Silky shark (Carcharhinus falciformis, Carcharhinidae) numbers have declined steeply in recent decades due to the fin fishery and bycatch in pelagic fisheries. Due to a lack of data on stock delineations, this species is currently managed in ocean-spanning jurisdictions defined by regional fisheries management organizations (RFMOs). Here we investigate the global stock structure of silky sharks and compare population structure to the four RFMO boundaries. Using high-throughput sequencing from pooled individuals (pool-seq) based on 628 specimens collected opportunistically across 11 circumglobal regions, yielding 854 nuclear single nucleotide polymorphisms (SNPs) and 23 mtDNA SNPs. Results indicate significant population genetic structure between all 11 regional sampling locations, with discriminant analysis of principal components (DAPC) identifying seven discrete groups. Within the Atlantic and Indo-Pacific Oceans, F ST values ranged from 0.014 to 0.035 for nuclear (nDNA) markers, and from 0.012 to 0.160 for whole mtDNA genomes, with much higher values between than within oceans (mtDNA: 0.383-0.844, nDNA: 0.042-0.078). Using an analysis of molecular variance (AMOVA) framework, 22.24% of the observed population variance is explained by RFMOs, 32.1% is explained among ocean basins, and 34.81% is explained by the DAPC-identified groups. We find significant population genetic structure within the jurisdiction of every RFMO, from which we have more than a single sampling site. Our genomic-scale results indicate discordance between population genetic structure and RFMOs, highlighting the need for a detailed study to accurately identify stock boundaries.
Bonefishes and other elopomorphs have a unique, transparent leptocephalus larval stage that is challenging to study due to its cryptic nature. Understanding life history is important especially considering adult bonefishes in Hawaiʻi are highly sought gamefish valued for their tenacious fight on rod-and-reel and delicate taste. In this study light traps were used to capture leptocephali at three nearshore locations around Oʻahu, Hawaiʻi. Across 130 + h of trapping, 59 larvae were captured, most during 2000–2100 h on rising tides. Lengths ranged from 54 to 66 mm, indicating late stage I larvae. Otolith analyses (N = 26) revealed ages from 28 to 72 days with an average age of about 48 days. Genetic species identification on a subset of the larvae showed that one of 28 total specimens was Albula virgata, which is endemic to Hawaiʻi, and the remaining were the Indo-Pacific A. glossodonta. Along with calm inshore waters, estuarine habitat appears to be a critical element for leptocephali recruitment success. Reducing impacts to these estuarine habitats and protecting and restoring freshwater input may have positive impacts on leptocephali recruitment, the essential starting point for thriving bonefish fisheries in Hawaiʻi.
Efforts to conserve biodiversity have been hampered by long-standing biases, including a disproportionate focus on particular taxa and ecosystems with minimal attention to underlying genetic diversity. We assessed whether these biases have persisted over the past four decades by analyzing trends in 17,502 research articles published in four top conservation-focused journals. Overall, we found that historical biases in conservation biology research remain entrenched. Despite increasing numbers of conservation articles published each decade from 1980 to 2020, research effort has increasingly focused on the same suite of taxa. Surprisingly, some of the most-studied species in these conservation articles had low conservation risk, including several domesticated animals. Animals and terrestrial ecosystems are consistently over-represented while plants, fungi, and freshwater ecosystems remain under-represented. Strategically funding investigations of understudied species and ecosystems will ensure more effective conservation effort across multiple levels of biodiversity, alleviate impediments to biodiversity targets, and ultimately prevent further extinctions.
The collector urchin, Tripneustes gratilla, is an ecologically important member of the grazing community of Hawaii's coral reefs. Beyond its ability to maintain balance between native seaweeds and corals, T. gratilla has also been used as a food source and a biocontrol agent against alien invasive algae species. Due to overexploitation, habitat degradation, and other stressors, their populations face local extirpation. However, artificial reproductive techniques, such as cryopreservation, could provide more consistent seedstock throughout the year to supplement aquaculture efforts. Although the sperm and larvae of temperate urchins have been successfully cryopreserved, tropical urchins living on coral reefs have not. Here, we investigated the urchin embryos' tolerance to various cryoprotectants and cooling rates to develop a cryopreservation protocol for T. gratilla. We found that using 1 M Me2SO with a cooling rate of 9.7 °C/min on gastrula stage embryos produced the best results with survival rates of up to 85.5% and up to 50.8% maturation to the 4-arm echinopluteus stage, assessed three days after thawing. Continued research could see cryopreservation added to the repertoire of artificial reproductive techniques for T. gratilla, thereby assisting in the preservation of this ecologically important urchin, all while augmenting aquaculture efforts that contribute to coral reef restoration.
If similar evolutionary forces maintain intra- and interspecific diversity, patterns of diversity at both levels of biological organization can be expected to covary across space. Although this prediction of a positive species-genetic diversity correlation (SGDC) has been tested for several taxa in natural landscapes, no study has yet evaluated the influence of the community delineation on these SGDCs. In this study, we focused on tropical fishes of the Indo-Pacific Ocean, using range-wide single nucleotide polymorphism data for a deep-sea fish ( Etelis coruscans ) and species presence data of 4878 Teleostei species. We investigated whether a diversity continuum occurred, for different community delineations (subfamily, family, order and class) and spatial extents, and which processes explained these diversity patterns. We found no association between genetic diversity and species richness (α-SGDC), regardless of the community and spatial extent. In contrast, we evidenced a positive relationship between genetic and species dissimilarities (β-SGDC) when the community was defined at the subfamily or family level of the species of interest, and when the Western Indian Ocean was excluded. This relationship was related to the imprint of dispersal processes across levels of biological organization in Lutjanidae. However, this positive β-SGDC was lost when considering higher taxonomic communities and at the scale of the entire Indo-Pacific, suggesting different responses of populations and communities to evolutionary processes at these scales. This study provides evidence that the taxonomic scale at which communities are defined and the spatial extent are pivotal to better understand the processes shaping diversity across levels of biological organization.
AbstractProteinase K (ProK) is regarded as an essential ingredient in most DNA extraction protocols for protein‐rich sample types such as tissue, blood, and mucus. However, ProK is expensive and may be unnecessary when samples are protein‐limited, such as environmental DNA (eDNA) from oligotrophic seawater. To investigate this, we filtered seawater through Sterivex cartridges from a mesocosm receiving input from the adjacent coral reef slope at the Hawai‘i Institute of Marine Biology. We tested whether the addition of varying levels of ProK (0 μL, 25 μL, 50 μL, 100 μL, or 150 μL—20 mg/mL stock concentrations) to 1.8 mL of lysis buffer affected DNA yield and the diversity, community composition, and detection of known organisms within the mesocosm community based on zero‐width operational taxonomic units (ZOTUs) obtained from DNA metabarcoding. We found no significant differences in diversity metrics among ProK quantities and dominant ZOTUs were consistent across concentrations. Over 50% of detected ZOTUs were shared among samples and only two ZOTUs were unique to samples of a particular ProK concentration. While the community composition among ProK quantities differed, pairwise community comparisons between quantities were not statistically significant and matched the known species composition of the mesocosm. These results suggest that rare ZOTUs and eDNA patchiness are driving overall community differences as opposed to extraction ingredients. Our data show that ProK is not essential when assessing communities from oligotrophic marine environments using eDNA and that the reduction or elimination of ProK can decrease sample preparation time and costs while maintaining data integrity.
Bonefishes and other elopomorphs have a unique, transparent leptocephalus larval stage that is challenging to study due to its cryptic nature. Understanding life history is important especially considering adult bonefishes in Hawai'i are highly sought gamefish valued for their tenacious fight on rod-and-reel and delicate taste. In this study light traps were used to capture leptocephali at three nearshore locations around O'ahu, Hawai'i. Across 130 + h of trapping, 59 larvae were captured, most during 2000-2100 h on rising tides. Lengths ranged from 54 to 66 mm, indicating late stage I larvae. Otolith analyses (N = 26) revealed ages from 28 to 72 days with an average age of about 48 days. Genetic species identification on a subset of the larvae showed that one of 28 total specimens was Albula virgata, which is endemic to Hawai'i, and the remaining were the Indo-Pacific A. glossodonta. Along with calm inshore waters, estuarine habitat appears to be a critical element for leptocephali recruitment success. Reducing impacts to these estuarine habitats and protecting and restoring freshwater input may have positive impacts on leptocephali recruitment, the essential starting point for thriving bonefish fisheries in Hawai'i.
Fishes are the original and most diverse group of vertebrates, including over 35,000 of the estimated 69,000 species with backbones. Most marine fishes have large geographic ranges that may provide some protection from extinction, but there are very important exceptions
Bonefishes are a nearshore species targeted by non-commercial anglers and subsistence fishers in the Central and South Pacific islands. Among the bonefish species in the Indo-Pacific region, Albula glossodonta are known to have one of the widest geographic ranges, from the Red Sea to the Central Pacific, but it is unknown how dispersive A. glossodonta are between geographically isolated islands. Volunteer anglers collected A. glossodonta fin clips from the main Hawaiian Islands in the North Pacific, Anaa Atoll in the South Pacific, and intermediate Kiritimati Island (Line Islands) to assess the scale of dispersal and population structure within the Pacific Ocean. Population genomics was conducted based on 208 individuals and 7225 SNPs. Although adult A. glossodonta exhibit strong site fidelity, genomic results show no population differentiation between Oahu and Maui in Hawai‘i. Bonefishes exhibit significant population structure between Anaa and Hawai‘i (FST = 0.096), with intermediate Kiritimati comprising admixed fishes. A lengthy larval duration likely promotes connectivity between Pacific islands. Regional management regimes may be most appropriate for a species with this level of dispersal.
Considerable research exists on the life history traits, evolutionary history, and environmental factors that shape the population genetic structure of marine organisms, including sharks and rays. Conservation concerns are particularly strong for this group as they are highly susceptible to anthropogenic stressors due to a combination of life history traits including late maturity and low fecundity. Here, we provide a review and synthesis of the global phylogeography of sharks and rays. We examined existing data for 40 species of sharks belonging to 17 genera and 19 species of rays belonging to 11 genera. Median joining haplotype networks were constructed for each species for the mtDNA cytochrome C oxidase subunit I (COI), and an Analysis of Molecular Variance (AMOVA) was conducted to understand patterns of genetic diversity and structure across the three major ocean basins-the Indian, Atlantic and Pacific Oceans. Haplotype networks showed very shallow coalescence in most species, a finding previously reported for marine teleosts. Star topologies were predominant among sharks while complex mutational topologies predominated among rays, a finding we attribute to extremely limited dispersal in the early life history of rays. Population structuring varied amongst species groups, apparently due to differences in life history traits including reproductive philopatry, site fidelity, pelagic habitat, migratory habits, and dispersal ability. In comparison to reef-associated and demersal species, pelagic and semi pelagic species showed lower levels of structure between and within ocean basins. As expected, there is variation between taxa and groups, but there are also some broad patterns that can guide management and conservation strategies.
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 Ka?ne'ohe Bay. Nearly half of the juveniles assigned to parents were found in the southern part of Ka?ne'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.
The Gila robusta species complex in the lower reaches of the Colorado River includes three nominal and contested species ( G. robusta, G. intermedia, and G. nigra ) originally defined by morphological and meristic characters. In subsequent investigations, none of these characters proved diagnostic, and species assignments were based on capture location. Two recent studies applied conservation genomics to assess species boundaries and reached contrasting conclusions: an ezRAD phylogenetic study resolved 5 lineages with poor alignment to species categories and proposed a single species with multiple population partitions. In contrast, a dd-RAD coalescent study concluded that the three nominal species are well-supported evolutionarily lineages. Here we developed a draft genome (~ 1.229 Gbp) to apply genome-wide coverage (10,246 SNPs) with nearly range-wide sampling of specimens ( G. robusta N = 266, G. intermedia N = 241, and G. nigra N = 117) to resolve this debate. All three nominal species were polyphyletic, whereas 5 of 8 watersheds were monophyletic. AMOVA partitioned 23.1% of genetic variance among nominal species, 30.9% among watersheds, and the Little Colorado River was highly distinct ( F ST ranged from 0.79 to 0.88 across analyses). Likewise, DAPC identified watersheds as more distinct than species, with the Little Colorado River having 297 fixed nucleotide differences compared to zero fixed differences among the three nominal species. In every analysis, geography explains more of the observed variance than putative taxonomy, and there are no diagnostic molecular or morphological characters to justify species designation. Our analysis reconciles previous work by showing that species identities based on type location are supported by significant divergence, but natural geographic partitions show consistently greater divergence. Thus, our data confirm Gila robusta as a single polytypic species with roughly a dozen highly isolated geographic populations, providing a strong scientific basis for watershed-based future conservation.
Mesophotic coral ecosystems (MCEs) are tropical reefs found at depths of ~30–150 m, below the region most heavily impacted by heat stress and other disturbances. Hence, MCEs may serve as potential refugia for threatened shallow reefs, but they also harbour depth‐endemic fauna distinct from shallow reefs. Previous studies have characterized biodiversity patterns along depth gradients, but focussed primarily on conspicuous taxa (fishes, corals, etc.). Environmental DNA (eDNA) metabarcoding offers a more holistic approach to assess biodiversity patterns across the tree of life. Here, we use three metabarcoding assays targeting fishes (16S rRNA), eukaryotes (18S rDNA) and metazoans (COI) to assess biodiversity change from the surface to ~90 m depth across 15‐m intervals at three sites within the Hawaiian Archipelago. We observed significant community differences between most depth zones, with distinct zonation centred at 45–60 m for eukaryotes and metazoans, but not for fishes. This finding may be attributable to the higher mobility of reef fishes, although methodological limitations are likely a contributing factor. The possibility for MCEs to serve as refugia is not excluded for fishes, but invertebrate communities >45 m are distinct, indicating limited connectivity for the majority of reef fauna. This study provides a new approach for surveying biodiversity on MCEs, revealing patterns in a much broader context than the limited‐taxon studies that comprise the bulk of our present knowledge.
We propose and define the "Habitat Persistence Hypothesis" (HPH) to explain the biogeographical distributions of organisms (especially fishes, invertebrates and algae) inhabiting tropical coral reefs. Both published and unpublished sources indicate that species occurring on deep coral reefs show higher rates of endemism and a less apparent biodiversity gradient across the Pacific Ocean than their counterparts inhabiting shallow coral reefs. The HPH accounts for these biogeographical differences by stipulating that deep reefs are relatively unaffected by sea level changes associated with glacial -interglacial cycles. Shallow -reef habitats may persist across sea level changes in regions with sloped bathymetry (e.g., continental regions and large islands), but are largely extirpated in regions with steep bathymetry (e.g., coral atolls). The HPH suggests that regions with habitat persistence are characterized by higher rates of endemism, and that patterns of attenuating diversity with increasing distance from centers of species richness are shaped by relatively recent recolonization of less persistent habitats from regions with greater habitat persistence. Whereas most existing hypotheses that attempt to explain biogeographical patterns observed on coral reefs (especially in the Indo-Pacific region) rely on observations limited to shallow (<30 m) coral -reef habitat and invoke processes operating on speciation time -scales (10(7) - 10(8) yr), the HPH incorporates patterns observed within the remaining 80% of coral -reef habitat (30 - 150 m) and invokes processes operating on time scales associated with sea -level changes (10(5) - 10(6) yr). The HPH posits seven specific predictions about coral -reef biogeography that can be directly tested to distinguish it from previous hypotheses. Our intention is to describe the rationale and qualitative support for the HPH with the hope of providing a framework for accumulating sufficient quantitative data to test the predictions, which we anticipate will require decades of robust field surveys.
Globally distributed marine taxa are well suited for investigations of biogeographic impacts on genetic diversity, connectivity, and population demography. The sea turtle genus Lepidochelys includes the wide-ranging and abundant olive ridley ( L. olivacea ), and the geographically restricted and ‘Critically Endangered’ Kemp’s ridley ( L. kempii ). To investigate their historical biogeography, we analyzed a large dataset of mitochondrial DNA (mtDNA) sequences from olive (n = 943) and Kemp’s (n = 287) ridleys, and genotyped 15 nuclear microsatellite loci in a global sample of olive ridleys (n = 285). We found that the ridley species split ~ 7.5 million years ago, before the Panama Isthmus closure. The most ancient mitochondrial olive ridley lineage, located in the Indian Ocean, was dated to ~ 2.2 Mya. Both mitochondrial and nuclear markers revealed significant structure for olive ridleys between Atlantic (ATL), East Pacific (EP), and Indo-West Pacific (IWP) areas. However, the divergence of mtDNA clades was very recent (< 1 Mya) with low within- clade diversity, supporting a recurrent extinction-recolonization model for these ocean regions. All data showed that ATL and IWP groups were more closely related than those in the EP, with mtDNA data supporting recent recolonization of the ATL from the IWP. Individual olive ridley dispersal between the ATL, EP, and IN/IWP could be interpreted as more male- than female-biased, and genetic diversity was lowest in the Atlantic Ocean. All populations showed signs of recent expansion, and estimated time frames were concordant with their recent colonization history. Investigating species abundance and distribution changes over time is central to evolutionary biology, and this study provides a historical biogeographic context for marine vertebrate conservation and management.
Novel methodologies now make it possible to track the complete geographical movements of seafood species from reproduction to human consumption. Doing so will better inform consumers and assist resource managers in matching fisheries and conservation policies with natural borders and pathways, including stock boundaries, networks of marine protected areas, and fisheries management areas. Such mapping necessitates an unprecedented synthesis of natural and social sciences, including knowledge of adult fish population abundance and movements, egg output, larval dispersal, and recruitment to juvenile and adult habitats, as well as fisheries stock assessment, capture, and distribution through human social networks. The challenge is to fully integrate oceanography, population genetics, ecology, and social sciences with fisheries biology to reveal the patterns and mechanisms of "Fish Flow" from spawning to supper. As practitioners representing all five of these disciplines, we believe that Fish Flow analyses will promote sustainable fisheries management and marine conservation efforts, and may foster public knowledge, wise seafood choices, and appreciation of social-ecological interconnections involving fisheries.
The Hawaiian Archipelago has served as a natural laboratory to assess genetic connectivity patterns across a broad spectrum of taxonomic and ecological diversity. Almost all these studies were based on a few targeted loci, but technologies now allow us to assess population structure with genomic coverage and greater resolution. Here, we provide a SNP-based analysis for an endemic surgeonfish, Acanthurus triostegus sandvicensis (manini) across the Hawaiian Archipelago and adjacent Johnston Atoll ( N = 461). Based on 3649 SNPs, manini showed population structure in the main Hawaiian Islands, but genetic homogeneity across most of the northwestern extent of the archipelago (overall F ST = 0.033, P < 0.001). Net migration occurred from Johnston Atoll into Hawai‘i, providing further support for Johnston Atoll being a pathway for dispersal (or colonization) into Hawai′i. These results highlight the higher efficacy of genomic sequencing to characterize fine-scale patterns of connectivity relative to a targeted loci approach and, moving forward, may invoke a reassessment of past connectivity studies in a genomics framework.
The California horn shark (Heterodontus francisci) is a small demersal species distributed from southern California and the Channel Islands to Baja California and the Gulf of California. These nocturnal reef predators maintain small home-ranges as adults and lay auger-shaped egg cases that become wedged into the substrate. While population trends are not well documented, this species is subject to fishing pressure through portions of its range and has been identified as vulnerable to overexploitation. Here, we present a survey of 318 specimens from across the range, using mtDNA control region sequences to provide the first genetic assessment of H. francisci. Overall population structure (ΦST = 0.266, P < 0.001) is consistent with limited dispersal as indicated by life history, with two distinct features. Population structure along the continuous coastline is low, with no discernable breaks from Santa Barbara, CA to Bahia Tortugas (Baja California Sur, Mexico); however, there is a notable partition at Punta Eugenia (BCS), a well-known biogeographic break between tropical and subtropical marine faunas. In contrast, population structure is much higher (max ΦST = 0.601, P < 0.05) between the coast and adjacent Channel Islands, a minimum distance of 19 km, indicating that horn sharks rarely disperse across deep habitat and open water. Population structure in most elasmobranchs is measured on a scale of hundreds to thousands of kilometers, but the California Horn Shark has population partitions on an unprecedented small scale, indicating a need for localized management strategies which ensure adequate protection of distinct stocks.
Mesophotic coral ecosystems (MCEs: ~30 to 100+ m depth) may be older and more stable than shallow coral ecosystems that are more prone to disturbances in both the long term (glacial sea level cycles) and short term (heavy weather and anthropogenic activities). Here, we assess the phylogeography of two MCE fishes, the soldierfish Myripristis chryseres (N = 85) and the squirrelfish Neoniphon aurolineatus (N = 74), with mtDNA cytochrome oxidase C subunit I. Our goal is to resolve population genetic diversity across the Central and West Pacific and compare these patterns to three shallow-reef species in the same taxonomic family (Holocentridae). Significant population structure (ΦST = 0.148, p = 0.01) was observed in N. aurolineatus, while no structure was detected in M. chryseres (ΦST = −0.031, p = 0.83), a finding that matches the shallow-water congener M. berndti (ΦST = −0.007, p = 0.63) across the same range. Nucleotide diversity in the MCE fishes was low (π = 0.0024–0.0028) compared to shallow counterparts (π = 0.003–0.006). Coalescence times calculated for M. chryseres (~272,000 years) and N. aurolineatus (~284,000 years) are more recent or comparable to the shallow-water holocentrids (~220,000–916,000 years). We conclude that the shallow genetic coalescence characteristic of shallow-water marine fishes cannot be attributed to frequent disturbance. We see no evidence from holocentrid species that MCEs are older or more stable habitats.