Diversification in the tropical pacific: comparisons between marine and terrestrial systems and the importance of founder speciation

Patterns of distribution and processes of differentiation haveoften been contrasted between terrestrial and marine biotas.The islands of Oceania offer an excellent setting to explorethis contrast, because the geographic setting for terrestrialand shallow-water, benthic, marine organisms are the same: themyriad islands strewn across the vast Pacific. The size of speciesranges and the geographic distribution of endemism are two biogeographicattributes that are thought to differ markedly between terrestrialand marine biotas in the Pacific. While terrestrial speciesare frequently confined to single islands or archipelagoes throughoutOceania, marine species tend to have wide to very wide distributions,and are rarely restricted to single island groups except forthe most isolated archipelagoes. We explore the conditions underwhich species can reach an island by dispersal and differentiate.Genetic differentiation can occur either through founder speciationor vicariance; these processes are requisite ends of a continuum.We show that founder speciation is most likely when few propagulesenter the dispersal medium and survive well while they travelfar. We argue that conditions favorable to founder speciationare common in marine as well as terrestrial systems, and thatterrestrial-type, archipelagic-level endemism is likely commonin marine taxa. We give examples of marine groups that showarchipelagic level endemism on most Pacific island groups aswell as of terrestrial species that are widespread. Thus boththe patterns and processes of insular diversification are variable,and overlap more between land and sea than previously considered.     

Hawaiian biogeography and the islands' freshwater fish fauna

Aim This paper describes known patterns in the distributions and relationships of Hawaiian freshwater fishes, and compares these patterns with those exhibited by Hawaii's terrestrial biota. Location The study is based in Hawaii, and seeks patterns across the tropical and subtropical Indo‐west Pacific. Methods The study is based primarily on literature analysis. Results The Hawaiian freshwater fish fauna comprises five species of goby in five different genera (Gobiidae). Four species are Hawaiian endemics, the fifth shared with islands in the western tropical Pacific Ocean. All genera are represented widely across the Indo‐west Pacific. All five species are present on all of the major Hawaiian islands. All five species are amphidromous – their larval and early juvenile life being spent in the sea. Although there has been some local phyletic evolution to produce Hawaiian endemics, there has been no local radiation to produce single‐island endemics across the archipelago. Nor is there evidence for genetic structuring among populations in the various islands. Main conclusions In this regard, the freshwater fish fauna of Hawaii differs from the well‐known patterns of local evolution and radiation in Hawaiian Island terrestrial taxa. Amphidromy probably explains the biogeographical idiosyncrasies of the fish fauna – dispersal through the sea initially brought the fish species to Hawaii, and gene flow among populations, across the archipelago, has hitherto inhibited the evolution of local island endemics, apparently even retarding genetic structuring on individual islands.     

Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago

Speciation remains a central enigma in biology, and nowhere is this more apparent than in shallow tropical seas where biodiversity rivals that of tropical rainforests. Obvious barriers to gene flow are few and most marine species have a highly dispersive larval stage, which should greatly decrease opportunities for speciation via geographic isolation. The disparity in the level of geographic isolation for terrestrial and marine species is exemplified in Hawai'i where opportunities for allopatric speciation abound in the terrestrial realm. In contrast, marine colonizers of Hawai'i are believed to produce only a single endemic species or population, due to the lack of isolating barriers. To test the assertion that marine species do not diversify within Hawai'i, we examine the evolutionary origin of three endemic limpets (Cellana exarata, C. sandwicensis and C. talcosa) that are vertically segregated across a steep ecocline on rocky shores. Analyses of three mtDNA loci (12S, 16S, COI; 1565bp) and two nDNA loci (ATPSβ, H3; 709bp) in 26 Indo-Pacific Cellana species (N=414) indicates that Hawai'i was colonized once ～3.4-7.2Ma from the vicinity of Japan. Trait mapping demonstrates that high-shore residence is the ancestral character state, such that mid- and low-shore species are the product of subsequent diversification. The Hawaiian Cellana are the first broadcast-spawners demonstrated to have speciated within any archipelago. The habitat stratification, extensive sympatry, and evolutionary history of these limpets collectively indicate a strong ecological component to speciation and support the growing body of evidence for non-allopatric speciation in the ocean.     

Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods

The perceived wide geographic range of organisms in the sea, facilitated by ready dispersal of waterborne dispersal stages, is a challenge for hypotheses of marine speciation but a boon to efforts of marine conservation. Wide species ranges are especially striking in the reef-rich Indo-west Pacific, the largest and most diverse marine biogeographic region, extending across half the planet. The insular marine biota of the tropical Pacific is characterized by wide-ranging species and provides the most striking examples of long distance dispersal, with endemism largely confined to the most remote island groups. Here we show that the gastropod Astralium "rhodostomum" has developed endemic clades on almost every Pacific archipelago sampled, a pattern unprecedented in marine biogeography, and reminiscent of the terrestrial biota of oceanic islands. Mitochondrial DNA sequences indicate that this species-complex is comprised of at least 30 geographically isolated clades, separated by as little as 180 km. Evidence suggests that such fine scale endemism and high diversity is not exceptional, but likely characterizes a substantial fraction of the reef biota. These results imply that (1) marine speciation can regularly occur over much finer spatial scales than generally accepted, (2) the diversity of coral reefs is even higher than suggested by morphology-based estimates, and (3) conservation efforts need to focus at the archipelagic level in the sea as on land.     

THE DISPERSAL BARRIER IN THE TROPICAL PACIFIC: IMPLICATIONS FOR MOLLUSCAN SPECIATION AND EXTINCTION

Stretches of deep ocean constitute barriers to the dispersal of many shallow-water marine species in the tropical Pacific. The purpose of this study was to assess the selectivity of these barriers with respect to the habitat characteristics, adult size, and predation-related shell architecture of gastropods, and to explore the implications of this selectivity for macroevolutionary patterns of extinction and speciation. The dispersal barrier between continental islands (represented in my collections by species from eastern Indonesia, the southern Philippines, and the north coast of New Guinea) and the nearby oceanic Palau Islands was studied by evaluating the percentage of each architectural and habitat category that is present on the continental islands but missing in Palau. The barrier is significantly more effective against sand-dwelling species than against rock-dwellers, and among rock-dwellers it is most effective against aperturally unarmored taxa. Barriers between Palau and Guam, Guam and the Hawaiian Islands, and the Line Islands and the tropical Eastern Pacific are generally unselective with respect to substratum type and architecture. The fact that narrow-apertured species are less affected by the barrier between the continental islands and Palau than are other rock-dwelling gastropods is consistent with the interpretation that this group has been unusually resistant to extinction and highly susceptible to founder speciation when oceanic circulation is altered. These patterns of susceptibility and geographical distribution may explain why armored gastropods have increased in numbers relative to unarmored ones in the tropical Pacific during the Cenozoic.     

Towards a panbiogeography of the seas

A contrast is drawn between the concept of speciation favoured in the Darwin–Wallace biogeographic paradigm (founder dispersal from a centre of origin) and in panbiogeography (vicariance or allopatry). Ordinary ecological dispersal is distinguished from founder dispersal. A survey of recent literature indicates that ideas on many aspects of marine biology are converging on a panbiogeographic view. Panbiogeographic conclusions supported in recent work include the following observations: fossils give minimum ages for groups and most taxa are considerably older than their earliest known fossil; Pacific/Atlantic divergence calibrations based on the rise of the Isthmus of Panama at 3 Ma are flawed; for these two reasons most molecular clock calibrations for marine groups are also flawed; the means of dispersal of taxa do not correlate with their actual distributions; populations of marine species may be closed systems because of self‐recruitment; most marine taxa show at least some degree of vicariant differentiation and vicariance is surprisingly common among what were previously assumed to be uniform, widespread taxa; mangrove and seagrass biogeography and migration patterns in marine taxa are best explained by vicariance; the Indian Ocean and the Pacific Ocean represent major biogeographic regions and diversity in the Indo‐Australian Archipelago is related to Indian Ocean/Pacific Ocean vicariance; distribution in the Pacific is not the result of founder dispersal; distribution in the south‐west Pacific is accounted for by accretion tectonics which bring about distribution by accumulation and juxtaposition of communities; tectonic uplift and subsidence can directly affect vertical distribution of marine communities; substantial parallels exist between the biogeography of terrestrial and marine taxa; biogeographically and geologically composite areas are tractable using panbiogeographic analysis; metapopulation models are more realistic than the mainland/island dispersal models used in the equilibrium theory of island biogeography; and regional biogeography is a major determinant of local community composition. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 675–723.     

A tale of three seas: consistency of natural history traits in a Caribbean–Atlantic barnacle introduced to Hawaii

Predictive models in invasion biology rely on knowledge of the life history and ecological role of invading species. However, species may change in key traits as they invade a new region, making prediction difficult. For marine invertebrate invaders there have been too few comparative studies to determine whether change in key traits is the exception or the rule. Here we examined populations of the intertidal barnacle Chthamalus proteus in three locations in its native range in the Caribbean and Atlantic, and in the Hawaiian Islands, where it has recently invaded, as a model system for such comparative studies. We measured body size, fecundity, population density and vertical distribution, compared habitat use and investigated aspects of the barnacle’s ecological role in Curaçao, Panama and Brazil and the main Hawaiian Islands. In terms of these measures, the barnacle has undergone little change in its invasion of Hawaii. Thus, if this barnacle had been studied in its native range, predictions about its spread in Hawaii could have been made. As little was known about this barnacle in either its native range or Hawaii, we also carried out studies of its larval life history, fecundity, growth, and mortality. Based on this work, we predict that this barnacle will continue to spread, aided by vessel traffic, throughout the Hawaiian Islands and elsewhere in the Pacific.     

Genomic signatures of geographic isolation and natural selection in coral reef fishes

The drivers of speciation remain among the most controversial topics in evolutionary biology. Initially, Darwin emphasized natural selection as a primary mechanism of speciation, but the architects of the modern synthesis largely abandoned that view in favour of divergence by geographic isolation. The balance between selection and isolation is still at the forefront of the evolutionary debate, especially for the world's tropical oceans where biodiversity is high, but isolating barriers are few. Here, we identify the drivers of speciation in Pacific reef fishes of the genus Acanthurus by comparative genome scans of two peripheral populations that split from a large Central‐West Pacific lineage at roughly the same time. Mitochondrial sequences indicate that populations in the Hawaiian Archipelago and the Marquesas Islands became isolated approximately 0.5 Ma. The Hawaiian lineage is morphologically indistinguishable from the widespread Pacific form, but the Marquesan form is recognized as a distinct species that occupies an unusual tropical ecosystem characterized by upwelling, turbidity, temperature fluctuations, algal blooms and little coral cover. An analysis of 3737 SNPs reveals a strong signal of selection at the Marquesas, with 59 loci under disruptive selection including an opsin Rh2 locus. While both the Hawaiian and Marquesan populations indicate signals of drift, the former shows a weak signal of selection that is comparable with populations in the Central‐West Pacific. This contrast between closely related lineages reveals one population diverging due primarily to geographic isolation and genetic drift, and the other achieving taxonomic species status under the influence of selection.     

PERIPATRIC SPECIATION DRIVES DIVERSIFICATION AND DISTRIBUTIONAL PATTERN OF REEF HERMIT CRABS (DECAPODA: DIOGENIDAE: CALCINUS)

The diversity on coral reefs has long captivated observers. We examine the mechanisms of speciation, role of ecology in speciation, and patterns of species distribution in a typical reef‐associated clade—the diverse and colorful Calcinus hermit crabs—to address the origin of tropical marine diversity. We sequenced COI, 16S, and H3 gene regions for ～90% of 56 putative species, including nine undescribed, “cryptic” taxa, and mapped their distributions. Speciation in Calcinus is largely peripatric at remote locations. Allopatric species pairs are younger than sympatric ones, and molecular clock analyses suggest that >2 million years are needed for secondary sympatry. Substantial niche conservatism is evident within clades, as well as a few major ecological shifts between sister species. Color patterns follow species boundaries and evolve rapidly, suggesting a role in species recognition. Most species prefer and several are restricted to oceanic areas, suggesting great dispersal abilities and giving rise to an ocean‐centric diversity pattern. Calcinus diversity patterns are atypical in that the diversity peaks in the west‐central oceanic Pacific rather than in the Indo‐Malayan “diversity center.” Calcinus speciation patterns do not match well‐worn models put forth to explain the origin of Indo‐West Pacific diversity, but underscore the complexity of marine diversification.     

Habitat utilization by Hawaiian stream fishes with reference to community structure in oceanic island streams

Synopsis Much of the freshwater biota on high Pacific islands is derived from marine ancestors. Traces of this marine origin are seen in the amphidromous life history patterns of these species. Investigation of the habitat utilization of an assemblage of freshwater gobies in the Hawaiian Islands indicates some resource partitioning within this group. The three major stream species appear to exhibit distinct habitat preferences, which in conjunction with their longitudinal zonation in streams may have served to facilitate their colonization or co-existence.     

Yeasts of the Miami,Florida, Area

The isolation and examination of yeasts from sea water, marine animals and decaying material has demonstrated different patterns of distribution and speciation among these substrates. Yeast species were found with low frequency in intestinal tracts of marine animals, occurring with greater abundance in other environs. Interchange of species between terrestrial and inshore marine locales is apparent.     

Speciation along a depth gradient in a marine adaptive radiation

Oceans are home to much of the world''s biodiversity, but we know little about the processes driving speciation in marine ecosystems with few geographical barriers to gene flow. Ecological speciation resulting from divergent natural selection between ecological niches can occur in the face of gene flow. Sister species in the young and ecologically diverse rockfish genus Sebastes coexist in the northeast Pacific, implying that speciation may not require geographical isolation. Here, I use a novel phylogenetic comparative analysis to show that rockfish speciation is instead associated with divergence in habitat depth and depth-associated morphology, consistent with models of parapatric speciation. Using the same analysis, I find no support for alternative hypotheses that speciation involves divergence in diet or life history, or that speciation involves geographic isolation by latitude. These findings support the hypothesis that rockfishes undergo ecological speciation on an environmental gradient.     

Molecular evidence of new variant Brucella in North Pacific common minke whales

Brucella, a causative agent of brucellosis, has been isolated recently from a variety of marine mammals. The molecular analysis of marine mammalian Brucella strains, without manifest pathology of brucellosis in the eastern North Atlantic, showed that they are distinct from terrestrial Brucella species. Previously, we reported abnormal gonads in common minke whales (Balaenoptera acutorostrata) in the western North Pacific and suggested the presence of Brucella infection in the whales in pathology and serology studies. In the present study, using polymerase chain reaction (PCR), Brucella was detected in granular testes of the whales showing caseation or calcification. The insertion of an IS711 transposable element specific for marine mammal isolates as well as a seal isolate-specific DNA fragment were also found. Molecular characterization of Brucella based on sequence analysis of the PCR products amplified from the outer membrane protein (omp) 2 gene showed that the Brucella from North Pacific common minke whales was different from terrestrial and North Atlantic marine mammal Brucella strains. The North Pacific Brucella showed the highest similarity to North Atlantic seal strains among the known Brucella strains.     

Phylogenetic relationships within laticaudine sea snakes (Elapidae)

The sea snake subfamily Laticaudinae consists of a single genus with eight named species, based on morphological characters. We used microsatellite and mitochondrial DNA (mtDNA) data to clarify the adaptive radiation of these oviparous sea snakes in the South Pacific, with special reference to New Caledonia and Vanuatu. A mitochondrial DNA data set (ND4 gene 793 bp) was obtained from 345 individuals of the five species of Laticauda sp. sea snakes endemic to the region. Maximum likelihood and Bayesian approaches yielded the same optimal tree topology, identifying two major clades (yellow-banded and blue-banded sea snakes). Although all laticaudine sea snakes rely on small islands as oviposition sites, the two lineages differ in their use of marine vs. terrestrial habitats. A highly aquatic species (Laticauda laticaudata) shows a strong pattern of genetic isolation by distance, implying that the patchy distribution of terrestrial habitats has had little impact on gene flow. The more terrestrial clade (Laticauda colubrina, Laticauda frontalis, Laticauda guineai, Laticauda saintgironsi) shows stronger geographic differentiation in allelic frequencies, associated with island groups rather than with geographic distance. Microsatellites and mtDNA suggest that L. frontalis (restricted to Vanuatu) represents a recent founder-induced speciation event, from allopatric migrants of the New Caledonian taxon L. saintgironsi. A major divergence in speciation patterns between the two major clades of laticaudine snakes thus correlates with (and perhaps, is driven by) differences in the importance of terrestrial habitats in the species' ecology.     

Population structure and phylogeography reveal pathways of colonization by a migratory marine reptile (Chelonia mydas) in the central and eastern Pacific

Climate, behavior, ecology, and oceanography shape patterns of biodiversity in marine faunas in the absence of obvious geographic barriers. Marine turtles are an example of highly migratory creatures with deep evolutionary lineages and complex life histories that span both terrestrial and marine environments. Previous studies have focused on the deep isolation of evolutionary lineages (>3 mya) through vicariance; however, little attention has been given to the pathways of colonization of the eastern Pacific and the processes that have shaped diversity within the most recent evolutionary time. We sequenced 770 bp of the mtDNA control region to examine the stock structure and phylogeography of 545 green turtles from eight different rookeries in the central and eastern Pacific. We found significant differentiation between the geographically separated nesting populations and identified five distinct stocks (F_ST = 0.08–0.44, P < 0.005). Central and eastern Pacific Chelonia mydas form a monophyletic group containing 3 subclades, with Hawaii more closely related to the eastern Pacific than western Pacific populations. The split between sampled central/eastern and western Pacific haplotypes was estimated at around 0.34 mya, suggesting that the Pacific region west of Hawaii has been a more formidable barrier to gene flow in C. mydas than the East Pacific Barrier. Our results suggest that the eastern Pacific was colonized from the western Pacific via the Central North Pacific and that the Revillagigedos Islands provided a stepping‐stone for radiation of green turtles from the Hawaiian Archipelago to the eastern Pacific. Our results fit with a broader paradigm that has been described for marine biodiversity, where oceanic islands, such as Hawaii and Revillagigedo, rather than being peripheral evolutionary “graveyards”, serve as sources and recipients of diversity and provide a mechanism for further radiation.     

Inferring the mode of speciation in Indo-West Pacific Conus (Gastropoda: Conidae)

Aim This study aims to initially explore the mode of speciation in Indo‐West Pacific Conus. Location The Indo‐West Pacific island arc, Indian and Pacific Oceans. Methods Relating evolutionary divergence in a molecular phylogeny [T.F. Duda & S.R. Palumbi (1999) Proceedings of the National Academy of Science USA, 96 , 10272] using node height with modern range extents as a possible measure of allopatric or sympatric speciation following that of T.G. Barraclough, A.P. Vogler & P.H. Harvey [(1999) Evolution of Biological Diversity. Oxford University Press, Oxford] models of sympatric and allopatric speciation. Results The analysis seems to indicate that the relationship of sympatry with node height is not informative. Species that have diverged quite recently show 100% sympatry with the sister species. A clearer signal of recent allopatric speciation is observed in species whose distribution is at the edge of the Indian and Pacific Ocean basins. In the widely distributed Conus ebraeus clade, the relationships of node heights and range extents of the member species support a key prediction of sympatric speciation. In highly ecologically specialized species, there is a smaller degree of sympatry than those species that are less specialized. Main conclusions The modes of speciation models presented in this study are not informative. This suggests that there had been large and possibly rapid changes in range size after speciation in the various clades. This could have been due to the fact that the wide dispersal life‐history strategy in the genus had been largely conserved in Conus evolution. There is evidence of sympatric and parapatric speciation in one Conus clade. Overall, the patterns of phylogeny and range distribution when related to the timing of speciation lend circumstantial support to a Neogene centre of origin hypothesis but not to speciation on the Pacific Plate. Speciation is likely to have been associated with the Tethys Sea closure event, with rapid speciation occurring after closure.     

Tracing ancestry with chromosomal sequences

Most of the large Drosophila species of Hawaii are single-island endemics. Chromosomal sequences show that species at the new end of the archipelago have been derived stepwise from ancestral populations on older islands. The oldest high island has an endemic species with sequences that match some in the Nearctic-Palearctic robusta species group. Colonization from a continent by long-distance dispersal seems a likely origin for the Hawaiian drosophilids. Telmatogeton, a worldwide genus of marine midges, has five Hawaiian species inhabiting freshwater streams. Chromosomal sequences of a marine species in Hawaiian waters match the freshwater forms, indicating colonization from the ocean.     

Biogeography and taxonomy of extinct and endangered monk seals illuminated by ancient DNA and skull morphology

Extinctions and declines of large marine vertebrates have major ecological impacts and are of critical concern in marine environments. The Caribbean monk seal, Monachus tropicalis, last definitively reported in 1952, was one of the few marine mammal species to become extinct in historical times. Despite its importance for understanding the evolutionary biogeography of southern phocids, the relationships of M. tropicalis to the two living species of critically endangered monk seals have not been resolved. In this study we present the first molecular data for M. tropicalis, derived from museum skins. Phylogenetic analysis of cytochrome b sequences indicates that M. tropicalis was more closely related to the Hawaiian rather than the Mediterranean monk seal. Divergence time estimation implicates the formation of the Panamanian Isthmus in the speciation of Caribbean and Hawaiian monk seals. Molecular, morphological and temporal divergence between the Mediterranean and “New World monk seals” (Hawaiian and Caribbean) is profound, equivalent to or greater than between sister genera of phocids. As a result, we classify the Caribbean and Hawaiian monk seals together in a newly erected genus, Neomonachus. The two genera of extant monk seals (Monachus and Neomonachus) represent old evolutionary lineages each represented by a single critically endangered species, both warranting continuing and concerted conservation attention and investment if they are to avoid the fate of their Caribbean relative.     

Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus

Background  

The study of speciation in the marine realm is challenging because of the apparent absence of physical barriers to dispersal, which are one of the main drivers of genetic diversity. Although phylogeographic studies using mitochondrial DNA (mtDNA) information often reveal significant genetic heterogeneity within marine species, the evolutionary significance of such diversity is difficult to interpret with these markers. In the northwestern (NW) Pacific, several studies have emphasised the potential importance of sea-level regression during the most recent glaciations as a driver of genetic diversity in marine species. These studies have failed, however, to determine whether the period of isolation was long enough for divergence to attain speciation. Among these marine species, the cosmopolitan estuarine-dependent fish Mugil cephalus represents an interesting case study. Several divergent allopatric mtDNA lineages have been described in this species worldwide, and three occur in sympatry in the NW Pacific.     

Pushing the limits in marine species distribution modelling: lessons from the land present challenges and opportunities

Aim Species distribution models (SDMs) have been used to address a wide range of theoretical and applied questions in the terrestrial realm, but marine‐based applications remain relatively scarce. In this review, we consider how conceptual and practical issues associated with terrestrial SDMs apply to a range of marine organisms and highlight the challenges relevant to improving marine SDMs. Location We include studies from both marine and terrestrial systems that encompass many geographic locations around the globe. Methods We first performed a literature search and analysis of marine and terrestrial SDMs in ISI Web of Science to assess trends and applications. Using knowledge from terrestrial applications, we critically evaluate the application of SDMs in marine systems in the context of ecological factors (dispersal, species interactions, aggregation and ontogenetic shifts) and practical considerations (data quality, alternative modelling approaches and model validation) that facilitate or create difficulties for model application. Results The relative importance of ecological factors to be considered when applying SDMs varies among terrestrial and marine organisms. Correctly incorporating dispersal is frequently considered an important issue for terrestrial models, but because there is greater potential for dispersal in the ocean, it is often less of a concern in marine SDMs. By contrast, ontogenetic shifts and feeding have received little attention in terrestrial SDM applications, but these factors are important to many marine SDMs. Opportunities also exist for applying more advanced SDM approaches in the marine realm, including mechanistic ecophysiological models, where water balance and heat transfer equations are simpler for some marine organisms relative to their terrestrial counterparts. Main conclusions SDMs have generally been under‐utilized in the marine realm relative to terrestrial applications. Correlative SDM methods should be tested on a range of marine organisms, and we suggest further development of methods that address ontogenetic shifts and feeding interactions. We anticipate developments in, and cross‐fertilization between, coupled correlative and process‐based SDMs, mechanistic eco‐physiological SDMs, and spatial population dynamic models for climate change and species invasion applications in particular. Comparisons of the outputs of different model types will provide insight that is useful for improved spatial management of marine species.