Pleistocene diversification of the Pomacentrus coelestis species complex (Pisces: Pomacentridae): historical biogeography and species boundaries

Pleistocene eustatic changes in sea level are often invoked to explain genetic divergence among marine organisms. However, molecular phylogenies have revealed relatively few examples of speciation events dating to the Pleistocene. We present a species-level hypothesis of the timing of evolution for the Pomacentrus coelestis species complex (Pomacentridae), based on the nuclear S7 intron and the mitochondrial Cytb gene, and reconstruct ancestral range distributions across the timetree. Ancestral range reconstruction suggests the complex originated in the Coral Triangle and East Indian Ocean, with subsequent range expansion outward from this region. We suggest that land barriers to dispersal (e.g., Indo-Pacific barrier) may be responsible for the divergence between Indian (P. alleni, P. similis, P. caeruleopunctatus, and P. caeruleus) and Pacific (P. micronesicus, P. auriventris, and P. coelestis) species groups, and subsequent isolation by Pleistocene sea-level fluctuations in certain areas of the Coral Triangle (glacial refugia) may play an important role in the diversification of this species complex. Additionally, our analyses show cryptic lineages within P. micronesicus and highlight the need for comprehensive sampling within and among species to reveal recent speciation events.     

Mitochondrial evolution and phylogeography in the hydrozoan<Emphasis Type="Italic"> Obelia geniculata</Emphasis> (Cnidaria)

The distribution and genetic structure of many marine invertebrates in the North Atlantic have been influenced by the Pleistocene glaciation, which caused local extinctions followed by recolonization in warmer periods. Mitochondrial DNA markers are typically used to reconstruct species histories. Here, two mitochondrial markers [16S rDNA and cytochrome c oxidase I (COI)] were used to study the evolution of the widely distributed hydrozoan Obelia geniculata (Linnaeus, 1758) from the North Atlantic and the Pacific and, more specifically, in the context of North Atlantic phylogeography. Samples were collected from six geographic localities between 1998 and 2002. Hydroids from the North Atlantic, North Pacific (Japan), and South Pacific (New Zealand) are reciprocally monophyletic and may represent cryptic species. Using portions of the 16S rDNA and COI genes and the date of the last trans-Arctic interchange (3.1–4.1 million years ago), the first calibrated rate of nucleotide substitutions in hydrozoans is presented. Whereas extremely low substitution rates have been reported in other cnidarians, mainly based on anthozoans, substitution rates in O. geniculata are comparable to other invertebrates. Despite a life history that ostensibly permits substantial dispersal, there is apparently considerable genetic differentiation in O. geniculata. Divergence estimates and the presence of unique haplotypes provide evidence for glacial refugia in Iceland and New Brunswick, Canada. A population in Massachusetts, USA, appears to represent a relatively recent colonization event.Communicated by J.P. Grassle, New Brunswick     

Post-glacial population history and genetic structure of the northern clingfish (Gobbiesox maeandricus), revealed from mtDNA analysis

Mitochondrial d-loop sequences were analyzed to characterize the phylogeographic and population genetic structure of the northern clingfish (Gobbiesox maeandricus Girard). Sequence analysis of 378 bp from 111 individuals sampled in 14 localities along the northeast Pacific coast and within the Strait of Georgia from 1996 to 1999 revealed marked genetic differentiation (Φ_ct=0.247) among regional population groupings. The gene genealogy distinguished two major clades of haplotypes separated by at least 1.1% sequence divergence. One clade with very low haplotype diversity (h=0.2095, n=18) occurred only within the recently unglaciated Strait of Georgia. The other clade had high haplotype diversity (h=0.8808, n=93) and was found in all populations. High haplotype diversity was found in open coastal populations, both north and south of the maximum extant of the Wisconsin ice sheet, suggesting that the clingfish range was not pushed to a southern refugium during the last glacial maximum. A nested clade analysis also did not detect a large northward expansion from a single southern refugium. The level of sequence divergence and coalescent-based analyses suggest that the observed patterns of polymorphism are the result of Pleistocene diversification within multiple refugia, followed by population expansion and asymmetrical lineage introgression. Received: 5 February 2000 / Accepted: 31 August 2000     

Genetic structure and phylogeography of the lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts

Marine invertebrates with high larval dispersal capacity typically exhibit low degrees of population differentiation, which reflects both contemporary and historical processes. We sampled 346 individuals from seven populations of the lined shore crab, Pachygrapsus crassipes Randall, along the northeastern Pacific Coast and Korea during summer 2003. DNA sequence analysis of 613 bp of the mitochondrial COI gene showed that overall gene diversity (h) was high (0.92±0.01), whereas overall nucleotide diversity (π) was low (0.009±0.005). A total of 154 mtDNA haplotypes were identified; however, 114 were present in only one individual. Analysis of molecular variance revealed significant genetic structuring at Point Conception, CA, USA, that is likely due to the oceanographic circulation patterns, which result in asymmetrical migration of haplotypes. However, genetic variation among eastern Pacific populations was generally low, probably because of high contemporary gene flow and recent common ancestry of haplotypes. Mismatch analysis and nested clade analysis suggested that the population history of this region is characterized by two contiguous northwards range expansions, which are congruent with Late Pleistocene glacial cycles. Highly significant genetic differentiation was detected between eastern Pacific populations and Korea, indicating transpacific gene flow is restricted. Time of divergence between the two transpacific lineages was estimated between 0.8 and 1.2 Myrs ago. The small, recently founded population of P. crassipes at Bamfield, BC, Canada, did not appear to have undergone a founder effect.     

Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range

The ocean quahog, Arctica islandica (Linnaeus, 1767), is a commercially important bivalve found on continental shelves throughout much of the North Atlantic. To assess genetic subdivision in this species, we sequenced 385 nucleotides of the mitochondrial cytochrome b (cyt b) gene from 83 specimens collected from 12 localities between September 1998 and July 1999 (based on preliminary data, the Internal Transcribed Spacers, ITS, of the nuclear ribosomal repeat were not useful). The cyt b data delimited 11 haplotypes with 0.26 to 8.1% nucleotide difference (coded by 36 variable nucleotide positions) among them. Only three haplotypes were detected in 39 specimens collected along the USA coastline, compared to five haplotypes from nine Icelandic individuals. The western Atlantic populations ranging from Penobscot Bay (Maine, USA) to southern Virginia showed relatively low diversity and appeared genetically similar in that region. Based on the presence of shared haplotypes, AMOVA analyses, and phylogenetic reconstructions, Icelandic populations appear to be more genetically similar to western Atlantic populations than eastern Atlantic populations. Specimens from the Faroe Islands (n=4) show mixed affinities. These data are consistent with the hypothesis that a warm Holocene climatic optimum (ca. 7,500 years BP), and not glacial refugia, shaped the present-day genetic structure in A. islandica. Received: 18 January 2000 / Accepted: 26 June 2000     

Divergence of mitochondrial DNA lineage of the rocky intertidal goby Chaenogobius gulosus around the Japanese Archipelago: reference to multiple Pleistocene isolation events in the Sea of Japan

Geographic variations in the mitochondrial cytochrome b gene sequence (1,062 nucleotides) of the rocky intertidal goby Chaenogobius gulosus were examined and compared against the phylogeographic pattern of its sympatric sister species Chaenogobius annularis, which we studied previously. We collected C. gulosus specimens from 17 localities around the Japanese Archipelago and Korean Peninsula. Thirty-one haplotypes were obtained. The phylogenetic tree showed three geographical lineages, of which one was distributed along the coast of the Sea of Japan, suggesting that a Pleistocene isolation event in the Sea of Japan affected the genetic divergence of this species, similar to that which was observed in C. annularis. The net nucleotide divergence between the Sea of Japan and Pacific Ocean lineages in C. gulosus was much lower than that of C. annularis. Both traditional molecular clock and hierarchical approximate Bayesian computational models suggest that different divergence events affected the genetic divergences of C. gulosus and C. annularis. Our study on the sister species pair strongly supports multiple isolation events in the Sea of Japan, leading to varying levels of genetic divergence between the Pacific Ocean and Sea of Japan lineages in the Japanese coastal marine species.     

Phylogeography of the European stalked barnacle (Pollicipes pollicipes): identification of glacial refugia

The alternation of glacial and interglacial events during the Pleistocene has produced changes in species distribution ranges leading to bottlenecks and alterations of patterns of gene flow. The European stalked barnacle, Pollicipes pollicipes, is a sessile pedunculate cirripede that inhabits the rocky intertidal frame, from Senegal to the northwestern coast of France. In this work, we have analyzed a fragment of the mitochondrial gene cytochrome c oxidase subunit I for 569 individuals of P. pollicipes in order to investigate whether the shifts in climatic conditions that occurred during the Pleistocene influenced the current pattern of distribution of genetic variation of P. pollicipes. A pre-last glacial maximum pattern of demographic expansion was found, in concordance with many other North Atlantic marine species. On the other hand, three potential glacial refugia were identified: North African coasts, northwestern Iberian Peninsula and English Channel/Brittany.     

Genetic structure of green turtle (Chelonia mydas) peripheral populations nesting in the northwestern Pacific rookeries: evidence for northern refugia and postglacial colonization

Several green turtle (Chelonia mydas) nesting populations have been reported in the northwestern Pacific region, the northernmost limit of its distribution range. However, the population history in this region as a whole is not well understood. To clarify how the green turtle nesting populations have evolved in the northwestern Pacific region, the genetic composition of mitochondrial DNA control region sequences in the northwestern Pacific was compared with that of the other Pacific populations. We analyzed 302 samples from the northwestern Pacific rookeries, including 78 newly collected samples from rookeries in the Ryukyu Archipelago, Japan (from 24.27°N, 123.76°E to 28.45°N, 129.61°E). Our results revealed that the northwestern Pacific populations consisted of one highly endemic lineage (Clade IV) in the northwestern Pacific rookeries and two other lineages (Clades I and V) which were widely observed in other Pacific populations. We concluded that the highly endemic lineage indicated that a refugial population existed in this region during the Last Glacial Maximum, and the other two lineages indicated that colonization from populations at lower latitudes occurred during interglacial periods. The green turtle nesting populations in the present periphery of their distribution range had been thought to have their origin in colonization from lower latitudes, which served as refugia during glacial periods. However, the present results indicated that the northwestern Pacific peripheral populations have been maintained on the evolutionary timescale of this species and should be treated as long-term conservation resources.     

Genetic structure in native and non-native populations of the direct-developing gastropod Crepidula convexa

In many marine invertebrate species, larval development plays an important role in population connectivity and gene flow: species with direct benthic development generally show more genetic structure than those with planktonic development. We used nuclear markers (microsatellites) to determine population genetic structure of the direct-developing snail Crepidula convexa (Gastropoda: Calyptraeidae) in seven populations with 15–85 individuals each within its native range of the northwest Atlantic and compared it to Crepidula fornicata, a congener with planktonic development. Our results are consistent with general expectations and previous work in these species with other markers: C. convexa had greater population structure and even at a regional scale shows significant isolation-by-distance, in contrast to C. fornicata. We also genotyped a single population of C. convexa introduced to the northeastern Pacific to investigate the prediction of reduced genetic diversity following introduction (founder effect). We did not find a reduction in genetic diversity, suggesting that this non-native population may be characterized by multiple introductions. This pattern is consistent with many other introduced populations of marine invertebrates, including C. fornicata.     

The cockle <Emphasis Type="Italic">Cerastoderma edule</Emphasis> at Northeast Atlantic shores: genetic signatures of glacial refugia

The cockle Cerastoderma (Cardium) edule (L.) ranges from NW Africa to northern Scandinavia. Abundance in shallow coastal sediment is often high, and it attracts commercial harvest. In this study, a complex genetic pattern has been revealed by mitochondrial DNA in 383 individuals from 19 sampling sites. Parsimony network analysis of 79 haplotypes identified two dominant central haplotypes separated by low divergence. One is characteristic for a homogenous southwestern group of populations from Africa to the British Isles. The other is characteristic for a heterogeneous northern group with a deviant Arctic population. At the entrance of the Baltic Sea, a mixture zone of the dominant haplotypes was found. The estimated population expansion time for the northern haplotype group predates that of the southwestern one, suggesting northern glacial refugia and a subsequent southern expansion of C. edule populations.     

Phylogeographic pattern and glacial refugia of a rocky shore species with limited dispersal capability: the case of Montagu’s blenny (Coryphoblennius galerita,Blenniidae)

Phylogeographic patterns among coastal fishes are expected to be influenced by distinct ecological, biological and life history traits, along with historical events and oceanography (past and present). This study focuses on the broad range phylogeography of the Montagu’s blenny Coryphoblennius galerita, a species with well-known ecological features, strictly tied to rocky environments and with limited dispersal capability. Eleven locations from the western Mediterranean to the Bay of Biscay (including the Macaronesian archipelagos) were sampled. Mitochondrial DNA control region (CR) and the first intron of the S7 ribosomal protein gene were used to address the population structure, the signatures of expansion/contraction events retained in the genealogies and potential glacial refugia. The genetic diversity of the Montagu’s blenny was high throughout the sampled area, reaching maximum values in the Mediterranean and western Iberian Peninsula. The results confirmed a marked structure of C. galerita along the sampled area, with a major separation found between the Mediterranean and the Atlantic populations, and suggesting also a separation between the Azores and the remaining Atlantic locations. This study revealed complex and deep genealogies for this species, with Montagu’s blenny populations presenting signatures of events clearly older than the Last Glacial Maximum, with lineages coalescing in early Pleistocene and Pliocene. Three potential glacial refugia where this species might have survived Pleistocene glaciations and from where the recolonization process might have taken place are suggested: South of Iberian Peninsula/North Africa, Mediterranean and Azores.     

Population variation in the mitochondrial cytochrome b gene of the orange roughy Hoplostethus atlanticus and the hoki Macruronus novaezelandiae

To describe the genetic relationship among regional populations of two commercially valuable species of marine fish, the orange roughy Hoplostethus atlanticus and the hoki Macruronus novaezelandiae, the mitochondrial (mt) DNA haplotypes of 59 individuals were defined by direct sequencing of the cytochrome b gene. Samples of orange roughy were collected on four fishing grounds around New Zealand, one off the west coast of Tasmania and one near South Africa from 1990–1991. Samples from hoki were collected on three fishing grounds around New Zealand and one off Tasmania during the same period. An average of 252 nucleotides were sequenced from each of 32 orange roughy and an average of 372 nucleotides from each of 27 hoki. Sequence variation allowed the definition of 9 unique orange roughy haplotypes and 5 hoki haplotypes. Genetic variation, as measured by both average sequence divergence and haplotype diversity, was high in the orange roughy (nucleotide diversity=0.590%, haplotype diversity=0.782) and low in the hoki (nucleotide diversity=0.076%, haplotype diversity=0.279) relative to a similar survey of the Atlantic cod, Gadus morhua. Differences in haplotype frequencies of orange roughy from New Zealand, Tasmania and South Africa were not significant, and the most common haplotype was found in similar frequencies in these three geographically distant regions. Differences in haplotype frequencies between the New Zealand and Tasmanian samples of hoki were significant, suggesting restricted gene flow between these two regions. The contrasting patterns of low but regionally subdivided genetic variation in the hoki versus high but geographically undifferentiated genetic variation in the orange roughy may be attributed to the low fecundity, slow maturation and long lifespan of the orange roughy relative to the hoki.     

Asymmetric genetic exchange in the brown seaweed Sargassum fusiforme (Phaeophyceae) driven by oceanic currents

Geological phenomena (e.g. drastic sea level fluctuations during the Quaternary Ice Age in the Northern Hemisphere) have been demonstrated to intensively affect the biogeographic patterns and tempo-spatial compositions of genetic diversity of marine organisms. However, it is poorly understood whether contemporary factors such as oceanic surface currents have also shaped inter-regional population genetics of specific coastal marine flora, with or without limited dispersal capability. In this study, we determined mtDNA Cox1 gene sequences of the brown seaweed Sargassum fusiforme from nine populations along the Chinese coast and one population from the west coast of South Korea, in an effort to understand what factors are contributing to their current genetic structure and geographic distribution patterns. Genetic analyses indicated a deep genetic break between the Yellow-Bohai Sea (YBS) and the other two marginal seas, the East China Sea (ECS) and the South China Sea (SCS). In particular, the amount of genetic exchange from the SCS to each of the ECS and YBS was significantly higher than that from the opposite directions. Our analyses supports the hypothesis that biogeographic patterns of genetic variation in S. fusiforme are probably an interactive consequence of post-glacial colonization from two scattered refugia driven by the offshore Kuroshio Current and asymmetric gene flow among adjacent sea margins.     

Effect of biogeographic history on population vulnerability in European amphibians

The genetic diversity of populations, which contributes greatly to their adaptive potential, is negatively affected by anthropogenic habitat fragmentation and destruction. However, continental‐scale losses of genetic diversity also resulted from the population expansions that followed the end of the last glaciation, an element that is rarely considered in a conservation context. We addressed this issue in a meta‐analysis in which we compared the spatial patterns of vulnerability of 18 widespread European amphibians in light of phylogeographic histories (glacial refugia and postglacial routes) and anthropogenic disturbances. Conservation statuses significantly worsened with distances from refugia, particularly in the context of industrial agriculture; human population density also had a negative effect. These findings suggest that features associated with the loss of genetic diversity in post‐glacial amphibian populations (such as enhanced fixation load or depressed adaptive potential) may increase their susceptibility to current threats (e.g., habitat fragmentation and pesticide use). We propose that the phylogeographic status of populations (i.e., refugial vs. post‐glacial) should be considered in conservation assessments for regional and national red lists.     

Deconstructing an assemblage of “turtle” barnacles: species assignments and fickle fidelity in Chelonibia

Barnacles in the genus Chelonibia are commensal with a variety of motile marine animals including sea turtles, crustaceans, and sirenians. We conducted a worldwide molecular phylogenetic survey of Chelonibia collected from nearly all known hosts to assess species relationships, host-fidelity, and phylogeographic structure. Using DNA sequences from a protein-coding mitochondrial gene (COI), a mitochondrial rRNA gene (12S), and one nuclear rRNA gene (28S), we found that of four species, three (C. testudinaria, C. patula, and C. manati) are genetically indistinguishable. In addition, we show each utilizes a rare androdioecious mode of reproduction involving complemental males. In contrast, the fourth species (C. caretta), which is hermaphroditic and specializes on turtles, is genetically distinct—leading to the conclusion that the three former taxa are morphotypes of the same species and should be synonymized under C. testudinaria. Phylogenetic analysis resulted in three geographic clades (Atlantic, Indian Ocean/western Pacific, and eastern Pacific) with haplotype parsimony networks revealing no shared haplotypes among geographic regions. Analysis of molecular variance detected significant differences among sequences by region (p < 0.005); conversely, there were no significant differences among sequences when grouped by host or taxonomic designation. Average pairwise genetic distances were lower between the eastern Pacific and Atlantic clades (0.053 ± 0.006) than between the eastern Pacific and Indian Ocean/western Pacific clades (0.073 ± 0.008), suggesting Atlantic and eastern Pacific populations were connected more recently, perhaps until the rise of the Isthmus of Panama. Host use by Chelonibia morphotypes is discussed along with speculation on possible ancestral hosts and support for a “turtle-first” hypothesis.     

Recent history of the European Nassarius nitidus (Gastropoda): phylogeographic evidence of glacial refugia and colonization pathways

Because marine species respond differentially to factors governing survival and gene flow, closely related taxa may display dissimilar phylogeographic histories. New data for the patchily distributed gastropod Nassarius nitidus throughout its Atlantic–Mediterranean range (collected during 2008 and 2009) were used to investigate its phylogeography and recent demography. Results based on mitochondrial COI sequences of 422?N. nitidus individuals from 15 localities revealed contrasting phylogeographic and demographic patterns among N. nitidus populations from each basin. Data suggest the existence of two glacial refugia, one in the Atlantic, around the Iberian Peninsula, and the other in the Paleo-Mediterranean Sea (Adriatic). Bayesian skyline reconstructions suggest that the Adriatic population of N. nitidus remained largely unaffected by the Last Glacial Maximum (LGM), whereas the Iberian Atlantic region experienced dramatic exponential growth after its conclusion. Contemporary North Sea populations of N. nitidus are the endpoint of a leading-edge recolonization process from a southern position. Additionally, a reanalysis of pre-existing material for the continuously distributed close congener N. reticulatus was used to compare both species in the late histories. In contrast to N. nitidus, N. reticulatus prospered during the LGM and experienced an earlier Atlantic expansion during the previous interglacial period. Despite similar life history and dispersal potential, the results here presented suggest that subtle differences in microhabitat requirements between the two species have had important consequences for their particular distribution in response to glacial events.     

Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific

Partial sequences of the mitochondrial DNA (mtDNA) gene cytochrome oxidase subunit 1 (COI) were analysed from individuals of the coralline demosponge Astrosclera willeyana sensu lato out of ten Indo-Pacific populations from the Red Sea to the central Pacific. This taxon is widely distributed in cryptic coral reef habitats of the Indo-Pacific and is regarded as a modern representative of long-extinct, formerly reef-building stromatoporoid-type sponges. The aims were to clarify phylogeographic and taxonomic relationships in this “living fossil” and to explore mitochondrial DNA sequence variation over a wide geographic range. Very low variability was observed across the Indo-Pacific, as only three COI haplotypes were identified, with a maximum p-distance of 0.418% and low nucleotide diversity (π=0.00049). Very low genetic structure was revealed among populations: Haplotype 1 was found in all specimens from nine Pacific populations (N=45), separated by distances of more than 7,000 km; haplotype 2 was restricted to the Red Sea population (N=4); haplotype 3 was only found in the Tuamoto specimens (N=7). COI data presented here do not support the hypothesis of at least two sibling species belonging to genus Astrosclera in the Pacific. Considering the maximum geographic distance of more than 20,000 km between sampled populations, mtDNA COI sequence variation observed here is among the lowest reported to date for a diploblastic taxon and adds to the growing evidence of a general mtDNA conservation in sponges. It is argued that this low mtDNA variation in A. willeyana s.l. is due to a low rate of mtDNA evolution caused by a combination of long generation time and low metabolic rate.     

Mitochondrial DNA evidence for rapid colonisation of the Indo–West Pacific by the mudcrab Scylla serrata

Scylla serrata (Forskål, 1775) is widely distributed throughout mangrove habitats of the Indo-West Pacific (IWP) coastal waters. This study investigated the phylogeographic distribution of S. serrata mitochondrial DNA haplotypes sampled throughout the species range. Adults were sampled from three west Indian Ocean locations (N?=?21), five west Pacific sites (N?=?28) and three sites from northern and eastern Australia (N?=?76). Temperature-gradient gel-electrophoresis and sequencing of 549 base pairs of a mtDNA gene (cytochrome oxidase 1) identified 18 distinct haplotypes. Haplotypes cluster into two clades separated by ?2% sequence-divergence. One clade is widespread throughout the IWP, the other is strictly confined to northern Australia. Genealogical assessment of sequenced haplotypes suggests that the historical spread of S. serrata throughout the IWP has occurred rapidly and recently (<1 million years before present) from a west Pacific origin. The fact that many locations contain a single unique haplotype suggests limited contemporary gene flow between trans-oceanic sites, and that recent historical episodes of population founding and retraction have both determined and affected the current distribution of S. serrata populations. Contrary to that reported for other widespread species of IWP taxa, there is no pattern of regional separation of Indian from Pacific Ocean populations. However, results do suggest a vicariant separation of northern Australian crabs prior to the IWP radiation. We speculate that this separation may have resulted in the formation of a new species of Scylla.     

RFLP analysis of the mtDNA control region in white shrimp (Litopenaeus vannamei) populations from the eastern Pacific

White shrimp (Litopenaeus vannamei) population genetic structure from the eastern Pacific was determined by restriction fragment length polymorphism analysis of the mitochondrial DNA control region. Four localities were surveyed with four endonucleases (Alu I, Taq I, Spe I, Ssp I) yielding 48 composite haplotypes. White shrimp showed high average within-locality haplotype (0.823) and nucleotide (5.41%) diversities and also high average nucleotide divergence between all pairs of localities (0.73%). A mismatch analysis of pairwise differences between haplotypes indicated that white shrimp does not fit the sudden population expansion model. An analysis of molecular variance showed significant geographic variation in the frequencies of haplotypes (Φ_ST=0.1382, P<0.0001). Population differentiation may be maintained by a combination of physical, oceanographic, and biological factors acting as barriers to gene flow among localities. Because of its high polymorphism, the control region might be useful as a genetic marker for monitoring genetic diversity in aquaculture stocks.     

Afro-Eurasia and the Americas present barriers to gene flow for the cosmopolitan neustonic nudibranch Glaucus atlanticus

Pelagic species have been traditionally thought to occupy vast, genetically interconnected, geographic ranges in an essentially homogeneous environment. Although this view has been challenged recently for some mesopelagic planktonic taxa, the population structure of hyponeustonic (surface-drifting) species remains unknown. Here, we test the hypothesis of panmixis in Glaucus atlanticus, a cosmopolitan neustonic nudibranch, by assessing the genetic differentiation of multiple representatives from a global neustonic sampling effort. Specimens were collected from all subtropical oceanic gyre systems (North Atlantic, South Atlantic, North Pacific, South Pacific, and Indian Ocean). We sequenced a fragment of the mitochondrial cytochrome oxidase I gene for 98 individuals and performed population structure, differentiation (analysis of molecular variance, spatial analysis of molecular variance, F _ST, Jost’s D), and molecular clock analyses. Our results indicate that G. atlanticus is not globally panmictic, but that populations appear to be panmictic within ocean basins. We detected several topologically ectopic haplotypes in the Atlantic Ocean, but the molecular clock analysis indicates that these have diverged from closely related Indo-Pacific haplotypes over 1.2 MYA, coinciding with cooling in waters around in the southern tip of Africa and resulting oceanographic changes. These data and the fact that G. atlanticus is not known from polar latitudes suggest that gene flow between ocean basins is hindered by physical barriers (supercontinents) and water temperatures in the Arctic and Southern Oceans.