Genomic evidence indicates small island-resident populations and sex-biased behaviors of Hawaiian reef Manta Rays.

BACKGROUND: Reef manta rays (Mobula alfredi) are globally distributed in tropical and subtropical seas. Their life history traits (slow growth, late maturity, low reproductive output) make them vulnerable to perturbations and therefore require informed management strategies. Previous studies have reported wide-spread genetic connectivity along continental shelves suggesting high gene flow along continuous habitats spanning hundreds of kilometers. However, in the Hawaiian Islands, tagging and photo-identification evidence suggest island populations are isolated despite proximity, a hypothesis that has not yet been evaluated with genetic data. RESULTS: This island-resident hypothesis was tested by analyzing whole mitogenome haplotypes and 2048 nuclear single nucleotide polymorphisms (SNPs) between M. alfredi (n = 38) on Hawai'i Island and Maui Nui (the 4-island complex of Maui, Moloka'i, Lana'i and Kaho'olawe). Strong divergence in the mitogenome (ΦST = 0.488) relative to nuclear genome-wide SNPs (neutral FST = 0.003; outlier FST = 0.186), and clustering of mitochondrial haplotypes among islands provides robust evidence that female reef manta rays are strongly philopatric and do not migrate between these two island groups. Combined with restricted male-mediated migration, equivalent to a single male moving between islands every 2.2 generations (~ 64 years), we provide evidence these populations are significantly demographically isolated. Estimates of contemporary effective population size (Ne) are 104 (95% CI: 99-110) in Hawai'i Island and 129 (95% CI: 122-136) in Maui Nui. CONCLUSIONS: Concordant with evidence from photo identification and tagging studies, these genetic results indicate reef manta rays in Hawai'i have small, genetically-isolated resident island populations. We hypothesize that due to the Island Mass Effect, large islands provide sufficient resources to support resident populations, thereby making crossing deep channels separating island groups unnecessary. Small effective population size, low genetic diversity, and k-selected life history traits make these isolated populations vulnerable to region-specific anthropogenic threats, which include entanglement, boat strikes, and habitat degradation. The long-term persistence of reef manta rays in the Hawaiian Islands will require island-specific management strategies.

The complete mitochondrial genome of the Reef Manta Ray, Mobula alfredi, from Hawaii.

We provide the complete mitochondrial genome of the reef manta ray, Mobula alfredi, using an ezRAD approach. The total length of the mitogenome was 18,166 bp and contained 13 protein-coding genes, 22 transfer RNAs genes, two ribosomal RNA genes, and one non-coding control region. The gene organization and length are similar to other Mobula species. This reference mitogenome that includes the control region is expected to be a valuable resource for molecular-based species identification, population genomics, and phylogeography.

Genomic assessment of larval odyssey: self-recruitment and biased settlement in the Hawaiian surgeonfish Acanthurus triostegus sandvicensis.

The gap between spawning and settlement location of marine fishes, where the larvae occupy an oceanic phase, is a great mystery in both natural history and conservation. Recent genomic approaches provide some resolution, especially in linking parent to offspring with assays of nucleotide polymorphisms. Here, the authors applied this method to the endemic Hawaiian convict tang (Acanthurus triostegus sandvicensis), a surgeonfish with a long pelagic larval stage of c. 54-77 days. They collected 606 adults and 607 juveniles from 23 locations around the island of O'ahu, Hawai'i. Based on 399 single nucleotide polymorphisms, the authors assigned 68 of these juveniles back to a parent (11.2% assignment rate). Each side of the island showed significant population differentiation, with higher levels in the west and north. The west and north sides of the island also had little evidence of recruitment, which may be due to westerly currents in the region or an artefact of uneven sampling. In contrast, the majority of juveniles (94%) sampled along the eastern shore originated on that side of the island, primarily within semi-enclosed Kane'ohe Bay. Nearly half of the juveniles assigned to parents were found in the southern part of Kane'ohe Bay, with local settlement likely facilitated by extended water residence time. Several instances of self-recruitment, when juveniles return to their natal location, were observed along the eastern and southern shores. Cumulatively, these findings indicate that most dispersal is between adjacent regions on the eastern and southern shores. Regional management efforts for Acanthurus triostegus and possibly other reef fishes will be effective only with collaboration among adjacent coastal communities, consistent with the traditional moku system of native Hawaiian resource management.

Species Radiations in the Sea: What the Flock?

Species flocks are proliferations of closely-related species, usually after colonization of depauperate habitat. These radiations are abundant on oceanic islands and in ancient freshwater lakes, but rare in marine habitats. This contrast is well documented in the Hawaiian Archipelago, where terrestrial examples include the speciose silverswords (sunflower family Asteraceae), Drosophila fruit flies, and honeycreepers (passerine birds), all derived from one or a few ancestral lineages. The marine fauna of Hawai'i is also the product of rare colonization events, but these colonizations usually yield only one species. Dispersal ability is key to understanding this evolutionary inequity. While terrestrial fauna rarely colonize between oceanic islands, marine fauna with pelagic larvae can make this leap in every generation. An informative exception is the marine fauna that lack a pelagic larval stage. These low-dispersal species emulate a "terrestrial" mode of reproduction (brooding, viviparity, crawl-away larvae), yielding marine species flocks in scattered locations around the world. Elsewhere, aquatic species flocks are concentrated in specific geographic settings, including the ancient lakes of Baikal (Siberia) and Tanganyika (eastern Africa), and Antarctica. These locations host multiple species flocks across a broad taxonomic spectrum, indicating a unifying evolutionary phenomenon. Hence marine species flocks can be singular cases that arise due to restricted dispersal or other intrinsic features, or they can be geographically clustered, promoted by extrinsic ecological circumstances. Here, we review and contrast intrinsic cases of species flocks in individual taxa, and extrinsic cases of geological/ecological opportunity, to elucidate the processes of species radiations.

Life-history characteristics of an exploited bonefish Albula glossodonta population in a remote South Pacific atoll.

Bonefishes Albula spp. are important components of subsistence fisheries and lucrative sport fishing industries throughout their circumtropical distribution. In Oceania, however, Albula spp. have historically been overexploited and there is a growing need to balance the demands of competing fishing sectors, making the description of their life history a regional priority. To this aim, we collected biological samples from Albula spp. of Anaa atoll, French Polynesia, to identify the species that compose the stock and estimate their life-history parameters including age, growth, reproduction and natural mortality. Our results indicate that Albula glossodonta is the species of bonefish present, with a maximum age that is below the, 20 year longevity of the genus (8 years in males and 10 years in females). Differential growth patterns existed between the two sexes (L∞ = 58, 78 cm fork length (LF ) and K = 0.38, 0.21 for males and females, respectively). Males attained sexual maturity at 43 cm LF (c. 3 years) whereas females matured at 48 cm LF (c. 4 years) and oocyte production was significantly related to body mass, with a maximum batch fecundity of 1,133,767 oocytes in a 4406 g (70 cm LF ) female. The gonado-somatic index of harvested fishes indicated that the spawning season extends from March through September. Based on the observation of a, 20 year bonefish at the proximate Tetiaroa Atoll and several empirical models, estimates of natural mortality ranged from 0.21 to 0.68; however, an estimate of 0.21 was deemed most appropriate. This information facilitated the resurgence of a Rahui (temporary fishing closure) and community-based management to protect A. glossodonta during a critical portion of their spawning season and in this context our results provide an important demographic baseline in evaluating the recovery of this fishery.

Shifting reef fish assemblages along a depth gradient in Pohnpei, Micronesia.

Mesophotic coral ecosystems (MCEs) continue to be understudied, especially in island locations spread across the Indo-Pacific Ocean. Pohnpei is the largest island in the Federated States of Micronesia, with a well-developed barrier reef, and steep slopes that descend to more than 1,000 m. Here we conducted visual surveys along a depth gradient of 0 to 60 m in addition to video surveys that extend to 130 m, with 72 belt transects and 12 roving surveys using closed-circuit rebreathers, to test for changes in reef fish composition from shallow to mesophotic depths. We observed 304 fish species across 47 families with the majority confined to shallow habitat. Taxonomic and trophic positions at 30 m showed similar compositions when compared against all other depths. However, assemblages were comprised of a distinct shallow (<30 m) and deep (>30 m) group, suggesting 30 m as a transition zone between these communities. Shallow specialists had a high probability of being herbivores and deep specialists had a higher probability of being planktivores. Acanthuridae (surgeonfishes), Holocentridae (soldierfishes), and Labridae (wrasses) were associated primarily with shallow habitat, while Pomacentridae (damselfishes) and Serranidae (groupers) were associated with deep habitat. Four species may indicate Central Pacific mesophotic habitat: Chromis circumaurea, Luzonichthys seaver, Odontanthias borbonius, and an undescribed slopefish (Symphysanodon sp.). This study supports the 30 m depth profile as a transition zone between shallow and mesophotic ecosystems (consistent with accepted definitions of MCEs), with evidence of multiple transition zones below 30 m. Disturbances restricted to either region are not likely to immediately impact the other and both ecosystems should be considered separately in management of reefs near human population centers.

The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages.

The banded coral shrimp, Stenopus hispidus (Crustacea: Decapoda: Stenopodidea) is a popular marine ornamental species with a circumtropical distribution. The planktonic larval stage lasts ∼120-253 days, indicating considerable dispersal potential, but few studies have investigated genetic connectivity on a global scale in marine invertebrates. To resolve patterns of divergence and phylogeography of S. hispidus, we surveyed 525 bp of mitochondrial cytochrome c oxidase subunit I (COI) from 198 individuals sampled at 10 locations across ∼27,000 km of the species range. Phylogenetic analyses reveal that S. hispidus has a Western Atlantic lineage and a widely distributed Indo-Pacific lineage, separated by sequence divergence of 2.1%. Genetic diversity is much higher in the Western Atlantic (h = 0.929; π = 0.004) relative to the Indo-Pacific (h = 0.105; π < 0.001), and coalescent analyses indicate that the Indo-Pacific population expanded more recently (95% HPD (highest posterior density) = 60,000-400,000 yr) than the Western Atlantic population (95% HPD = 300,000-760,000 yr). Divergence of the Western Atlantic and Pacific lineages is estimated at 710,000-1.8 million years ago, which does not readily align with commonly implicated colonization events between the ocean basins. The estimated age of populations contradicts the prevailing dispersal route for tropical marine biodiversity (Indo-Pacific to Atlantic) with the oldest and most diverse population in the Atlantic, and a recent population expansion with a single common haplotype shared throughout the vast Indian and Pacific oceans. In contrast to the circumtropical fishes, this diminutive reef shrimp challenges our understanding of conventional dispersal capabilities of marine species.

Regal phylogeography: Range-wide survey of the marine angelfish Pygoplites diacanthus reveals evolutionary partitions between the Red Sea, Indian Ocean, and Pacific Ocean.

The regal angelfish (Pygoplites diacanthus; family Pomacanthidae) occurs on reefs from the Red Sea to the central Pacific, with an Indian Ocean/Rea Sea color morph distinct from a Pacific Ocean morph. To assess population differentiation and evaluate the possibility of cryptic evolutionary partitions in this monotypic genus, we surveyed mtDNA cytochrome b and two nuclear introns (S7 and RAG2) in 547 individuals from 15 locations. Phylogeographic analyses revealed four mtDNA lineages (d=0.006-0.015) corresponding to the Pacific Ocean, the Red Sea, and two admixed lineages in the Indian Ocean, a pattern consistent with known biogeographic barriers. Christmas Island in the eastern Indian Ocean had both Indian and Pacific lineages. Both S7 and RAG2 showed strong population-level differentiation between the Red Sea, Indian Ocean, and Pacific Ocean (ΦST=0.066-0.512). The only consistent population sub-structure within these three regions was at the Society Islands (French Polynesia), where surrounding oceanographic conditions may reinforce isolation. Coalescence analyses indicate the Pacific (1.7Ma) as the oldest extant lineage followed by the Red Sea lineage (1.4Ma). Results from a median-joining network suggest radiations of two lineages from the Red Sea that currently occupy the Indian Ocean (0.7-0.9Ma). Persistence of a Red Sea lineage through Pleistocene glacial cycles suggests a long-term refuge in this region. The affiliation of Pacific and Red Sea populations, apparent in cytochrome b and S7 (but equivocal in RAG2) raises the hypothesis that the Indian Ocean was recolonized from the Red Sea, possibly more than once. Assessing the genetic architecture of this widespread monotypic genus reveals cryptic evolutionary diversity that merits subspecific recognition. We recommend P.d. diacanthus and P.d. flavescens for the Pacific and Indian Ocean/Red Sea forms.

Ecological and morphological traits predict depth-generalist fishes on coral reefs.

Ecological communities that occupy similar habitats may exhibit functional convergence despite significant geographical distances and taxonomic dissimilarity. On coral reefs, steep gradients in key environmental variables (e.g. light and wave energy) restrict some species to shallow depths. We show that depth-generalist reef fishes are correlated with two species-level traits: caudal fin aspect ratio and diet. Fishes with high aspect ratio (lunate) caudal fins produce weaker vortices in the water column while swimming, and we propose that 'silent swimming' reduces the likelihood of detection and provides an advantage on deeper reefs with lower light irradiance and water motion. Significant differences in depth preference among trophic guilds reflect variations in the availability of different food sources along a depth gradient. The significance of these two traits across three geographically and taxonomically distinct assemblages suggests that deep-water habitats exert a strong environmental filter on coral reef-fish assemblages.

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.

Large-scale introduction of the Indo-Pacific damselfish Abudefduf vaigiensis into Hawai'i promotes genetic swamping of the endemic congener A. abdominalis.

Hybridization in the ocean was once considered rare, a process prohibited by the rapid evolution of intrinsic reproductive barriers in a high-dispersal medium. However, recent genetic surveys have prompted a reappraisal of marine hybridization as an important demographic and evolutionary process. The Hawaiian Archipelago offers an unusual case history in this arena, due to the recent arrival of the widely distributed Indo-Pacific sergeant (Abudefduf vaigiensis), which is hybridizing with the endemic congener, A. abdominalis. Surveys of mtDNA and three nuclear loci across Hawai'i (N = 396, Abudefduf abdominalis and N = 314, A. vaigiensis) reveal that hybridization is significantly higher in the human-perturbed southeast archipelago (19.8%), tapering off to 5.9% in the pristine northwest archipelago. While densities of the two species varied throughout Hawai'i, hybridization was highest in regions with similar species densities, contradicting the generalization that the rarity of one species promotes interspecific mating. Our finding of later generation hybrids throughout the archipelago invokes the possibility of genetic swamping of the endemic species. Exaptation, an adaptation with unintended consequences, may explain these findings: the endemic species has transient yellow coloration during reproduction, whereas the introduced species has yellow coloration continuously as adults, in effect a permanent signal of reproductive receptivity. Haplotype diversity is higher in Hawaiian A. vaigiensis than in our samples from the native range, indicating large-scale colonization almost certainly facilitated by the historically recent surge of marine debris. In this chain of events, marine debris promotes colonization, exaptation promotes hybridization, and introgression invokes the possible collapse of an endemic species.