Tethyan vicariance, relictualism and speciation: evidence from a global molecular phylogeny of the opisthobranch genus Bulla

Aim Our aims were: (1) to reconstruct a molecular phylogeny of the cephalaspidean opisthobranch genus Bulla, an inhabitant of shallow sedimentary environments; (2) to test if divergence times are consistent with Miocene and later vicariance among the four tropical marine biogeographical provinces; (3) to examine the phylogenetic status of possible Tethyan relict species; and (4) to infer the timing and causes of speciation events. Location Tropical and warm‐temperate regions of the Atlantic, Indo‐West Pacific, Australasia and eastern Pacific. Methods Ten of the 12 nominal species of Bulla were sampled, in a total sample of 65 individuals, together with cephalaspidean outgroups. Phylogenetic relationships were inferred by Bayesian analysis of partial sequences of the mitochondrial cytochrome c oxidase I (COI) and 16S rRNA and nuclear 28S rRNA genes. Divergence times and rates of evolution were estimated using uncorrelated relaxed‐clock Bayesian methods with fossil calibrations (based on literature review and examination of fossil specimens), implemented in beast . The geographical pattern of speciation was assessed by estimating the degree of overlap between sister lineages. Results Four clades were supported: Indo‐West Pacific (four species), Australasia (one species), Atlantic plus eastern Pacific (three species) and Atlantic (two species), with estimated mean ages of 35–46 Ma. Nominal species were monophyletic, but deep divergences were found within one Indo‐West Pacific and one West Atlantic species. Species‐level divergences occurred in the Miocene or earlier. The age of a sister relationship across the Isthmus of Panama was estimated at 7.9–32.1 Ma, and the divergence of a pair of sister species on either side of the Atlantic Ocean occurred 20.4–27.2 Ma. Main conclusions Fossils suggest that Bulla originated in the Tethys realm during the Middle Eocene. Average ages of the four main clades fall in the Eocene, and far pre‐date the 18–19 Ma closure of the Tethys Seaway. This discrepancy could indicate earlier vicariant events, selective extinction or errors of calibration. Similarly, the transisthmian divergence estimate far pre‐dates the uplift of the Panamanian Isthmus at about 3 Ma. Speciation events occurred in the Miocene, consistent with tectonic events in the central Indo‐West Pacific, isolation of the Arabian Sea by upwelling and westward trans‐Atlantic dispersal. Differences in habitat between sister species suggest that ecological speciation may also have played a role. The basal position of the Australasian species supports its interpretation as a Tethyan relict.     

Biogeographic responses to geodynamics: A key study all around the Oligo–Miocene Tethyan Seaway

Extensive terrestrial exchanges were initiated by the closure of the Tethyan Seaway during the Early Miocene. Proboscideans are among the most prominent African immigrants, which arrived in Eurasia about 19 Ma ago via the “Gomphotherium Landbridge”. Several distinct waves of continental migrations, however, document that the formation of this landbridge was a multiphase process. Until the closure, a marine faunal exchange was enabled via the Mesopotamian Trough and the Zagros Basin, as reflected by contributions of Indonesian corals in the Iranian basins and by the occurrence of “western” gastropods in Pakistan and India. Nevertheless, the emergence of the landbridge was preceded in the marine biosphere by first biogeographic divergences on both sides of the seaway already during Oligocene times (e.g. within the tridacnines and strombids). Around the closure event, the breakdown of biogeographic relations was near-complete and the Proto-Mediterranean faunas bear little in common with those of the Indo-West Pacific Region (IWPR). Some of the discussed examples suggest that the Western Tethys Region (WTR) had acted as centre of origin and diversity during Oligocene and Early Miocene times. After the closure of the seaway, this centre had shifted to the southeast, heralding the enormous biodiversity of the modern IWPR. Some originally WTR elements managed to follow this shift and formed the Miocene stock for the modern IWPR faunas. In contrast, the marine fauna in the Mediterranean cul-de-sac suffered strong impoverishment due to the Miocene cooling, the Messinian Salinity Crisis and the late Pliocene and Pleistocene glacials – a fact which might explain the receptivity of the Mediterranean Sea for Lessepsian migrants.

This synthesis tries to document the practical problem of recognising biogeographic patterns despite the heterochronous developments in different systematic groups, which, in addition, are often obscured by a stratigraphically incomplete and geographically patchy fossil record.     

中国长臂虾总科的动物地理学特点

本文讨论了长臂虾总科在中国分布的3个科,即拟贝隐虾科、叶颚虾科和长臂虾科的属、种在中国的分布情况及区系特点。拟贝隐虾科和叶颚虾科种类较少,分布于热带海域,我国分别在南沙群岛和西沙群岛发现1属1种和3属3种,均为广布的常见种。长臂虾科是本总科中种类最多、分布最广、十分常见的科,包括2亚科102属,世界性分布,海洋、淡水均有,我国大量分布。其起源中心应在印度－西太平洋暖水区,一部分浅海沿岸种经河口进入淡水水域, 大量发展,很少种可分布至温带区边缘;另一部分在热带珊瑚礁环境大量发展,并与许多动物类群共栖或共生。长臂虾亚科基本上是浅海－淡水自由生活类群,我国已记录9属61种,主要分布于南部,多数为东洋界热带和亚热带种,分别属东洋界(淡水)和印度－西太平洋区(海水、半咸水);而极少数种分布至北方,温带性的淡水种有2种白虾,1种小长臂虾和仅见于东北部的条纹长臂虾,属于古北界区系(淡水),海水种有黄、东海的敖氏长臂虾及细指长臂虾,属于北太平洋温带区系(海水、半咸水)。隐虾亚科全部为海洋种,主要分布在热带、亚热带海域,以珊瑚礁为主要栖息地,大部分分布于印度－西太平洋海域,80%以上的种类或多或少与其他海洋生物共栖,自由生活的种很少。根据推论,隐虾类的起源中心应在印度－西太平洋热带水域的珊瑚礁环境, 并在这一水域得到了充分的分化与发展,分别适应与腔肠动物、双壳类软体动物、海绵动物、棘皮动物和海鞘类被囊动物共栖生活;而热带美洲的类群则是在隐虾类演化到可与石珊瑚类共栖时由印度－西太平洋水域扩散过去的, 共栖宿主仅涉及腔肠动物和棘皮动物。我国南海水域已发现31属96种,极少数种也分布到东海,属于印度－西太平洋热带水域珊瑚礁区系。     

Biogeographic patterns in major marine realms: function not taxonomy unites fish assemblages in reef,seagrass and mangrove systems

We examine the effects of different biogeographic histories on assemblage composition in three major marine habitats in two biogeographically distinct marine realms. Specifically, we quantify the taxonomic and functional composition of fish assemblages that characterise coral reef, seagrass and mangrove habitats, to explore the potential effects of biogeographic history and environment on assemblage composition. The three habitats were surveyed in the Caribbean and on the Great Barrier Reef using a standardised underwater visual census method to record fish size and abundance data. The taxonomic composition of assemblages followed biogeographic expectations, with realm‐specific family‐level compositions. In marked contrast, the functional composition of assemblages separated habitats regardless of their biogeographic locations. In essence, taxonomy characterises biogeographic realms while functional groups characterise habitats. The Caribbean and Indo‐West Pacific have been separated for approximately 15 million years. The two realms have different taxonomic structures which reflect this extended separation, however, the three dominant shallow‐water marine habitats all retain distinct functional characteristics: seagrass fishes are functionally similar regardless of their taxonomic composition or biogeographic location. Likewise, for coral reefs and mangroves. The results emphasise the advantages and limitations of taxonomic vs. functional metrics in evaluating patterns. Taxonomy primarily reflects biogeographic and evolutionary history while functional characteristics may better reflect ecological constraints.     

Marine shelf habitat: biogeography and evolution

We synthesize the evolutionary implications of recent advances in the fields of phylogeography, biogeography and palaeogeography for shallow‐water marine species, focusing on marine speciation and the relationships among the biogeographic regions and provinces of the world. A recent revision of biogeographic provinces has resulted in the recognition of several new provinces and a re‐evaluation of provincial relationships. These changes, and the information that led to them, make possible a clarification of distributional dynamics and evolutionary consequences. Most of the new conclusions pertain to biodiversity hotspots in the tropical Atlantic, tropical Indo‐West Pacific, cold‐temperate North Pacific, and the cold Southern Ocean. The emphasis is on the fish fauna, although comparative information on invertebrates is utilized when possible. Although marine biogeographic provinces are characterized by endemism and thus demonstrate evolutionary innovation, dominant species appear to arise within smaller centres of high species diversity and maximum interspecies competition. Species continually disperse from such centres of origin and are readily accommodated in less diverse areas. Thus, the diversity centres increase or maintain species diversity within their areas of influence, and are part of a global system responsible for the maintenance of biodiversity over much of the marine world.     

Biogeography,habitat transitions and hybridization in a radiation of South American silverside fishes revealed by mitochondrial and genomic RAD data

Rivers and lake systems in the southern cone of South America have been widely influenced by historical glaciations, carrying important implications for the evolution of aquatic organisms, including prompting transitions between marine and freshwater habitats and by triggering hybridization among incipient species via waterway connectivity and stream capture events. Silverside fishes (Odontesthes) in the region comprise a radiation of 19 marine and freshwater species that have been hypothesized on the basis of morphological or mitochondrial DNA data to have either transitioned repeatedly into continental waters from the sea or colonized marine habitats following freshwater diversification. New double digest restriction‐site associated DNA data presented here provide a robust framework to investigate the biogeographical history of and habitat transitions in Odontesthes. We show that Odontesthes silversides originally diversified in the Pacific but independently colonized the Atlantic three times, producing three independent marine‐to‐freshwater transitions. Our results also indicate recent introgression of marine mitochondrial haplotypes into two freshwater clades, with more recurring instances of hybridization among Atlantic‐ versus Pacific‐slope species. In Pacific freshwater drainages, hybridization with a marine species appears to be geographically isolated and may be related to glaciation events. Substantial structural differences of estuarine gradients between these two geographical areas may have influenced the frequency, intensity and evolutionary effects of hybridization events.     

Molecular phylogenetics and biogeography of transisthmian and amphi-Atlantic needlefishes (Belonidae: Strongylura and Tylosurus): perspectives on New World marine speciation

Phylogenetic relationships among New World and eastern Atlantic species in the belonid genera Strongylura and Tylosurus were hypothesized using 3689bp of nucleotide sequence; including the entire mitochondrial (mtDNA) ATP synthase 6 and 8 genes; partial cytochrome b; 12S and 16S ribosomal genes; and introns and exons, 2 and 3 of the nuclear-encoded creatine kinase B gene. Concordant mtDNA and nuclear genealogies permitted well-supported inference of species relationships within Strongylura and Tylosurus, and of the chronology of diversification in the two genera. Our phylogenetic hypothesis permitted an assessment of Rosen's [Syst. Zool. 24 (1975) 431] model of species diversification across the eastern Atlantic to eastern Pacific marine biogeographic track. The spatial predictions of the Rosen model were generally supported, but not the temporal predictions. Furthermore, long branches leading to terminal Belonidae indicated that many species have persisted for millions of years or that nucleotide substitution rates were elevated for some clades. Though heterogeneity of nucleotide substitution rate was indicated across some belonid lineages, molecular clock estimates were used to hypothesize biogeographic scenarios for Strongylura across the eastern Pacific and Atlantic region. Furthermore, use of a molecular clock indicated; that early diversification among contemporary Strongylura may have been initiated by changes in Atlantic Ocean circulation precipitated by closure of the Tethys Sea; and provided approximate dates for the isolation of the freshwater species on the American continents.     

Provenance Of Atlantic Lingulid Brachiopods

Living lingulid brachiopods are ubiquitous in low-latitude, marine infaunas. Lingula occurs throughout the Pacific and Indian oceans with the only Atlantic species, L. parva, confined to West Africa. Glottidia is restricted to offshore America from Virginia to California and Peru, and is assumed to have descended from a Pacific Lingula during the early Tertiary. Lingulid organophosphatic shells differ structurally. That of Glottidia is characterizedby trellised rods (baculate); that of Indo-Pacific species of Lingula by spheroidal and rod-like microstructures (virgose); and that of L. parva by apatitic rods arranged as spherulites. A spherulitic fabric is unknown in fossil lingulids, but the distinction between GlottidiaLingula can be traced back to the Carboniferous, which accords with the deep molecular divergence between the two genera. The common occurrence of lingulids with baculate shells in European post-Palaeozoic sediments suggests that ancestral Glottidia entered the Atlantic by the Tethyan Current during the Late Cretaceous/early Cenozoic, and migrated into the Pacific before the formation of the Panama Isthmus. Penecontemporaneously, antecedents of L. parva possibly migrated from east Tethys along the trans-Saharan seaway.     

Historical colonization and demography of the Mediterranean damselfish, Chromis chromis

The desiccation of the Mediterranean Sea during the Messinian Salinity Crisis 6.0-5.3 million years ago (Ma), caused a major extinction of the marine ichthyofauna of the Mediterranean. This was followed by an abrupt replenishment of the Mediterranean from the Atlantic after the opening of the Strait of Gibraltar. In this study, we combined demographic and phylogeographic approaches using mitochondrial and nuclear DNA markers to test the alternative hypotheses of where (Atlantic or Mediterranean) and when (before or after the Messinian Salinity Crisis) speciation occurred in the Mediterranean damselfish, Chromis chromis. The closely related geminate transisthmian pair Chromis multilineata and Chromis atrilobata was used as a way of obtaining an internally calibrated molecular clock. We estimated C. chromis speciation timing both by determining the time of divergence between C. chromis and its Atlantic sister species Chromis limbata (0.93-3.26 Ma depending on the molecular marker used, e.g. 1.23-1.39 Ma for the control region), and by determining the time of coalescence for C. chromis based on mitochondrial control region sequences (0.14-0.21 Ma). The time of speciation of C. chromis was always posterior to the replenishment of the Mediterranean basin, after the Messinian Salinity Crisis. Within the Mediterranean, C. chromis population structure and demographic characteristics revealed a genetic break at the Peloponnese, Greece, with directional and eastbound gene flow between western and eastern groups. The eastern group was found to be more recent and with a faster growing population (coalescent time = 0.09-0.13 Ma, growth = 485.3) than the western group (coalescent time = 0.13-0.20 Ma, growth = 325.6). Our data thus suggested a western origin of C. chromis, most likely within the Mediterranean. Low sea water levels during the glacial periods, the hydrographic regime of the Mediterranean and dispersal restriction during the short pelagic larval phase of C. chromis (18-19 days) have probably played an important role in C. chromis historical colonization.     

The Messinian marine molluscs record and the dawn of the eastern Atlantic biogeography

The biological impact of the Messinian Salinity Crisis (MSC) and its bearing on the Pliocene Mediterranean marine molluscan fauna has been analyzed on the basis of the biogeographic and stratigraphic distributions of the taxa of 16 early Messinian outcrops. The extinction of the last paleoendemic Proto-Mediterranean taxa is historically significant but it appears to be numerically less important than the extinction of the Tortonian and Messinian neoendemic taxa. The available data suggest that the MSC caused a regional mass disappearance but only a limited number of extinctions. It is also emphasized that the Late Pliocene (Monegatti et al., 2002) extinctions were far heavier than those caused by the MSC. We suggest that the greatest Messinian extinctions were triggered, during the salinity crisis, in the Atlantic “sanctuary” by the Messinian glacial events TG22, TG20, TG14, and TG12, of Shackleton et al. (1994), dated between 5.79 and 5.55 Ma by Krijgsman et al. (2004). A comparison between the Mediterranean Messinian and the Redonian molluscan faunas was also carried out. Finally, the possible latitudinal stability of the climatic thresholds, despite the shifting of the climatic zones throughout the Neogene along the European coast, is pointed out.     

Species Diversity,Phylogeny and Large Scale Biogeographic Patterns of the Genus Padina (Phaeophyceae,Dictyotales)

The brown algal genus Padina (Dictyotales, Phaeophyceae) is distributed worldwide in tropical and temperate seas. Global species diversity and distribution ranges, however, remain largely unknown. Species‐level diversity was reassessed using DNA‐based, algorithmic species delineation techniques based on cox3 and rbcL sequence data from 221 specimens collected worldwide. This resulted in estimates ranging from 39 to 61 putative species (ESUs), depending on the technique as well as the locus. We discuss the merits, potential pitfalls, and evolutionary and biogeographic significance of algorithmic species delineation. We unveil patterns whereby ESUs are in all but one case restricted to either the Atlantic or Indo‐Pacific Ocean. Within ocean basins we find evidence for the vast majority of ESUs to be confined to a single marine realm. Exceptions, whereby ESUs span up to three realms, are located in the Indo‐Pacific Ocean. Patterns of range‐restricted species likely arise by repeated founder events and subsequent peripatric speciation, hypothesized to dominate speciation mechanisms for coastal marine organisms in the Indo‐Pacific. Using a three‐gene (cox3, psaA and rbcL), relaxed molecular clock phylogenetic analysis we estimated divergence times, providing a historical framework to interpret biogeographic patterns.     

Oligocene and Early Miocene gastropods from Kutch (NW India) document an early biogeographic switch from Western Tethys to Indo-Pacific

Shallow marine gastropod assemblages from Chattian, Aquitanian and Burdigalian sections in the Indian Kutch Basin are described. They provide insight into the composition and biogeographic relations of the gastropod assemblages at this junction between the Western Tethys and Proto-Indo-Pacific Ocean. For the first time, an improved biostratigraphy allows a clear separation of the assemblages, especially for the hitherto undifferentiated Early Miocene faunas. Throughout the Oligocene, about one-third of the species are also frequently found in the Western Tethys, documenting a passable Tethyan Seaway for nearshore molluscs. A considerable provincialism is evident as well. The expected turnover during the Early Miocene, due to the closing of the Tethyan Seaway, is reflected in the Miocene assemblages. Surprisingly, however, the cut appears very early, i.e. already during the Aquitanian, when the West–East interrelation drops to zero despite the passage having been open during this interval. In contrast, the Burdigalian assemblages witness a minor re-appearance of Western Tethys taxa, suggesting the re-establishment of rather ineffective migration pathways prior to the final closure of the Tethyan Seaway. Cerithium bermotiense and Lyria (Indolyria) maniyaraensis are introduced as new species.     

Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break?

The geological history of the Mediterranean Sea, its hydrography and connection with the Atlantic Ocean have been well documented. Despite a wealth of historical and oceanographic data, the Atlantic-Mediterranean transition remains controversial at the biological level as there are discordant results regarding the biogeographical separation between the Atlantic and Mediterranean biota. The opening of the Strait of Gibraltar at the end of the Messinian Salinity Crisis (some 5.33 million years ago), removed the land barrier that impeded the marine biota allowing it to disperse freely into the Mediterranean Sea. However, present day genetic patterns suggest a limitation to gene flow for some marine species, preventing population admixture. In the last few years, a large number of studies have challenged the hypothesis of the Strait of Gibraltar representing a phylogeographical break. A review of more than 70 papers reveals no obvious relationship between either dispersal ability or life history, and observed patterns of partial or complete genetic isolation between Atlantic and Mediterranean populations. We re-analysed a selection of this large body of data (20 studies in total) in order to provide a homogeneous and coherent view on the generality of the phylogeographical patterns and the presence of a phylogeographical barrier. This offered the opportunity to summarize the state of the art on this matter and reach some general conclusions on the evolutionary history across the Atlantic-Mediterranean range. Geographically, some species in the transition zone showed step changes of allele frequencies associated with the Almeria-Oran Front rather than with the Strait of Gibraltar itself. A major part of the data describe evolutionary events well within the time frame of the Quaternary age as very few taxa pre-date closure of the Tethys Sea. Results point to a combined signature of vicariance, palaeoclimate fluctuation and life-history traits on the Atlantic-Mediterranean phylogeographical patterns. Principal component analysis failed to show any particular association between biological traits and genetic variables. It would argue that organismal determinism may play a far less significant role than marine biogeographers have generally believed.     

POPULATION STRUCTURE AND SPECIATION IN TROPICAL SEAS: GLOBAL PHYLOGEOGRAPHY OF THE SEA URCHIN DIADEMA

Abstract.— The causes of speciation in the sea are rarely obvious, because geographical barriers are not conspicuous and dispersal abilities or marine organisms, particularly those of species with planktonic larvae, are hard to determine. The phylogenetic relations of species in cosmopolitan genera can provide information on the likely mode of their formation. We reconstructed the phylogeny of the pantropical and subtropical sea urchin genus Diadema, using sequences of mitochondrial DNA from 482 individuals collected around the world, to determine the efficacy of barriers to gene flow and to ascertain the history of possible dispersal and vicariance events that led to speciation. We also compared 22 isozyme loci between all described species except D. palmeri. The mitochondrial DNA data show that the two deepest lineages are found in the Indian and West Pacific Oceans. (Indo‐Pacific) Diadema setosum diverged first from all other extant Diadema, probably during the initiation of wide fluctuations in global sea levels in the Miocene. The D. setosum clade then split 3‐5 million years ago into two clades, one found around the Arabian Peninsula and the other in the Indo‐West Pacific. On the lineage leading to the other species of Diadema, the deepest branch is composed of D. palmeri, apparently separated when the climate of New Zealand became colder and other tropical echinoids at these islands went extinct. The next lineage to separate is composed of a currently unrecognized species of Diadema that is found at Japan and the Marshall Islands. Diadema mexicanum in the eastern Pacific separated next, whereas D. paucispinum, D. savignyi, and D. antillarum from the western and central Atlantic, and (as a separate clade) D. antillarum from the eastern Atlantic form a shallow polytomy. Apparently, Indo‐Pacific populations of Diadema maintained genetic contact with Atlantic ones around the southern tip of Africa for some time after the Isthmus of Panama was complete. Diadema paucispinum contains two lineages: D. paucispinum sensu stricto is not limited to Hawaii as previously thought, but extends to Easter Island, Pitcairn, and Okinawa; A second mitochondrial clade of D. paucispinum extends from East Africa and Arabia to the Philippines and New Guinea. A more recent separation between West Indian Ocean and West Pacific populations was detected in D. setosum. Presumably, these genetic discontinuities are the result of water flow restrictions in the straits between northern Australia and Southeast Asia during Pleistocene episodes of low sea level. Diadema savignyi is characterized by high rates of gene flow from Kiribati in the central Pacific all the way to the East African Coast. In the Atlantic, there is a biogeographic barrier between the Caribbean and Brazil, possibly caused by fresh water outflow from the Amazon and the Orinoco Rivers. Diadema antillarum populations of the central Atlantic islands of Ascension and St. Helena are genetically isolated and phylogenetically derived from Brazil. Except for its genetic separation by the mid‐Atlantic barrier, Diadema seems to have maintained connections through potential barriers to dispersal (including the Isthmus of Panama) more recently than did Eucidaris or Echinometra, two other genera of sea urchins in which phylogeography has been studied. Nevertheless, the mtDNA phylogeography of Diadema includes all stages expected from models of allopatric differentiation. There are anciently separated clades that now overlap in their geographic distribution, clades isolated in the periphery of the genus range that have remained in the periphery, clades that may have been isolated in the periphery but have since spread towards the center, closely related clades on either side of an existing barrier, and closely related monophyletic entities on either side of an historical barrier that have crossed the former barrier line, but have not attained genetic equilibrium. Except for D. paucispinum and D. savignyi, in which known hybridization may have lodged mtDNA from one species into the genome of the other, closely related clades are always allopatric, and only distantly related ones overlap geographically. Thus, the phylogenetic history and distribution of extant species of Diadema is by and large consistent with allopatric speciation.     

Phylogeography of the humbug damselfish,Dascyllus aruanus (Linnaeus, 1758): evidence of Indo‐Pacific vicariance and genetic differentiation of peripheral populations

The phylogeographical structure of coral‐associated reef fishes may have been severely affected, more than species from deeper habitats, by habitat loss during periods of low sea level. The humbug damselfish, Dascyllus aruanus, is widely distributed across the Indo‐West Pacific, and exclusively inhabits branching corals. We used mitochondrial cytochrome b sequence and seven microsatellite loci on D. aruanus samples (260 individuals) from 13 locations across the Indo‐West Pacific to investigate its phylogeographical structure distribution‐wide. A major genetic partition was found between the Indian and Pacific Ocean populations, which we interpret as the result of geographical isolation on either side of the Indo‐Pacific barrier during glacial periods. The peripheral populations of the Red Sea and the Society Islands exhibited lower genetic diversity, and substantial genetic differences with the other populations, suggesting relative isolation. Thus, vicariance on either side of the Indo‐Pacific barrier and peripheral differentiation are considered to be the main drivers that have shaped the phylogeographical patterns presently observed in D. aruanus. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 931–942.     

Origins and relationships of the Pleuronectoidei: Molecular and morphological analysis of living and fossil taxa

Flatfishes (Pleuronectiformes) are a species‐rich and distinct group of fishes characterized by cranial asymmetry. Flatfishes occupy a wide diversity of habitats, including the tropical deep‐sea and freshwaters, and often are small‐bodied fishes. Most scientific effort, however, has been focused on large‐bodied temperate marine species important in fisheries. Phylogenetic study of flatfishes has also long been limited in scope and focused on the placement and monophyly of flatfishes. As a result, several questions in systematic biology have persisted that molecular phylogenetic study can answer. We examine the Pleuronectoidei, the largest suborder of Pleuronectiformes with >99% of species diversity of the order, in detail with a multilocus nuclear and mitochondrial data set of 57 pleuronectoids from 13 families covering a wide range of habitats. We combine the molecular data with a morphological matrix to construct a total evidence phylogeny that places fossil flatfishes among extant lineages. Utilizing a time‐calibrated phylogeny, we examine the timing of diversification, area of origin and ancestral temperature preference of Pleuronectoidei. We find polyphyly or paraphyly of two flatfish families, the Paralichthyidae and the Rhombosoleidae, and support the creation of two additional families—Cyclopsettidae and Oncopteridae—to resolve their non‐monophyletic status. Our findings also support the distinctiveness of Paralichthodidae and refine the placement of that lineage. Despite a core fossil record in Europe, the observed recent diversity of pleuronectoids in the Indo‐West Pacific is most likely a result of the Indo‐West Pacific being the area of origin for pleuronectoids and the ancestral temperature preference of flatfishes is most likely tropical.     

Speciation and diversity on tropical rocky shores: a global phylogeny of snails of the genus Echinolittorina

A phylogenetic approach to the origin and maintenance of species diversity ideally requires the sampling of all species within a clade, confirmation that they are evolutionarily distinct entities, and knowledge of their geographical distributions. In the marine tropics such studies have mostly been of fish and reef-associated organisms, usually with high dispersal. In contrast, snails of the genus Echinolittorina (Littorinidae) are restricted to rocky shores, have a four-week pelagic development (and recorded dispersal up to 1400 km), and show different evolutionary patterns. We present a complete molecular phylogeny of Echinolittorina, derived from Bayesian analysis of sequences from nuclear 28S rRNA and mitochondrial 12S rRNA and COI genes (nodal support indicated by posterior probabilities, maximum likelihood, and neighbor-joining bootstrap). This consists of 59 evolutionarily significant units (ESUs), including all 50 known taxonomic species. The 26 ESUs found in the Indo-West Pacific region form a single clade, whereas the eastern Pacific and Atlantic species are basal. The earliest fossil occurred in the Tethys during the middle Eocene and we suggest that the Indo-West Pacific clade has been isolated since closure of the Tethyan seaway in the early Miocene. The geographical distributions of all species (based on more than 3700 locality records) appear to be circumscribed by barriers of low temperature, unsuitable sedimentary habitat, stretches of open water exceeding about 1400 km, and differences in oceanographic conditions on the continuum between oceanic and continental. The geographical ranges of sister species show little or no overlap, indicating that the speciation mode is predominantly allopatric. Furthermore, range expansion following speciation appears to have been limited, because a high degree of allopatry is maintained through three to five branching points of the phylogeny. This may be explained by infrequent long-distance colonization, habitat specialization on the oceanic/continental gradient, and perhaps by interspecific competition. In the eastern Pacific plus Atlantic we identify five cases of divergence on either side of the Isthmus of Panama, but our estimates of their ages pre-date the emergence of the Isthmus. There are three examples of sister relationships between species in the western Atlantic and eastern Atlantic, all resulting from dispersal to the east. Within the Indo-West Pacific, we find no geographical pattern of speciation events; narrowly endemic species of recent origin are present in both peripheral and central parts of the region. Evidence from estimated divergence times of sister species, and from a plot of the number of lineages over time, suggest that there has been no acceleration of diversification during the glacio-eustatic cycles of the Plio-Pleistocene. In comparison with reefal organisms, species of Echinolittorina on rocky shores may be less susceptible to extinction or isolation during sea-level fluctuations. The species richness of Echinolittorina in the classical biogeographic provinces conforms to the common pattern of highest diversity (11 species) in the central "East Indies Triangle" of the Indo-West Pacific, with a subsidiary focus in the eastern Pacific and western Atlantic, and lowest diversity in the eastern Atlantic. The diversity focus in the East Indies Triangle is produced by a mosaic of restricted allopatric species and overlap of a few widespread ones, and is the result of habitat specialization rather than historical vicariance. This study emphasizes the plurality of biogeographic histories and speciation patterns in the marine tropics.     

Phylogenetic relationships of tropical western Atlantic snappers in subfamily Lutjaninae (Lutjanidae: Perciformes) inferred from mitochondrial DNA sequences

Phylogenetic relationships among 20 nominal species of tropical lutjanine snappers (Lutjanidae) (12 from the western Atlantic, one from the eastern Pacific, and seven from the Indo‐Pacific) were inferred based on 2206 bp (712 variable, 614 parsimony informative) from three protein‐coding mitochondrial genes. Also included in the analysis were DNA sequences from two individuals, identified initially as Lutjanus apodus, which were sampled off the coast of Bahia State in Brazil (western Atlantic), and from three individuals labelled as ‘red snapper’ in the fish market in Puerto Armuelles, Panama (eastern Pacific). Bayesian posterior probabilities and maximum‐likelihood bootstrap percentages strongly supported monophyly of all lutjanines sampled and the hypothesis that western Atlantic lutjanines are derived from an Indo‐Pacific lutjanine lineage. The phylogenetic hypothesis also indicated that oceans where lutjanines are distributed (western Atlantic, eastern Pacific, and Indo‐Pacific) are not reciprocally monophyletic for the species distributed within them. There were three strongly supported clades that included all western Atlantic lutjanines: one included six species of Lutjanus from the western Atlantic, two species of Lutjanus from the eastern Pacific, and the monotypic genera Rhomboplites and Ocyurus (western Atlantic); one that included three, probably four, species of Lutjanus in the western Atlantic; and one that included Lutjanus cyanopterus (western Atlantic), an unknown species of Lutjanus from the eastern Pacific, and three species of Lutjanus from the Indo‐Pacific. Molecular‐clock calibrations supported an early Miocene diversification of an Indo‐Pacific lutjanine lineage that dispersed into the western Atlantic via the Panamanian Gateway. Divergent evolution among these lutjanines appears to have occurred both by vicariant and ecological speciation: the former following significant geographic or geological events, including both shoaling and closure of the Panamanian Gateway and tectonic upheavals, whereas the latter occurred via phenotypic diversification inferred to indicate adaptation to life in different habitats. Taxonomic revision of western Atlantic lutjanines appears warranted in that monotypic Ocyurus and Rhomboplites should be subsumed within the genus Lutjanus. Finally, it appears that retail mislabelling of ‘red snapper’ in commercial markets extends beyond the USA. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 915–929.     

Vicariance across major marine biogeographic barriers: temporal concordance and the relative intensity of hard versus soft barriers

The marine tropics contain five major biogeographic regions (East Pacific, Atlantic, Indian Ocean, Indo-Australian Archipelago (IAA) and Central Pacific). These regions are separated by both hard and soft barriers. Reconstructing ancestral vicariance, we evaluate the extent of temporal concordance in vicariance events across three major barriers (Terminal Tethyan Event (TTE), Isthmus of Panama (IOP), East Pacific Barrier, EPB) and two incomplete barriers (either side of the IAA) for the Labridae, Pomacentridae and Chaetodontidae. We found a marked lack of temporal congruence within and among the three fish families in vicariance events associated with the EPB, TTE and IOP. Vicariance across hard barriers separating the Atlantic and Indo-Pacific (TTE, IOP) is temporally diffuse, with many vicariance events preceding barrier formation. In marked contrast, soft barriers either side of the IAA hotspot support tightly concordant vicariance events (2.5 Myr on Indian Ocean side; 6 Myr on Central Pacific side). Temporal concordance in vicariance points to large-scale temporally restricted gene flow during the Late Miocene and Pliocene. Despite different and often complex histories, both hard and soft barriers have comparably strong effects on the evolution of coral reef taxa.     

Deep-sea squat lobster biogeography (Munidopsidae: Leiogalathea) unveils Tethyan vicariance and evolutionary patterns shared by shallow-water relatives

The ecology, abundance and diversity of galatheoid squat lobsters make them an ideal group to study deep-sea diversification processes. Here, we reconstructed the evolutionary and biogeographic history of Leiogalathea, a genus of circum-tropical deep-sea squat lobsters, in order to compare patterns and processes that have affected shallow-water and deep-sea squat lobster species. We first built a multilocus phylogeny and a calibrated species tree with a relaxed clock using StarBEAST2 to reconstruct evolutionary relationships and divergence times among Leiogalathea species. We used BioGeoBEARS and a DEC model, implemented in RevBayes, to reconstruct ancestral distribution ranges and the biogeographic history of the genus. Our results showed that Leiogalathea is monophyletic and comprises four main lineages; morphological homogeneity is common within and between clades, except in one; the reconstructed ancestral range of the genus is in the Atlantic and Indian oceans (Tethys). They also revealed the divergence of the Atlantic species around 25 million years ago (Ma), intense cladogenesis 15–25 Ma and low levels of speciation over the last 5 million years (Myr). The four Leiogalathea lineages showed similar patterns of speciation: allopatric speciation followed by range expansion and subsequent stasis. Leiogalathea started diversifying during the Oligocene, likely in the Tethyan. The Atlantic lineage then split from its Indo-Pacific sister group due to vicariance driven by closure of the Tethys Seaway. The Atlantic lineage is less speciose compared with the Indo-Pacific lineages, with the Tropical Southwestern Pacific being the current centre of diversity. Leiogalathea diversification coincided with cladogenetic peaks in shallow-water genera, indicating that historical biogeographic events similarly shaped the diversification and distribution of both deep-sea and shallow-water squat lobsters.