Publications by authors named "Kevin A Feldheim"

49 Publications

Phylogeography and population genetics of the cryptic bonnethead shark Sphyrna aff. tiburo in Brazil and the Caribbean inferred from mtDNA markers.

J Fish Biol 2021 Dec 22;99(6):1899-1911. Epub 2021 Oct 22.

Predator Ecology and Conservation Lab, Biological Sciences Department, Florida International University, Miami, Florida, 33181, USA.

Resolving the identity, phylogeny and distribution of cryptic species within species complexes is an essential precursor to management. The bonnethead shark, Sphyrna tiburo, is a small coastal shark distributed in the Western Atlantic from North Carolina (U.S.A.) to southern Brazil. Genetic analyses based on mitochondrial markers revealed that bonnethead sharks comprise a species complex with at least two lineages in the Northwestern Atlantic and the Caribbean (S. tiburo and Sphyrna aff. tiburo, respectively). The phylogeographic and phylogenetic analysis of two mitochondrial markers [control region (mtCR) and cytochrome oxidase I (COI)] showed that bonnethead sharks from southeastern Brazil correspond to S. aff. tiburo, extending the distribution of this cryptic species >5000 km. Bonnethead shark populations are only managed in the U.S.A. and in the 2000s were considered to be regionally extinct or collapsed in southeast Brazil. The results indicate that there is significant genetic differentiation between S. aff. tiburo from Brazil and other populations from the Caribbean (Φ  = 0.9053, P < 0.000), which means that collapsed populations in the former are unlikely to be replenished from Caribbean immigration. The species identity of bonnethead sharks in the Southwest Atlantic and their relationship to North Atlantic and Caribbean populations still remains unresolved. Taxonomic revision and further sampling are required to reevaluate the status of the bonnethead shark complex through its distribution range.
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http://dx.doi.org/10.1111/jfb.14896DOI Listing
December 2021

Artificial insemination and parthenogenesis in the whitespotted bamboo shark Chiloscyllium plagiosum.

Sci Rep 2021 05 13;11(1):9966. Epub 2021 May 13.

South-East Zoo Alliance for Reproduction & Conservation, Yulee, FL, 32097, USA.

Non-lethal methods for semen collection from elasmobranchs to better understand species reproduction has accompanied the development of artificial insemination. Ejaculates (n = 82) collected from whitespotted bamboo sharks Chiloscyllium plagiosum (n = 19) were assessed and cold-stored raw or extended at 4 °C. Females (n = 20) were inseminated with fresh or 24-48 h cold-stored raw or extended semen and paternity of offspring determined with microsatellite markers. Insemination of females with fresh semen (n = 10) resulted in 80 hatchlings and 27.6% fertility. Insemination of females with semen cold-stored 24 h (n = 4) and 48 h (n = 1) semen resulted in 17 hatchlings and fertilization rates of 28.1% and 7.1% respectively. Two females inseminated with fresh or cold-stored semen laid eggs that hatched from fertilization and parthenogenesis within the same clutch. Parthenogenesis rate for inseminated females was 0.71%. Results demonstrate artificial insemination with cold-stored semen can provide a strategy for transport of male genetics nationally and internationally, precluding the need to transport sharks. Production of parthenotes in the same clutch as sexually fertilized eggs highlights the prevalence of parthenogenesis in whitespotted bamboo sharks and poses important considerations for population management.
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http://dx.doi.org/10.1038/s41598-021-88568-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8116330PMC
May 2021

Annual breeding in a captive smalltooth sawfish, Pristis pectinata.

J Fish Biol 2020 Nov 16;97(5):1586-1589. Epub 2020 Sep 16.

Pritzker Laboratory for Molecular Systematics and Evolution, Field Museum, Chicago, Illinois, USA.

The critically endangered smalltooth sawfish Pristis pectinata reproduces biennially in central west Florida, U.S.A. Here we demonstrate that smalltooth sawfish are physiologically capable of reproducing annually in a captive environment. The smalltooth sawfish are held in an open system, with abiotic conditions that vary naturally with the surrounding environment in The Bahamas. This suggests wild smalltooth sawfish may also be capable of annual reproduction provided there are adequate prey resources, limited competition and mate availability.
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http://dx.doi.org/10.1111/jfb.14523DOI Listing
November 2020

Species composition of the largest shark fin retail-market in mainland China.

Sci Rep 2020 07 31;10(1):12914. Epub 2020 Jul 31.

Department of Biological Sciences, Florida International University, 3000 NE 151st Street, North Miami, FL, 33181, USA.

Species-specific monitoring through large shark fin market surveys has been a valuable data source to estimate global catches and international shark fin trade dynamics. Hong Kong and Guangzhou, mainland China, are the largest shark fin markets and consumption centers in the world. We used molecular identification protocols on randomly collected processed fin trimmings (n = 2000) and non-parametric species estimators to investigate the species composition of the Guangzhou retail market and compare the species diversity between the Guangzhou and Hong Kong shark fin retail markets. Species diversity was similar between both trade hubs with a small subset of species dominating the composition. The blue shark (Prionace glauca) was the most common species overall followed by the CITES-listed silky shark (Carcharhinus falciformis), scalloped hammerhead shark (Sphyrna lewini), smooth hammerhead shark (S. zygaena) and shortfin mako shark (Isurus oxyrinchus). Our results support previous indications of high connectivity between the shark fin markets of Hong Kong and mainland China and suggest that systematic studies of other fin trade hubs within Mainland China and stronger law-enforcement protocols and capacity building are needed.
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http://dx.doi.org/10.1038/s41598-020-69555-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7395743PMC
July 2020

Metagenomic 16S rDNA amplicon data on bacterial diversity profiling and its predicted metabolic functions of varillales in Allpahuayo-Mishana National Reserve.

Data Brief 2020 Jun 28;30:105625. Epub 2020 Apr 28.

Unidad Especializada de Biotecnología, Centro de Investigación de Recursos Naturales de la Amazonía (CIRNA), Universidad Nacional de la Amazonia Peruana (UNAP), Iquitos, Perú.

The white-sands forests or varillales of the Peruvian Amazon are characterized by their distinct physical characteristics, patchy distribution, and endemism [1, 2]. Much research has been conducted on the specialized plant and animal communities that inhabit these ecosystems, yet their soil microbiomes have yet to be studied. Here we provide metagenomic 16S rDNA amplicon data of soil microbiomes from three types of varillales in Allpahuayo-Mishana National Reserve near Iquitos, Peru. Composite soil samples were collected from very low varillal, high-dry varillal, and high-wet varillal. Purified metagenomic DNA was used to prepare and sequence 16S rDNA metagenomic libraries on the Illumina MiqSeq platform. Raw paired-endsequences were analyzed using the Metagenomics RAST server (MG-RAST) and Parallel-Meta3 software and revealed the existence of a high percentage of undiscovered sequences, potentially indicating specialized bacterial communities in these forests. Also, were predicted several metabolic functions in this dataset. The raw sequence data in fastq format is available in the public repository Discover Mendeley Data (https://data.mendeley.com/datasets/syktzxcnp6/2). Also, is available at NCBI's Sequence Read Archive (SRA) with accession numbers SRX7891206 (very low varillal), SRX7891207 (high-dry varillal), and SRX7891208 (high-wet varillal).
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http://dx.doi.org/10.1016/j.dib.2020.105625DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7201190PMC
June 2020

Microsatellite primer development in elasmobranchs using next generation sequencing of enriched libraries.

Mol Biol Rep 2020 Apr 4;47(4):2669-2675. Epub 2020 Mar 4.

Pritzker Laboratory for Molecular Systematics and Evolution, Field Museum of Natural History, 1400 South Lake Shore Dr., Chicago, IL, 60605, USA.

Microsatellites are useful in studies of population genetics, sibship, and parentage. Here, we screened for microsatellites from multiple elasmobranch genomic libraries using an enrichment protocol followed by sequencing on an Illumina platform. We concurrently screened five and then nine genomes and describe the number of potential loci from each respective round of sequencing. To validate the efficacy of the protocol, we developed and tested primers for the pelagic thresher shark, Alopias pelagicus. The method described here is a cost-effective protocol to increase the pool of potential useful loci and allows the concurrent screening of multiple libraries.
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http://dx.doi.org/10.1007/s11033-020-05357-yDOI Listing
April 2020

No apparent negative tagging effects after 13 years at liberty for lemon shark, Negaprion brevirostris implanted with acoustic transmitter.

J Fish Biol 2019 Jan 11;94(1):173-177. Epub 2018 Dec 11.

Bimini Biological Field Station Foundation, Bimini, Bahamas.

An intact and uncompromised internal acoustic transmitter was non-lethally recovered from a lemon shark Negaprion brevirostris, after 13 years at liberty. The shark, first tagged at an estimated age of 2 years old near South Bimini, Bahamas in 2004, was recaptured in 2017 with a total length of 264 cm. The tagged shark displayed typical growth rate, pregnancy, natal homing and pupping behaviour of other individuals in this population. This observation provides important evidence regarding the effects from long-term retention of implanted acoustic transmitters in a carcharhinid shark.
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http://dx.doi.org/10.1111/jfb.13856DOI Listing
January 2019

Species composition of the international shark fin trade assessed through a retail-market survey in Hong Kong.

Conserv Biol 2018 04 15;32(2):376-389. Epub 2017 Dec 15.

Stony Brook University, Stony Brook, NY 11794, U.S.A.

The shark fin trade is a major driver of shark exploitation in fisheries all over the world, most of which are not managed on a species-specific basis. Species-specific trade information highlights taxa of particular concern and can be used to assess the efficacy of management measures and anticipate emerging threats. The species composition of the Hong Kong Special Administrative Region of China, one of the world's largest fin trading hubs, was partially assessed in 1999-2001. We randomly selected and genetically identified fin trimmings (n = 4800), produced during fin processing, from the retail market of Hong Kong in 2014-2015 to assess contemporary species composition of the fin trade. We used nonparametric species estimators to determine that at least 76 species of sharks, batoids, and chimaeras supplied the fin trade and a Bayesian model to determine their relative proportion in the market. The diversity of traded species suggests species substitution could mask depletion of vulnerable species; one-third of identified species are threatened with extinction. The Bayesian model suggested that 8 species each comprised >1% of the fin trimmings (34.1-64.2% for blue [Prionace glauca], 0.2-1.2% for bull [Carcharhinus leucas] and shortfin mako [Isurus oxyrinchus]); thus, trade was skewed to a few globally distributed species. Several other coastal sharks, batoids, and chimaeras are in the trade but poorly managed. Fewer than 10 of the species we modeled have sustainably managed fisheries anywhere in their range, and the most common species in trade, the blue shark, was not among them. Our study and approach serve as a baseline to track changes in composition of species in the fin trade over time to better understand patterns of exploitation and assess the effects of emerging management actions for these animals.
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http://dx.doi.org/10.1111/cobi.13043DOI Listing
April 2018

Risky business for a juvenile marine predator? Testing the influence of foraging strategies on size and growth rate under natural conditions.

Proc Biol Sci 2017 Apr;284(1852)

Institute for Ocean Conservation Science/School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, USA.

Mechanisms driving selection of body size and growth rate in wild marine vertebrates are poorly understood, thus limiting knowledge of their fitness costs at ecological, physiological and genetic scales. Here, we indirectly tested whether selection for size-related traits of juvenile sharks that inhabit a nursery hosting two dichotomous habitats, protected mangroves (low predation risk) and exposed seagrass beds (high predation risk), is influenced by their foraging behaviour. Juvenile sharks displayed a continuum of foraging strategies between mangrove and seagrass areas, with some individuals preferentially feeding in one habitat over another. Foraging habitat was correlated with growth rate, whereby slower growing, smaller individuals fed predominantly in sheltered mangroves, whereas larger, faster growing animals fed over exposed seagrass. Concomitantly, tracked juveniles undertook variable movement behaviours across both the low and high predation risk habitat. These data provide supporting evidence for the hypothesis that directional selection favouring smaller size and slower growth rate, both heritable traits in this shark population, may be driven by variability in foraging behaviour and predation risk. Such evolutionary pathways may be critical to adaptation within predator-driven marine ecosystems.
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http://dx.doi.org/10.1098/rspb.2017.0166DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5394670PMC
April 2017

Global population genetic dynamics of a highly migratory, apex predator shark.

Mol Ecol 2016 11 18;25(21):5312-5329. Epub 2016 Oct 18.

Save Our Seas Shark Research Center and Guy Harvey Research Institute, Halmos College of Natural Sciences & Oceanography, Nova Southeastern University, 8000 N. Ocean Drive, Dania Beach, FL, 33004, USA.

Knowledge of genetic connectivity dynamics in the world's large-bodied, highly migratory, apex predator sharks across their global ranges is limited. One such species, the tiger shark (Galeocerdo cuvier), occurs worldwide in warm temperate and tropical waters, uses remarkably diverse habitats (nearshore to pelagic) and possesses a generalist diet that can structure marine ecosystems through top-down processes. We investigated the phylogeography and the global population structure of this exploited, phylogenetically enigmatic shark by using 10 nuclear microsatellites (n = 380) and sequences from the mitochondrial control region (CR, n = 340) and cytochrome oxidase I gene (n = 100). All three marker classes showed the genetic differentiation between tiger sharks from the western Atlantic and Indo-Pacific ocean basins (microsatellite F  > 0.129; CR Φ  > 0.497), the presence of North vs. southwestern Atlantic differentiation and the isolation of tiger sharks sampled from Hawaii from other surveyed locations. Furthermore, mitochondrial DNA revealed high levels of intraocean basin matrilineal population structure, suggesting female philopatry and sex-biased gene flow. Coalescent- and genetic distance-based estimates of divergence from CR sequences were largely congruent (d  = 0.0015-0.0050), indicating a separation of Indo-Pacific and western Atlantic tiger sharks <1 million years ago. Mitochondrial haplotype relationships suggested that the western South Atlantic Ocean was likely a historical connection for interocean basin linkages via the dispersal around South Africa. Together, the results reveal unexpectedly high levels of population structure in a highly migratory, behaviourally generalist, cosmopolitan ocean predator, calling for management and conservation on smaller-than-anticipated spatial scales.
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http://dx.doi.org/10.1111/mec.13845DOI Listing
November 2016

Surgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes.

Mol Phylogenet Evol 2016 08 30;101:203-215. Epub 2016 Apr 30.

Hawai'i Institute of Marine Biology, Kāne'ohe, HI 96744, USA.

Closely related species can provide valuable insights into evolutionary processes through comparison of their ecology, geographic distribution and the history recorded in their genomes. In the Indo-Pacific, many reef fishes are divided into sister species that come into secondary contact at biogeographic borders, most prominently where Indian Ocean and Pacific Ocean faunas meet. It is unclear whether hybridization in this contact zone represents incomplete speciation, secondary contact, an evolutionary dead-end (for hybrids) or some combination of the above. To address these issues, we conducted comprehensive surveys of two widely-distributed surgeonfish species, Acanthurus leucosternon (N=141) and A. nigricans (N=412), with mtDNA cytochrome b sequences and ten microsatellite loci. These surgeonfishes are found primarily in the Indian and Pacific Oceans, respectively, but overlap at the Christmas and Cocos-Keeling Islands hybrid zone in the eastern Indian Ocean. We also sampled the two other Pacific members of this species complex, A. achilles (N=54) and A. japonicus (N=49), which are known to hybridize with A. nigricans where their ranges overlap. Our results indicate separation between the four species that range from the recent Pleistocene to late Pliocene (235,000-2.25million years ago). The Pacific A. achilles is the most divergent (and possibly ancestral) species with mtDNA dcorr≈0.04, whereas the other two Pacific species (A. japonicus and A. nigricans) are distinguishable only at a population or subspecies level (ΦST=0.6533, P<0.001). Little population structure was observed within species, with evidence of recent population expansion across all four geographic ranges. We detected sharing of mtDNA haplotypes between species and extensive hybridization based on microsatellites, consistent with later generation hybrids but also the effects of allele homoplasy. Despite extensive introgression, 98% of specimens had concordance between mtDNA lineage and species identification based on external morphology, indicating that species integrity may not be eroding. The A. nigricans complex demonstrates a range of outcomes from incomplete speciation to secondary contact to decreasing hybridization with increasing evolutionary depth.
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http://dx.doi.org/10.1016/j.ympev.2016.04.036DOI Listing
August 2016

Facultative parthenogenesis in a critically endangered wild vertebrate.

Curr Biol 2015 Jun;25(11):R446-7

School of Marine and Atmospheric Science, Stony Brook University, Stony Brook, NY 11794, USA. Electronic address:

Facultative parthenogenesis - the ability of sexually reproducing species to sometimes produce offspring asexually - is known from a wide range of ordinarily sexually reproducing vertebrates in captivity, including some birds, reptiles and sharks [1-3]. Despite this, free-living parthenogens have never been observed in any of these taxa in the wild, although two free-living snakes were recently discovered each gestating a single parthenogen - one copperhead (Agkistrodon contortrix) and one cottonmouth (Agkistrodon piscivorus) [1]. Vertebrate parthenogens are characterized as being of the homogametic sex (e.g., females in sharks, males in birds) and by having elevated homozygosity compared to their mother [1-3], which may reduce their viability [4]. Although it is unknown if either of the parthenogenetic snakes would have been carried to term or survived in the wild, facultative parthenogenesis might have adaptive significance [1]. If this is true, it is reasonable to hypothesize that parthenogenesis would be found most often at low population density, when females risk reproductive failure because finding mates is difficult [5]. Here, we document the first examples of viable parthenogens living in a normally sexually reproducing wild vertebrate, the smalltooth sawfish (Pristis pectinata). We also provide a simple approach to screen any microsatellite DNA database for parthenogens, which will enable hypothesis-driven research on the significance of vertebrate parthenogenesis in the wild.
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http://dx.doi.org/10.1016/j.cub.2015.04.018DOI Listing
June 2015

Isolation and development of microsatellite loci in an African Woodpecker (Campethera nivosa) using polymerase chain reaction and DNA sequencing.

BMC Res Notes 2015 May 30;8:201. Epub 2015 May 30.

Department of Biological and Chemical Sciences, Roosevelt University, 430S Michigan Ave, Chicago, USA.

Background: The Buff-spotted Woodpecker (Campethera nivosa) is a resident bird species that is distributed in lowland rainforest habitats from western to eastern Africa. We developed species-specific microsatellite markers to examine the population genetics of this species.

Findings: Twenty-one microsatellite loci were isolated from C. nivosa. Of these, 15 were found to amplify consistently. These loci were then tested for variability in 15 individuals from different lowland forest localities. The number of alleles ranged from 3 to 13 per locus, with observed and expected heterozygosity ranging from 0.100 to 0.917 and 0.485 to 0.901, respectively. Four loci exhibited significant heterozygote deficiency while one had an excess of heterozygotes. None of the loci exhibited linkage disequilibrium.

Conclusion: These polymorphic microsatellite markers will be used to study genetic variability in populations of C. nivosa across either sides of the Congo River to evaluate the effect of the river as a barrier to gene flow.
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http://dx.doi.org/10.1186/s13104-015-1165-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4449581PMC
May 2015

A quantitative genetic approach to assess the evolutionary potential of a coastal marine fish to ocean acidification.

Evol Appl 2015 Apr 13;8(4):352-62. Epub 2015 Feb 13.

Department of Marine Sciences, University of Connecticut Groton, CT, USA.

Assessing the potential of marine organisms to adapt genetically to increasing oceanic CO2 levels requires proxies such as heritability of fitness-related traits under ocean acidification (OA). We applied a quantitative genetic method to derive the first heritability estimate of survival under elevated CO2 conditions in a metazoan. Specifically, we reared offspring, selected from a wild coastal fish population (Atlantic silverside, Menidia menidia), at high CO2 conditions (∼2300 μatm) from fertilization to 15 days posthatch, which significantly reduced survival compared to controls. Perished and surviving offspring were quantitatively sampled and genotyped along with their parents, using eight polymorphic microsatellite loci, to reconstruct a parent-offspring pedigree and estimate variance components. Genetically related individuals were phenotypically more similar (i.e., survived similarly long at elevated CO2 conditions) than unrelated individuals, which translated into a significantly nonzero heritability (0.20 ± 0.07). The contribution of maternal effects was surprisingly small (0.05 ± 0.04) and nonsignificant. Survival among replicates was positively correlated with genetic diversity, particularly with observed heterozygosity. We conclude that early life survival of M. menidia under high CO2 levels has a significant additive genetic component that could elicit an evolutionary response to OA, depending on the strength and direction of future selection.
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http://dx.doi.org/10.1111/eva.12248DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4408146PMC
April 2015

Genetic Diversity of White Sharks, Carcharodon carcharias, in the Northwest Atlantic and Southern Africa.

J Hered 2015 May-Jun;106(3):258-65. Epub 2015 Mar 10.

From the School of Marine and Atmospheric Science, Stony Brook University, Stony Brook, NY 11394 (O'Leary, Fields, and Chapman); the Pritzker Laboratory for Molecular Systematics and Evolution, The Field Museum, Chicago, IL 60605 (Feldheim); the National Marine Fisheries Service, Apex Predators Program, Narragansett, RI 02882 (Natanson); the KwaZulu-Natal Sharks Board and Biomedical Resource Unit, University of KwaZulu-Natal, Durban 4000, South Africa (Wintner); the Great Lakes Institute for Environmental Research University of Windsor, Windsor, Ontario N9B3P4, Canada (Hussey); the Save our Seas Shark Center and Guy Harvey Research Institute, Nova Southeastern University, FL 33004 (Shivji); and the Institute of Ocean Conservation Science, Stony Brook, NY 11794 (Chapman).

The white shark, Carcharodon carcharias, is both one of the largest apex predators in the world and among the most heavily protected marine fish. Population genetic diversity is in part shaped by recent demographic history and can thus provide information complementary to more traditional population assessments, which are difficult to obtain for white sharks and have at times been controversial. Here, we use the mitochondrial control region and 14 nuclear-encoded microsatellite loci to assess white shark genetic diversity in 2 regions: the Northwest Atlantic (NWA, N = 35) and southern Africa (SA, N = 131). We find that these 2 regions harbor genetically distinct white shark populations (Φ ST = 0.10, P < 0.00001; microsatellite F ST = 0.1057, P < 0.021). M-ratios were low and indicative of a genetic bottleneck in the NWA (M-ratio = 0.71, P < 0.004) but not SA (M-ratio = 0.85, P = 0.39). This is consistent with other evidence showing a steep population decline occurring in the mid to late 20th century in the NWA, whereas the SA population appears to have been relatively stable. Estimates of effective population size ranged from 22.6 to 66.3 (NWA) and 188 to 1998.3 (SA) and evidence of inbreeding was found (primarily in NWA). Overall, our findings indicate that white population dynamics within NWA and SA are determined more by intrinsic reproduction than immigration and there is genetic evidence of a population decline in the NWA, further justifying the strong domestic protective measures that have been taken for this species in this region. Our study also highlights how assessment of genetic diversity can complement other sources of information to better understand the status of threatened marine fish populations.
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http://dx.doi.org/10.1093/jhered/esv001DOI Listing
August 2015

Population structure and dispersal of the coral-excavating sponge Cliona delitrix.

Mol Ecol 2015 Apr 20;24(7):1447-66. Epub 2015 Mar 20.

Nova Southeastern University, Oceanographic Center, 8000 North Ocean Drive, Dania Beach, FL, 33004, USA.

Some excavating sponges of the genus Cliona compete with live reef corals, often killing and bioeroding entire colonies. Important aspects affecting distribution of these species, such as dispersal capability and population structure, remain largely unknown. Thus, the aim of this study was to determine levels of genetic connectivity and dispersal of Cliona delitrix across the Greater Caribbean (Caribbean Sea, Bahamas and Florida), to understand current patterns and possible future trends in their distribution and effects on coral reefs. Using ten species-specific microsatellite markers, we found high levels of genetic differentiation between six genetically distinct populations: one in the Atlantic (Florida-Bahamas), one specific to Florida and four in the South Caribbean Sea. In Florida, two independent breeding populations are likely separated by depth. Gene flow and ecological dispersal occur among other populations in the Florida reef tract, and between some Florida locations and the Bahamas. Similarly, gene flow occurs between populations in the South Caribbean Sea, but appears restricted between the Caribbean Sea and the Atlantic (Florida-Bahamas). Dispersal of C. delitrix was farther than expected for a marine sponge and favoured in areas where currents are strong enough to transport sponge eggs or larvae over longer distances. Our results support the influence of ocean current patterns on genetic connectivity, and constitute a baseline to monitor future C. delitrix trends under climate change.
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http://dx.doi.org/10.1111/mec.13134DOI Listing
April 2015

Comparative population genetics and evolutionary history of two commonly misidentified billfishes of management and conservation concern.

BMC Genet 2014 Dec 14;15:141. Epub 2014 Dec 14.

The Field Museum of Natural History, Pritzker Laboratory for Molecular Systematics and Evolution, 1400 South Lake Shore Drive, Chicago, IL, 60605, USA.

Background: Misidentifications between exploited species may lead to inaccuracies in population assessments, with potentially irreversible conservation ramifications if overexploitation of either species is occurring. A notable showcase is provided by the realization that the roundscale spearfish (Tetrapturus georgii), a recently validated species, has been historically misidentified as the morphologically very similar and severely overfished white marlin (Kajikia albida) (IUCN listing: Vulnerable). In effect, no information exists on the population status and evolutionary history of the enigmatic roundscale spearfish, a large, highly vagile and broadly distributed pelagic species. We provide the first population genetic evaluation of the roundscale spearfish, utilizing nuclear microsatellite and mitochondrial DNA sequence markers. Furthermore, we re-evaluated existing white marlin mitochondrial genetic data and present our findings in a comparative context to the roundscale spearfish.

Results: Microsatellite and mitochondrial (control region) DNA markers provided mixed evidence for roundscale spearfish population differentiation between the western north and south Atlantic regions, depending on marker-statistical analysis combination used. Mitochondrial DNA analyses provided strong signals of historical population growth for both white marlin and roundscale spearfish, but higher genetic diversity and effective female population size (1.5-1.9X) for white marlin.

Conclusions: The equivocal indications of roundscale spearfish population structure, combined with a smaller effective female population size compared to the white marlin, already a species of concern, suggests that a species-specific and precautionary management strategy recognizing two management units is prudent for this newly validated billfish.
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http://dx.doi.org/10.1186/s12863-014-0141-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4278234PMC
December 2014

Validation of microsatellite multiplexes for parentage analysis and species discrimination in two hybridizing species of coral reef fish (Plectropomus spp., Serranidae).

Ecol Evol 2014 Jun 24;4(11):2046-57. Epub 2014 Apr 24.

Red Sea Research Center, King Abdullah University of Science and Technology 23955-6900, Thuwal, Saudi Arabia.

Microsatellites are often considered ideal markers to investigate ecological processes in animal populations. They are regularly used as genetic barcodes to identify species, individuals, and infer familial relationships. However, such applications are highly sensitive the number and diversity of microsatellite markers, which are also prone to error. Here, we propose a novel framework to assess the suitability of microsatellite datasets for parentage analysis and species discrimination in two closely related species of coral reef fish, Plectropomus leopardus and P. maculatus (Serranidae). Coral trout are important fisheries species throughout the Indo-Pacific region and have been shown to hybridize in parts of the Great Barrier Reef, Australia. We first describe the development of 25 microsatellite loci and their integration to three multiplex PCRs that co-amplify in both species. Using simulations, we demonstrate that the complete suite of markers provides appropriate power to discriminate between species, detect hybrid individuals, and resolve parent-offspring relationships in natural populations, with over 99.6% accuracy in parent-offspring assignments. The markers were also tested on seven additional species within the Plectropomus genus with polymorphism in 28-96% of loci. The multiplex PCRs developed here provide a reliable and cost-effective strategy to investigate evolutionary and ecological dynamics and will be broadly applicable in studies of wild populations and aquaculture brood stocks for these closely related fish species.
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http://dx.doi.org/10.1002/ece3.1002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4201420PMC
June 2014

There and back again: a review of residency and return migrations in sharks, with implications for population structure and management.

Ann Rev Mar Sci 2015 18;7:547-70. Epub 2014 Sep 18.

Institute for Ocean Conservation Science and School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York 11794-5000; email:

The overexploitation of sharks has become a global environmental issue in need of a comprehensive and multifaceted management response. Tracking studies are beginning to elucidate how shark movements shape the internal dynamics and structure of populations, which determine the most appropriate scale of these management efforts. Tracked sharks frequently either remain in a restricted geographic area for an extended period of time (residency) or return to a previously resided-in area after making long-distance movements (site fidelity). Genetic studies have shown that some individuals of certain species preferentially return to their exact birthplaces (natal philopatry) or birth regions (regional philopatry) for either parturition or mating, even though they make long-distance movements that would allow them to breed elsewhere. More than 80 peer-reviewed articles, constituting the majority of published shark tracking and population genetic studies, provide evidence of at least one of these behaviors in a combined 31 shark species from six of the eight extant orders. Residency, site fidelity, and philopatry can alone or in combination structure many coastal shark populations on finer geographic scales than expected based on their potential for dispersal. This information should therefore be used to scale and inform assessment, management, and conservation activities intended to restore depleted shark populations.
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http://dx.doi.org/10.1146/annurev-marine-010814-015730DOI Listing
July 2016

Two decades of genetic profiling yields first evidence of natal philopatry and long-term fidelity to parturition sites in sharks.

Mol Ecol 2014 Jan 9;23(1):110-7. Epub 2013 Dec 9.

Pritzker Laboratory for Molecular Systematics and Evolution, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL, 60605, USA.

Sharks are a globally threatened group of marine fishes that often breed in their natal region of origin. There has even been speculation that female sharks return to their exact birthplace to breed ('natal philopatry'), which would have important conservation implications. Genetic profiling of lemon sharks (Negaprion brevirostris) from 20 consecutive cohorts (1993-2012) at Bimini, Bahamas, showed that certain females faithfully gave birth at this site for nearly two decades. At least six females born in the 1993-1997 cohorts returned to give birth 14-17 years later, providing the first direct evidence of natal philopatry in the chondrichthyans. Long-term fidelity to specific nursery sites coupled with natal philopatry highlights the merits of emerging spatial and local conservation efforts for these threatened predators.
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http://dx.doi.org/10.1111/mec.12583DOI Listing
January 2014

Vectored dispersal of Symbiodinium by larvae of a Caribbean gorgonian octocoral.

Mol Ecol 2013 Sep;22(17):4413-32

Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbaker Causeway, Miami, FL 33149, USA.

The ability of coral reefs to recover from natural and anthropogenic disturbance is difficult to predict, in part due to uncertainty regarding the dispersal capabilities and connectivity of their reef inhabitants. We developed microsatellite markers for the broadcast spawning gorgonian octocoral Eunicea (Plexaura) flexuosa (four markers) and its dinoflagellate symbiont, Symbiodinium B1 (five markers), and used them to assess genetic connectivity, specificity and directionality of gene flow among sites in Florida, Panama, Saba and the Dominican Republic. Bayesian analyses found that most E. flexuosa from the Florida reef tract, Saba and the Dominican Republic were strongly differentiated from many E. flexuosa in Panama, with the exception of five colonies from Key West that clustered with colonies from Panama. In contrast, Symbiodinium B1 was more highly structured. At least seven populations were detected that showed patterns of isolation by distance. The symbionts in the five unusual Key West colonies also clustered with symbionts from Panama, suggesting these colonies are the result of long-distance dispersal. Migration rate tests indicated a weak signal of northward immigration from the Panama population into the lower Florida Keys. As E. flexuosa clonemates only rarely associated with the same Symbiodinium B1 genotype (and vice versa), these data suggest a dynamic host-symbiont relationship in which E. flexuosa is relatively well dispersed but likely acquires Symbiodinium B1 from highly structured natal areas prior to dispersal. Once vectored by host larvae, these symbionts may then spread through the local population, and/or host colonies may acquire different local symbiont genotypes over time.
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http://dx.doi.org/10.1111/mec.12405DOI Listing
September 2013

Severe inbreeding and small effective number of breeders in a formerly abundant marine fish.

PLoS One 2013 7;8(6):e66126. Epub 2013 Jun 7.

School of Marine and Atmospheric Science, Stony Brook University, Stony Brook, New York, United States of America.

In contrast to freshwater fish it is presumed that marine fish are unlikely to spawn with close relatives due to the dilution effect of large breeding populations and their propensity for movement and reproductive mixing. Inbreeding is therefore not typically a focal concern of marine fish management. We measured the effective number of breeders in 6 New York estuaries for winter flounder (Pseudopleuronectes americanus), a formerly abundant fish, using 11 microsatellite markers (6-56 alleles per locus). The effective number of breeders for 1-2 years was remarkably small, with point estimates ranging from 65-289 individuals. Excess homozygosity was detected at 10 loci in all bays (FIS = 0.169-0.283) and individuals exhibited high average internal relatedness (IR; mean = 0.226). These both indicate that inbreeding is very common in all bays, after testing for and ruling out alternative explanations such as technical and sampling artifacts. This study demonstrates that even historically common marine fish can be prone to inbreeding, a factor that should be considered in fisheries management and conservation plans.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0066126PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3676343PMC
January 2014

The behavioural and genetic mating system of the sand tiger shark, Carcharias taurus, an intrauterine cannibal.

Biol Lett 2013 Jun 1;9(3):20130003. Epub 2013 May 1.

School of Marine and Atmospheric Science, Institute for Ocean Conservation Science, Stony Brook University, Stony Brook, NY 11794, USA.

Sand tiger sharks (Carcharias taurus) have an unusual mode of reproduction, whereby the first embryos in each of the paired uteri to reach a certain size ('hatchlings') consume all of their smaller siblings during gestation ('embryonic cannibalism' or EC). If females commonly mate with multiple males ('behavioural polyandry') then litters could initially have multiple sires. It is possible, however, that EC could exclude of all but one of these sires from producing offspring thus influencing the species genetic mating system ('genetic monogamy'). Here, we use microsatellite DNA profiling of mothers and their litters (n = 15, from two to nine embryos per litter) to quantify the frequency of behavioural and genetic polyandry in this system. We conservatively estimate that nine of the females we examined (60%) were behaviourally polyandrous. The genetic mating system was characterized by assessing sibling relationships between hatchlings and revealed only 40 per cent genetic polyandry (i.e. hatchlings were full siblings in 60% of litters). The discrepancy stemmed from three females that were initially fertilized by multiple males but only produced hatchlings with one of them. This reveals that males can be excluded even after fertilizing ova and that some instances of genetic monogamy in this population arise from the reduction in litter size by EC. More research is needed on how cryptic post-copulatory and post-zygotic processes contribute to determining paternity and bridging the behavioural and genetic mating systems of viviparous species.
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http://dx.doi.org/10.1098/rsbl.2013.0003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3645029PMC
June 2013

Phylogeography of two closely related Indo-Pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites.

J Hered 2012 Sep-Oct;103(5):617-29. Epub 2012 Aug 11.

Hawai'i Institute of Marine Biology Kaāne'ohe, HI, USA.

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.
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http://dx.doi.org/10.1093/jhered/ess056DOI Listing
March 2013

Larval export from marine reserves and the recruitment benefit for fish and fisheries.

Curr Biol 2012 Jun 24;22(11):1023-8. Epub 2012 May 24.

School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia.

Marine reserves, areas closed to all forms of fishing, continue to be advocated and implemented to supplement fisheries and conserve populations. However, although the reproductive potential of important fishery species can dramatically increase inside reserves, the extent to which larval offspring are exported and the relative contribution of reserves to recruitment in fished and protected populations are unknown. Using genetic parentage analyses, we resolve patterns of larval dispersal for two species of exploited coral reef fish within a network of marine reserves on the Great Barrier Reef. In a 1,000 km(2) study area, populations resident in three reserves exported 83% (coral trout, Plectropomus maculatus) and 55% (stripey snapper, Lutjanus carponotatus) of assigned offspring to fished reefs, with the remainder having recruited to natal reserves or other reserves in the region. We estimate that reserves, which account for just 28% of the local reef area, produced approximately half of all juvenile recruitment to both reserve and fished reefs within 30 km. Our results provide compelling evidence that adequately protected reserve networks can make a significant contribution to the replenishment of populations on both reserve and fished reefs at a scale that benefits local stakeholders.
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http://dx.doi.org/10.1016/j.cub.2012.04.008DOI Listing
June 2012

Genetic diversity despite population collapse in a critically endangered marine fish: the smalltooth sawfish (Pristis pectinata).

J Hered 2011 Nov-Dec;102(6):643-52. Epub 2011 Sep 15.

Institute for Ocean Conservation Science & School of Marine and Atmospheric Science, Stony Brook University, Stony Brook, NY 11794, USA.

Sawfish (family Pristidae) are among the most critically endangered marine fish in the world, yet very little is known about how genetic bottlenecks, genetic drift, and inbreeding depression may be affecting these elasmobranchs. In the US Atlantic, the smalltooth sawfish (Pristis pectinata) has declined to 1-5% of its abundance in the 1900s, and its core distribution has contracted to southwest Florida. We used 8 polymorphic microsatellite markers to show that this remnant population still exhibits high genetic diversity in terms of average allelic richness (18.23), average alleles per locus (18.75, standard deviation [SD] 6.6) and observed heterozygosity (0.43-0.98). Inbreeding is rare (mean individual internal relatedness = -0.02, SD 0.14; F(IS) = -0.011, 95% confidence interval [CI] = -0.039 to 0.011), even though the estimated effective population size (N(e)) is modest (250-350, 95% CI = 142-955). Simulations suggest that the remnant smalltooth sawfish population will probably retain >90% of its current genetic diversity over the next century even at the lower estimate of N(e). There is no evidence of a genetic bottleneck accompanying last century's demographic bottleneck, and we discuss hypotheses that could explain this. We also discuss features of elasmobranch life history and population biology that could make them less vulnerable than other large marine vertebrates to genetic change associated with reduced population size.
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http://dx.doi.org/10.1093/jhered/esr098DOI Listing
February 2012

Investigating the allelic evolution of an imperfect microsatellite locus in the Hawaiian mushroom Rhodocollybia laulaha.

J Hered 2011 Nov-Dec;102(6):727-34. Epub 2011 Sep 13.

Committee on Evolutionary Biology, University of Chicago, Chicago, IL, USA.

The evolutionary mechanisms that give rise to microsatellite alleles remain poorly understood in general and are especially understudied for fungal microsatellite loci. The unusual G28 microsatellite locus was developed from the Hawaiian mushroom Rhodocollybia laulaha. Here, we employ a novel approach to test for allele size homoplasy and examine competing mechanistic models of microsatellite evolution in the context of biogeographic expectations for this locus based on Hawaiian geologic history. Seven G28 alleles have been identified from a sampling of 153 individuals. The G28 locus is composed of a trinucleotide imperfect motif, which permits examination of the relationships between alleles and allows for detection of potential size homoplasy within the repetitive element. Alignment of G28 allele sequence data across multiple unrelated individuals suggests that alleles of like size are homologous within Hawaii. A variety of gap coding methods are explored in the inference of allele evolution. Length differences between alleles appear to be the result of polymerase slippage at multiple positions in the repetitive element, suggesting an intricate process of allelic evolution, which is not necessarily stepwise. Complex migration scenarios must be invoked to explain the current geographic distribution of alleles if their evolution was in fact sequential (from longest to shortest or from shortest to longest) as predicted by the "progression rule."
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http://dx.doi.org/10.1093/jhered/esr099DOI Listing
February 2012

Microsatellite loci for dreissenid mussels (Mollusca: Bivalvia: Dreissenidae) and relatives: markers for assessing exotic and native populations.

Mol Ecol Resour 2011 Jul 1;11(4):725-32. Epub 2011 Apr 1.

Field Museum, 1400 S Lake Shore Dr, Chicago, IL 60605, USA.

We developed and tested 14 new polymorphic microsatellite loci for dreissenid mussels, including the two species that have invaded many freshwater habitats in Eurasia and North America, where they cause serious industrial fouling damage and ecological alterations. These new loci will aid our understanding of their genetic patterns in invasive populations as well as throughout their native Ponto-Caspian distributions. Eight new loci for the zebra mussel Dreissena polymorpha polymorpha and six for the quagga mussel D. rostriformis bugensis were compared with new results from six previously published loci to generate a robust molecular toolkit for dreissenid mussels and their relatives. Taxa tested include D. p. polymorpha, D. r. bugensis, D. r. grimmi, D. presbensis, the 'living fossil'Congeria kusceri, and the dark false mussel Mytilopsis leucophaeata (the latter also is invasive). Overall, most of the 24 zebra mussel (N = 583) and 13 quagga mussel (N = 269) population samples conformed to Hardy-Weinberg equilibrium expectations for the new loci following sequential Bonferroni correction. The 11 loci (eight new, three previously published) evaluated for D. p. polymorpha averaged 35.1 alleles and 0.72 mean observed heterozygosity per locus, and 25.3 and 0.75 for the nine loci (six new, three previously published) developed for D. r. bugensis. All but three of these loci successfully amplified the other species of Dreissena, and all but one also amplified Congeria and Mytilopsis. All species and populations tested were significantly divergent using the microsatellite data, with neighbour-joining trees reflecting their evolutionary relationships; our results reveal broad utility for resolving their biogeographic, evolutionary, population and ecological patterns.
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http://dx.doi.org/10.1111/j.1755-0998.2011.03012.xDOI Listing
July 2011

Anthropogenic disturbance and evolutionary parameters: a lemon shark population experiencing habitat loss.

Evol Appl 2011 Jan 6;4(1):1-17. Epub 2010 Apr 6.

Redpath Museum and Department of Biology, McGill University Montréal, QC, Canada.

The level of genetic variation in natural populations influences evolutionary potential, and may therefore influence responses to selection in the face of future environmental changes. By combining long-term monitoring of marked individuals with genetic pedigree reconstruction, we assessed whether habitat loss influenced genetic variation in a lemon shark (Negaprion brevirostris) population at an isolated nursery lagoon (Bimini, Bahamas). We also tracked changes in the strength and direction of natural selection. Contrary to initial expectations, we found that after the habitat loss neutral genetic variation increased, as did additive genetic variance for juvenile morphological traits (body length and mass). We hypothesize that these effects might result from philopatric behavior in females coupled with a possible influx of male genotypes from other nursery sites. We also found changes in the strength of selection on morphological traits, which weakened considerably after the disturbance; habitat loss therefore changed the phenotypes favored by natural selection. Because such human-induced shifts in the adaptive landscape may be common, we suggest that conservation biologists should not simply focus on neutral genetic variation per se, but also on assessing and preserving evolutionary parameters, such as additive genetic variation and selection.
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http://dx.doi.org/10.1111/j.1752-4571.2010.00125.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3352521PMC
January 2011
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