Luiz A. Rocha

PHYLOGEOGRAPHY OF THE TRUMPETFISHES ( AULOSTOMUS ): RING SPECIES COMPLEX ON A GLOBAL SCALE

Abstract The distribution of circumtropical marine species is limited by continental boundaries, cold temperate conditions, and oceanic expanses, but some of these barriers are permeable over evolutionary time scales. Sister taxa that evolved in separate ocean basins can come back into contact, and the consequences of this renewed sympatry may be a key to understanding evolutionary processes in marine organisms. The circumtropical trumpetfishes (Aulostomus) include a West Atlantic species (A. maculatus), an Indian-Pacific species (A. chinensis), and an East Atlantic species (A. strigosus) that may be the product of a recent invasion from the Indian Ocean. To resolve patterns of divergence and speciation, we surveyed 480 bp of mitochondrial DNA cytochrome b in 196 individuals from 16 locations. Based on a conventional molecular clock of 2% sequence divergence per million years, the deepest partitions in a neighbor-joining tree (d = 0.063–0.082) are consistent with separation of West Atlantic and Indian-Pacific species by the Isthmus of Panama, 3–4 million years ago. By the same criteria, trumpetfish in the East Atlantic were isolated from the Indian Ocean about 2.5 million years ago (d = 0.044–0.054), coincident with the advent of glacial cycles and cold-water upwelling around South Africa. Continental barriers between tropical oceans have only rarely been surmounted by trumpetfishes, but oceanic barriers do not appear to be substantial, as indicated by weak population partitioning (ϕST = 0.093) in A. chinensis across the Indian and Pacific Oceans. Finally, morphological and mitochondrial DNA data indicate hybridization of A. strigosus and A. maculatus in Brazil. After 3–4 million years and a globe-spanning series of vicariant and dispersal events, trumpetfish lineages have come back into contact in the southwest Atlantic and appear to be merging. This ring species phenomenon may occur in a broad array of marine organisms, with clear implications for the production and maintenance of biodiversity in marine ecosystems. Corresponding Editor: L. Bernatchez

Ecological speciation in tropical reef fishes.

The high biodiversity in tropical seas provides a long-standing challenge to allopatric speciation models. Physical barriers are few in the ocean and larval dispersal is often extensive, a combination that should reduce opportunities for speciation. Yet coral reefs are among the most species-rich habitats in the world, indicating evolutionary processes beyond conventional allopatry. In a survey of mtDNA sequences of five congeneric west Atlantic reef fishes (wrasses, genus Halichoeres) with similar dispersal potential, we observed phylogeographical patterns that contradict expectations of geographical isolation, and instead indicate a role for ecological speciation. In Halichoeres bivittatus and the species pair Halichoeres radiatus/brasiliensis, we observed strong partitions (3.4% and 2.3% divergence, respectively) between adjacent and ecologically distinct habitats, but high genetic connectivity between similar habitats separated by thousands of kilometres. This habitat partitioning is maintained even at a local scale where H. bivittatus lineages are segregated between cold- and warm-water habitats in both Bermuda and Florida. The concordance of evolutionary partitions with habitat types, rather than conventional biogeographical barriers, indicates parapatric ecological speciation, in which adaptation to alternative environmental conditions in adjacent locations overwhelms the homogenizing effect of dispersal. This mechanism can explain the long-standing enigma of high biodiversity in coral reef faunas.

Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae).

Although many reef fishes of the tropical Atlantic are widely distributed, there are large discontinuities that may strongly influence phylogeographical patterns. The freshwater outflow of the Amazon basin is recognized as a major barrier that produces a break between Brazilian and Caribbean faunas. The vast oceanic distances between Brazil and the mid‐Atlantic ridge islands represent another formidable barrier. To assess the relative importance of these barriers, we compared a fragment of the mitochondrial DNA (mtDNA) cytochrome b gene among populations of three species of Atlantic surgeonfishes: Acanthurus bahianus, A. chirurgus and A. coeruleus. These species have similar life histories but different adult habitat preferences. The mtDNA data show no population structure between Brazil and the mid‐Atlantic islands, indicating that this oceanic barrier is readily traversed by the pelagic larval stage of all three surgeonfishes, which spend ~45–70 days in the pelagic environment. The Amazon is a strong barrier to dispersal of A. bahianus (d = 0.024, ΦST = 0.724), a modest barrier for A. coeruleus (ΦST = 0.356), and has no discernible effect as a barrier for A. chirurgus. The later species has been collected on soft bottoms with sponge habitats under the Amazon outflow, indicating that relaxed adult habitat requirements enable it to readily cross that barrier. A limited ability to use soft bottom habitats may also explain the low (but significant) population structure in A. coeruleus. In contrast, A. bahianus has not been collected over deep sponge bottoms, and rarely settles outside shallow reefs. Overall, adult habitat preferences seem to be the factor that differentiates phylogeographical patterns in these reef‐associated species.

The origins of tropical marine biodiversity

Recent phylogeographic studies have overturned three paradigms for the origins of marine biodiversity. (i) Physical (allopatric) isolation is not the sole avenue for marine speciation: many species diverge along ecological boundaries. (ii) Peripheral habitats such as oceanic archipelagos are not evolutionary graveyards: these regions can export biodiversity. (iii) Speciation in marine and terrestrial ecosystems follow similar processes but are not the same: opportunities for allopatric isolation are fewer in the oceans, leaving greater opportunity for speciation along ecological boundaries. Biodiversity hotspots such as the Caribbean Sea and the Indo-Pacific Coral Triangle produce and export species, but can also accumulate biodiversity produced in peripheral habitats. Both hotspots and peripheral ecosystems benefit from this exchange in a process dubbed biodiversity feedback.

Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish

The last tropical connection between Atlantic and Indian–Pacific habitats closed c. 2 million years ago (Ma), with the onset of cold‐water upwelling off southwestern Africa. Yet comparative morphology indicates more recent connections in several taxa, including reef‐associated gobies (genus Gnatholepis). Coalescence and phylogenetic analyses of mtDNA cytochrome b sequences demonstrate that Gnatholepis invaded the Atlantic during an interglacial period ∼145 000 years ago (d = 0.0054), colonizing from the Indian Ocean to the western Atlantic, and subsequently to the central (∼100 000 years ago) and eastern Atlantic (∼30 000 years ago). Census data show a contemporary range expansion in the northeastern Atlantic linked to global warming.

Phylogeography of the reef fish Cephalopholis argus(Epinephelidae) indicates Pleistocene isolation across the indo-pacific barrier with contemporary overlap in the coral triangle

BackgroundThe Coral Triangle (CT), bounded by the Philippines, the Malay Peninsula, and New Guinea, is the epicenter of marine biodiversity. Hypotheses that explain the source of this rich biodiversity include 1) the center of origin, 2) the center of accumulation, and 3) the region of overlap. Here we contribute to the debate with a phylogeographic survey of a widely distributed reef fish, the Peacock Grouper (Cephalopholis argus; Epinephelidae) at 21 locations (N = 550) using DNA sequence data from mtDNA cytochrome b and two nuclear introns (gonadotropin-releasing hormone and S7 ribosomal protein).ResultsPopulation structure was significant (ΦST = 0.297, P < 0.001; FST = 0.078, P < 0.001; FST = 0.099, P < 0.001 for the three loci, respectively) among five regions: French Polynesia, the central-west Pacific (Line Islands to northeastern Australia), Indo-Pacific boundary (Bali and Rowley Shoals), eastern Indian Ocean (Cocos/Keeling and Christmas Island), and western Indian Ocean (Diego Garcia, Oman, and Seychelles). A strong signal of isolation by distance was detected in both mtDNA (r = 0.749, P = 0.001) and the combined nuclear loci (r = 0.715, P < 0.001). We detected evidence of population expansion with migration toward the CT. Two clusters of haplotypes were detected in the mtDNA data (d = 0.008), corresponding to the Pacific and Indian Oceans, with a low level of introgression observed outside a mixing zone at the Pacific-Indian boundary.ConclusionsWe conclude that the Indo-Pacific Barrier, operating during low sea level associated with glaciation, defines the primary phylogeographic pattern in this species. These data support a scenario of isolation on the scale of 105 year glacial cycles, followed by population expansion toward the CT, and overlap of divergent lineages at the Pacific-Indian boundary. This pattern of isolation, divergence, and subsequent overlap likely contributes to species richness at the adjacent CT and is consistent with the region of overlap hypothesis.

Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes

How do biogeographically different provinces arise in response to oceanic barriers to dispersal? Here, we analyse how traits related to the pelagic dispersal and adult biology of 985 tropical reef fish species correlate with their establishing populations on both sides of two Atlantic marine barriers: the Mid-Atlantic Barrier (MAB) and the Amazon–Orinoco Plume (AOP). Generalized linear mixed-effects models indicate that predictors for successful barrier crossing are the ability to raft with flotsam for the deep-water MAB, non-reef habitat usage for the freshwater and sediment-rich AOP, and large adult-size and large latitudinal-range for both barriers. Variation in larval-development mode, often thought to be broadly related to larval-dispersal potential, is not a significant predictor in either case. Many more species of greater taxonomic diversity cross the AOP than the MAB. Rafters readily cross both barriers but represent a much smaller proportion of AOP crossers than MAB crossers. Successful establishment after crossing both barriers may be facilitated by broad environmental tolerance associated with large body size and wide latitudinal-range. These results highlight the need to look beyond larval-dispersal potential and assess adult-biology traits when assessing determinants of successful movements across marine barriers.

Mitochondrial DNA and Color Pattern Variation in Three Western Atlantic Halichoeres (Labridae), with the Revalidation of Two Species

Abstract Genetic surveys of widely distributed marine species often find previously undetected biodiversity. In the present study, populations of three species of Halichoeres were sampled across their entire geographical ranges: Halichoeres cyanocephalus and Halichoeres maculipinna were sampled on both sides of the Amazon freshwater outflow, the main biogeographic barrier in the tropical western Atlantic; and Halichoeres garnoti was sampled in the Caribbean and Bermuda. Genetic divergences between populations separated by the Amazon ranged from 2.3% in H. cyanocephalus to 6.5% in H. maculipinna. There is inconsistency between color differences and genetic partitions in the species surveyed. The color differences between populations of H. cyanocephalus and H. maculipinna correspond to deep genetic partitions at the cytochrome b locus. However, genetic similarity at this same locus was observed between populations of H. garnoti with striking color differences. Based on the combination of the observed genetic differences with diagnostic color differences, the Brazilian species Halichoeres dimidiatus (Agassiz) and Halichoeres penrosei Starks, 1913 are revalidated. In addition, a neotype is designated to H. cyanocephalus (Bloch, 1791), to clarify its taxonomic status and type locality. All species analyzed have a similar larval dispersal potential, but varying degrees of genetic divergences were observed, indicating that benthic stage ecology may also play a role in speciation in this group.

Fish biodiversity and conservation in South America

The freshwater and marine fish faunas of South America are the most diverse on Earth, with current species richness estimates standing above 9100 species. In addition, over the last decade at least 100 species were described every year. There are currently about 5160 freshwater fish species, and the estimate for the freshwater fish fauna alone points to a final diversity between 8000 and 9000 species. South America also has c. 4000 species of marine fishes. The mega-diverse fish faunas of South America evolved over a period of >100 million years, with most lineages tracing origins to Gondwana and the adjacent Tethys Sea. This high diversity was in part maintained by escaping the mass extinctions and biotic turnovers associated with Cenozoic climate cooling, the formation of boreal and temperate zones at high latitudes and aridification in many places at equatorial latitudes. The fresh waters of the continent are divided into 13 basin complexes, large basins consolidated as a single unit plus historically connected adjacent coastal drainages, and smaller coastal basins grouped together on the basis of biogeographic criteria. Species diversity, endemism, noteworthy groups and state of knowledge of each basin complex are described. Marine habitats around South America, both coastal and oceanic, are also described in terms of fish diversity, endemism and state of knowledge. Because of extensive land use changes, hydroelectric damming, water divergence for irrigation, urbanization, sedimentation and overfishing 4-10% of all fish species in South America face some degree of extinction risk, mainly due to habitat loss and degradation. These figures suggest that the conservation status of South American freshwater fish faunas is better than in most other regions of the world, but the marine fishes are as threatened as elsewhere. Conserving the remarkable aquatic habitats and fishes of South America is a growing challenge in face of the rapid anthropogenic changes of the 21st century, and deserves attention from conservationists and policy makers.

Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae).

The high biodiversity of tropical marine hotspots has long intrigued evolutionary biologists and biogeographers. The genus Haemulon (grunts) is one of the most important (numerically, ecologically, and economically) reef fish groups in the New World and an excellent candidate to test hypotheses of speciation and diversity generation in the Greater Caribbean, the richest Atlantic biodiversity hotspot, as well as the eastern Pacific. To elucidate the phylogenetic relationships among the species of Haemulon, we obtained a combined total of 2639 base pairs from two mitochondrial genes (cytochrome b and cytochrome oxidase I), and two nuclear genes (TMO-4C4 and RAG2) from all nominal species. Parsimony, Maximum likelihood, and Bayesian analyses resulted in a well-resolved phylogeny with almost identical topologies. Previous phylogenetic hypotheses based on adult morphology, such as the close relationship among H. aurolineatum, H. boschmae, and H. striatum were not supported, whereas others using developmental characters, such as the relationship between H. plumieri and H. sciurus, were confirmed. Our data also indicate that the populations of the nominal H. steindachneri from the two sides of the Isthmus of Panama are genetically divergent at the species level in each ocean, and that the boga, Inermia vittata (family Inermiidae), belongs in the genus Haemulon. This evidence implies that there are 21 valid species of Haemulon, two more than previously recognized. The Amazon barrier and the Isthmus of Panama seem to have played roles in allopatric speciation of Haemulon. However, the majority of sister species pairs have completely overlapping distributions, indicating that vicariance is not the only process driving speciation in this genus. We conclude that both vicariance between biogeographic provinces, and ecological mechanisms of speciation within provinces contribute to species richness in the genus Haemulon.