo in Brazil and the Caribbean inferred from mtDNA markers

Resolving the identity, phylogeny and distribution of cryptic species within species complexes is an essential precursor to management. The bonnethead shark, Sphyrna tiburo, is a small coastal shark distributed in the Western Atlantic from North Carolina (U.S.A.) to southern Brazil. Genetic analyses based on mitochondrial markers revealed that bonnethead sharks comprise a species complex with at least two lineages in the Northwestern Atlantic and the Caribbean (S. tiburo and Sphyrna aff. tiburo, respectively). The phylogeographic and phylogenetic analysis of two mitochondrial markers [control region (mtCR) and cytochrome oxidase I (COI)] showed that bonnethead sharks from southeastern Brazil correspond to S. aff. tiburo, extending the distribution of this cryptic species >5000 km. Bonnethead shark populations are only managed in the U.S.A. and in the 2000s were considered to be regionally extinct or collapsed in southeast Brazil. The results indicate that there is significant genetic differentiation between S. aff. tiburo from Brazil and other populations from the Caribbean (Φ_ST = 0.9053, P < 0.000), which means that collapsed populations in the former are unlikely to be replenished from Caribbean immigration. The species identity of bonnethead sharks in the Southwest Atlantic and their relationship to North Atlantic and Caribbean populations still remains unresolved. Taxonomic revision and further sampling are required to reevaluate the status of the bonnethead shark complex through its distribution range.     

Global distribution of cryptic native,introduced and hybrid lineages in the widespread estuarine amphipod Ampithoe valida

Biological invasions can pose a severe threat to coastal ecosystems, but are difficult to track due to inaccurate species identifications and cryptic diversity. Here, we clarified the cryptic diversity and introduction history of the marine amphipod Ampithoe valida by sequencing a mtDNA locus from 683 individuals and genotyping 10,295 single-nucleotide polymorphisms (SNPs) for 349 individuals from Japan, North America and Argentina. The species complex consists of three cryptic lineages: two native Pacific and one native Atlantic mitochondrial lineage. It is likely that the complex originated in the North Pacific and dispersed to the north Atlantic via a trans-arctic exchange approximately 3 MYA. Non-native A. valida in Argentina have both Atlantic mitochondrial and nuclear genotypes, strongly indicating an introduction from eastern North America. In two eastern Pacific estuaries, San Francisco Bay and Humboldt Bay, California, genetic data indicate human-mediated hybridization of Atlantic and Pacific sources, and possible adaptive introgression of mitochondrial loci, nuclear loci, or both. The San Francisco Bay hybrid population periodically undergoes population outbreaks and profoundly damages eelgrass Zostera marina thalli via direct consumption, and these ecological impacts have not been documented elsewhere. We speculate that novel combinations of Atlantic and Pacific lineages could play a role in A. valida’s unique ecology in San Francisco Bay. Our results reinforce the notion that we can over-estimate the number of non-native invasions when there is cryptic native structure. Moreover, inference of demographic and evolutionary history from mitochondrial loci may be misleading without simultaneous survey of the nuclear genome.

     

Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa

One of the key hypotheses of paleoceanography is that planktonic foraminiferal morphospecies record reasonably stable and homogeneous oceanographic and climatic characteristics over their geographic and stratigraphic ranges. The discovery of numerous genetically-defined cryptic species challenges the morphospecies concept in planktonic foraminifera and paleoceanographic interpretations based on them. Here, we present a combined genetic and biometric analysis of Orbulina universa specimens in the Atlantic, Indian and Pacific Oceans. Our study is based on shells retained after DNA extractions. On those genotyped shells, we perform biometric analyses (shell size and thickness, inner porosity and pore surface distribution). Our genetic data confirm the presence of three cryptic species of O. universa in the world ocean, whose distributions are primarily correlated to the productivity of the surface waters. The Mediterranean species of O. universa is most abundant in the vertically mixed and nutrient-rich areas of the low to mid-latitudes, whereas the Caribbean and Sargasso species occur in stratified and oligotrophic subtropical waters. Our biometric data show no correlation between shell size and inner porosity within each cryptic species of O. universa. Combining Principal Component Analyses with MANOVAs performed on shell pore surface distribution, we demonstrate that the three different cryptic species are characterized by significant morphological differentiation. The Caribbean species typically exhibits large pores and higher porosity values, while the Mediterranean and Sargasso species are characterized by smaller pore areas and shell porosity. A model based upon pore surface distribution correctly assigns 60% to 90% of the specimens to their corresponding genotype. Although the inner shell surface of the Sargasso species resembles that of the Mediterranean species, our model demonstrates that the pore surface distributions of these two cryptic species can be distinguished. Finally, the Sargasso species exhibits significantly thinner shells than the two other cryptic species.