Brian Bowen | University of Hawaii (original) (raw)

Papers by Brian Bowen

Cell Reports Sustainability, 2024

Efforts to conserve biodiversity have been hampered by long-standing biases, including a dispropo... more 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.

Environmental DNA, 2024

Successful nucleic acid purification during DNA extraction from tissues requires the effective di... more Successful nucleic acid purification during DNA extraction from tissues requires the effective disruption of cells, denaturation of nucleoprotein complexes, and the inactivation of nucleases. A fundamental component of most DNA extraction protocols is the enzyme Proteinase K (ProK). It breaks down protein components of cell membranes, digests various proteins such as histones bound to DNA, and inactivates enzymes such as DNases and RNases that de

Cryobiology, 2024

The collector urchin, Tripneustes gratilla, is an ecologically important member of the grazing co... more The collector urchin, Tripneustes gratilla, is an ecologically important member of the grazing community of Hawai'i'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.

Fishes, 2023

Bonefishes are a nearshore species targeted by non-commercial anglers and subsistence fishers in ... more 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.

Molecular Ecology, 2023

Mesophotic coral ecosystems (MCEs) are tropical reefs found at depths of ~30–150 m, below the reg... more 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.

Scientific Reports, 2023

The Gila robusta species complex in the lower reaches of the Colorado River includes three nomina... more 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.

PeerJ, 2023

Considerable research exists on the life history traits, evolutionary history, and environmental ... more 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.

Journal of Heredity, Jul 1, 2020

Deep-sea habitats may drive unique dispersal and demographic patterns for fishes, but population ... more Deep-sea habitats may drive unique dispersal and demographic patterns for fishes, but population genetic analyses to address these questions have rarely been conducted for fishes in these environments. This study investigates the population structure of 3 tropical deepwater snappers of the genus Etelis that reside at 100-400 m depth, with broad and overlapping distributions in the Indo-Pacific. Previous studies showed little population structure within the Hawaiian Archipelago for 2 of these species: Etelis coruscans and E. carbunculus. Here we extend sampling to the entire geographic range of each species to resolve the population genetic architecture for these 2 species, as well as a recently exposed cryptic species (Etelis sp.). One goal was to determine whether deepwater snappers are more dispersive than shallow-water fishes. A second goal was to determine whether submesophotic fishes have older, more stable populations than shallow reef denizens that are subject to glacial sea-level fluctuations. Both goals are pertinent to the management of these valuable food fishes. A total of 1153 specimens of E. coruscans from 15 geographic regions were analyzed, along with 1064 specimens of E. carbunculus from 11 regions, and 590 specimens of E. sp. from 16 regions. The first 2 species were analyzed with mtDNA and 9-11 microsatellite loci, while E. sp. was analyzed with mtDNA only. Etelis coruscans had a nonsignificant microsatellite global F ST , but significant global mtDNA Ф ST = 0.010 (P = 0.0007), with the isolation of Seychelles in the western Indian Ocean, and intermittent signals of isolation for the Hawaiian Archipelago. Etelis carbunculus had a non-significant microsatellite global F ST , and significant global mtDNA Ф ST = 0.021 (P = 0.0001), with low but significant levels of isolation for Hawaiʻi, and divergence between Tonga and Fiji. Etelis sp. had mtDNA Ф ST = 0.018 (P = 0.0005), with a strong pattern of isolation for both Seychelles and Tonga. Overall, we observed low population

Marine Ecology Progress Series, Sep 15, 2011

Most coral reef fishes have non-migratory adults and depend on a pelagic larval stage for dispers... more Most coral reef fishes have non-migratory adults and depend on a pelagic larval stage for dispersal. Species with long pelagic larval duration (PLD) can have tremendous dispersal potential and thus display little geographic-genetic differentiation among reef habitats. Restricted adult niche breadth due to habitat specialization can have the opposite effect of fragmenting populations and increasing geographic-genetic differentiation. If long PLD suffices to ensure widespread gene flow among reef populations, we predict similar geographic-genetic homogeneity within species whose adults differ in niche breadth. We tested this hypothesis using a comparative phylogeographic study of 4 sympatric moray eel species that differ in the amount of available habitat within their reported ranges. We generated molecular genetic data for Echidna nebulosa (N = 79) and Gymnomuraena zebra (N = 67) to measure geographic-genetic structure within these species, whose adult habitat is very restricted for moray eels, and compared these results to identical measurements previously published for habitat generalists Gymnothorax undulatus and Gymnothorax flavimarginatus. These 4 species share an ocean-wide distribution with adults occupying the same reefs; however, adults of E. nebulosa and G. zebra are restricted to shallow waters and occupy only 20% of the area occupied by the Gymnothorax species. Mitochondrial (632 bp of cytochrome b and 596 bp of cytochrome oxidase I) genomic sequences revealed high genetic variation (h = 0.995 to 0.998) and low geographic-genetic differentiation (pairwise Φ ST < 0.07 and not significant) for each species across 22 000 km of the Indo-Pacific. Nuclear genomic sequences (420 bp of RAG-1 and 746 bp of RAG-2) demonstrated 16 to 25 haplotypes per marker within each species with minimal geographic-genetic differentiation among populations. This suggests that in cosmopolitan and highly dispersive species such as morays, larval life history can ensure widespread gene flow despite a 5-fold difference in the habitat breadth occupied by adult populations.

Journal of Heredity, Jun 16, 2017

The lionfish is an iconic marine fish, and recently renowned for a disastrous introduction into t... more The lionfish is an iconic marine fish, and recently renowned for a disastrous introduction into the West Atlantic. Genetic surveys of the putative invaders (Pterois volitans and Pterois miles) in their natural Indo-Pacific range can illuminate both topics. Previous research indicated that P. volitans and P. miles are sister species that hybridize in the invasive range, but hybridization in the native range is unknown. Here, we apply mtDNA COI and 2 nuclear introns (S7 RP1 and Gpd2) from 229 lionfish including the 2 invaders and 2 closely-related taxa (44 P. miles, 91 P. volitans, 31 Pterois lunulata, and 63 Pterois russelii) from 10 locations in their native ranges. Genetic data are supplemented with key morphological characters: dorsal, anal, and pectoral fin ray counts. We observed 2 lineages (d = 4.07%, 0.89%, and 2.75% at COI, S7 RP1, and Gpd2, respectively) among the 4 putative species: an Indian Ocean lineage represented by P. miles, and a Pacific Ocean lineage represented by P. lunulata and P. russelii. All specimens of the invasive P. volitans appear to be hybrids between the Indian Ocean P. miles and a Pacific lineage encompassing P. lunulata/russelii, a conclusion supported by both genetics and morphology. The divergences between Indian and Pacific forms are within the range of species-level partitions in fishes, and we recommend retention of the names P. miles and P. russelii for Indian and Pacific forms. The hybrid origin of the Atlantic invasion invokes the possibility of heterosis as a contributing factor to invasion success.

Journal of Biogeography, Oct 20, 2015

Aim Broadly distributed reef fishes tend to have high gene flow mediated by a pelagic larval phas... more Aim Broadly distributed reef fishes tend to have high gene flow mediated by a pelagic larval phase. Here we survey a reef-associated fish distributed across half the tropical oceans, from the Red Sea to the central Pacific. Our goal is to determine whether genetic structure of the broadly distributed Yellowstripe Goatfish (Mulloidichthys flavolineatus) is defined by biogeographic barriers, or smoothed via larval dispersal. Location Red Sea, Indian Ocean, Pacific Ocean Methods Specimens were obtained at 19 locations from the Red Sea to Hawai'i. Genetic data include mtDNA cytochrome b (N = 217) and twelve microsatellite loci (N = 185). Analysis of molecular variance (AMOVA), STRUCTURE, a parsimony network and coalescence analyses were used to resolve recent population history and connectivity. Results Population structure was significant (mtDNA  ST = 0.68, P < 0.001; microsatellite F ST = 0.08, P < 0.001), but mostly driven by samples from the Northwestern (NW) Indian Ocean (including the Red Sea) and Hawai'i. There was little population structure across the Indian Ocean to the central Pacific. Hawai'i was distinguished as a highly isolated population (mtDNA  ST = 0.03 to 0.08, P = N. S.; microsatellite F ST = 0.05 to 0.10, P < 0.001). Specimens from the NW Indian Ocean clustered as a distinct phylogenetic lineage that diverged approximately 493 ka (d =1.7%), which indicates that these fish persisted in isolation through several Pleistocene glacial cycles. Main Conclusion These data reinforce the emerging themes that: 1) phylogeographical breaks within species often coincide with biogeographical breaks based on species distributions and 2) populations on the periphery of the range (NW Indian Ocean and Hawai'i) are isolated and these areas may be evolutionary incubators.

Conservation Biology, Feb 1, 1999

The alligator snapping turtle (Macroclemys temminckii) is a long-lived, slow-growing chelydrid tu... more The alligator snapping turtle (Macroclemys temminckii) is a long-lived, slow-growing chelydrid turtle found in Gulf of Mexico drainages from Florida to Texas (U.S.A.). Populations are thought to be depleted throughout the range due in part to an increased harvest in the 1960s through 1980s. To identify population and evolutionary units, 420 base pairs were sequenced within the mitochondrial DNA control region of 158 specimens from 12 drainages. Results indicate substantial phylogeographic structuring and strong population-level separations among river drainages. Eight of 11 haplotypes were observed to be river-specific, providing diagnostic markers for most drainages. Three partitions are resolved in the mtDNA genealogy, corresponding to the eastern, central, and western portion of the species' range. These separations coincide with recognized biogeographic provinces. The population structure by river system indicates that many drainages are distinct management units, with the Suwannee River lineage possibly deserving special attention, based on the criterion of genetic distinctiveness. The partitioning of M. temminckii into river-specific populations illustrates the management framework and conservation challenges that apply to a broad array of riverine species. Drainage-specific molecular markers may be used to identify the geographic origin of turtle products in the marketplace.

Coral Reefs, Jun 15, 2022

Frontiers in Marine Science, Jun 18, 2019

Research on so-called "minor taxa" at mesophotic depths has lagged behind that of more commonly r... more Research on so-called "minor taxa" at mesophotic depths has lagged behind that of more commonly researched groups such as fish or hard corals. Exemplar taxa include species of the order Zoantharia, benthic colonial anemones that are cosmopolitan in distribution but understudied in many ecoregion and ecosystems. In this study, we examine the results of rare mesophotic to deep sea surveys (one rebreather, one remotely operated submersible (ROV) + net survey, two ROV surveys) from Japan and Israel. We examined the collected images and video data to provide a first estimate of Zoantharia diversity at mesophotic depths. Zoantharians were observed in all surveys, indicating their ubiquitous presence in mesophotic and deeper ecosystems. Additionally, specimens (n = 12) acquired via these surveys were phylogenetically analyzed with three DNA markers. Phylogenetic results showed the presence of undescribed species based on the uniqueness of acquired DNA sequences, including one specimen belonging to the family Abyssoanthidae, previously only reported from depths below 2000 m. Other specimens belong to groups that inhabit shallower and deeper depths (Antipathozoanthus, Epizoanthus, and Parazoanthidae). These results depart from surveys of mesophotic coral ecosystem fishes and crustaceans, which indicate affiliations almost exclusively with shallow genera and families. We hypothesize that mesophotic depths are an ecotone for zoantharian diversity, with links to both deeper and shallower ecosystem diversity. Future surveys in mesophotic depths should incorporate phylogenetic methods to better catalog so-called "minor taxa" (not only including Zoantharia) and enhance the scientific foundation for conserving the biodiversity of these threatened ecosystems.

Molecular Phylogenetics and Evolution, Nov 1, 2010

This article appeared in a journal published by Elsevier. The attached copy is furnished to the a... more This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier's archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright

Journal of Heredity, 2012

Marine biogeographic barriers can have unpredictable consequences, even among closely related spe... more Marine biogeographic barriers can have unpredictable consequences, even among closely related species. To resolve phylogeographic patterns for Indo-Pacific reef fauna, we conducted range-wide surveys of sister species, the scrawled butterflyfish (Chaetodon meyeri; N = 134) and the ornate butterflyfish (Chaetodon ornatissimus; N = 296), using mitochondrial DNA cytochrome b sequences and 10 microsatellite loci. The former is distributed primarily in the Indian Ocean but also extends to the Line Islands in the Central Pacific, whereas the latter is distributed primarily in the Central-West Pacific (including Hawaii and French Polynesia) but extends to the eastern margin of the Indian Ocean. Analyses of molecular variance and Bayesian STRUCTURE results revealed 1 range-wide group for C. meyeri and 3 groups for C. ornatissimus: 1) eastern Indian Ocean and western Pacific, 2) Central Pacific, and 3) Hawaii. Estimates of the last population expansion were much more recent for C. meyeri (61 500 to 95 000 years) versus C. ornatissimus (184 700 to 286 300 years). Despite similarities in ecology, morphology, life history, and a broadly overlapping distribution, these sister species have divergent patterns of dispersal and corresponding evolutionary history. The mtDNA and microsatellite markers did not provide concordant results within 1 of our study species (C. meyeri), or in 7 out of 12 other cases of marine fishes in the published literature. This discordance renews caution in relying on one or a few markers for reconstructing historical demography.

Journal of Fish Biology, Aug 5, 2019

This article has been accepted for publication in the Journal of Fish Biology and undergone full ... more This article has been accepted for publication in the Journal of Fish Biology and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Conservation Genetics Resources, Nov 1, 2009

Journal of Biogeography, 2020

AimSpecies ranges provide a valuable foundation for resolving biogeographical regions, evolutiona... more AimSpecies ranges provide a valuable foundation for resolving biogeographical regions, evolutionary processes and extinction risks. To inform conservation priorities, here we develop the first bioregionalization based on reef fish abundance of the Hawaiian Archipelago, which spans nearly 10° of latitude across 2,400 km, including 8 high volcanic islands in the populated main Hawaiian Islands (MHI), and 10 low islands (atolls, shoals and islets) in the remote northwestern Hawaiian Islands (NWHI).LocationThe Hawaiian Archipelago.TaxonFishes (276 taxa).MethodsWe compiled 5,316 visual fish surveys at depths of 1–30 m from throughout the Hawaiian Archipelago. Geographical range (km2) for each species was measured as extent of occurrence (EOO) and area of occurrence (AOO). PERMANOVA and PCO were used to investigate drivers of fish assemblage structure. Distance‐based multivariate analyses were used to evaluate the relationship between fish assemblage structure and predictor variables incl...