Publications by authors named "Brendan F Wringe"

14 Publications

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Chromosome level reference of Atlantic halibut Hippoglossus hippoglossus provides insight into the evolution of sexual determination systems.

Mol Ecol Resour 2021 Mar 2. Epub 2021 Mar 2.

Biology Department, Dalhousie University, Halifax, NS, Canada.

Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes. To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multitissue transcriptomes, and reduced representation population data for the Atlantic halibut (Hippoglossus hippoglossus), which has an XY/XX sex determination mechanism and has recently diverged (0.9-3.8 Ma) from the Pacific halibut (Hippoglossus stenolepis), which has a ZZ/ZW system. We used frequency and coverage-based population approaches to identify a putative sex-determining factor, GSDF. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a nascent sex chromosome. We detected testis-specific expression of GSDF, the sequence of which is highly conserved across flatfishes. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfishes, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic halibut. Changes to the ancestral sex-determining gene DMRT1 in regulating the downstream gene GSDF probably coincided with GSDF, or a proximal regulatory element of it, becoming the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multitissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes.
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http://dx.doi.org/10.1111/1755-0998.13369DOI Listing
March 2021

Estimating the relative fitness of escaped farmed salmon offspring in the wild and modelling the consequences of invasion for wild populations.

Evol Appl 2019 Apr 28;12(4):705-717. Epub 2019 Jan 28.

Science Branch, Fisheries and Oceans Canada St. John's Newfoundland and Labrador Canada.

Throughout their native range, wild Atlantic salmon populations are threatened by hybridization and introgression with escapees from net-pen salmon aquaculture. Although domestic-wild hybrid offspring have shown reduced fitness in laboratory and field experiments, consequential impacts on population abundance and genetic integrity remain difficult to predict in the field, in part because the strength of selection against domestic offspring is often unknown and context-dependent. Here, we follow a single large escape event of farmed Atlantic salmon in southern Newfoundland and monitor changes in the in-river proportions of hybrids and feral individuals over time using genetically based hybrid identification. Over a three-year period following the escape, the overall proportion of wild parr increased consistently (total wild proportion of 71.6%, 75.1% and 87.5% each year, respectively), with subsequent declines in feral (genetically pure farmed individuals originating from escaped, farmed adults) and hybrid parr. We quantify the strength of selection against parr of aquaculture ancestry and explore the genetic and demographic consequences for populations in the region. Within-cohort changes in the relative proportions of feral and F1 parr suggest reduced relative survival compared to wild individuals over the first (0.15 and 0.81 for feral and F1, respectively) and second years of life (0.26, 0.83). These relative survivorship estimates were used to inform an individual-based salmon eco-genetic model to project changes in adult abundance and overall allele frequency across three invasion scenarios ranging from short-term to long-term invasion and three relative survival scenarios. Modelling results indicate that total population abundance and time to recovery were greatly affected by relative survivorship and predict significant declines in wild population abundance under continued large escape events and calculated survivorship. Overall, this work demonstrates the importance of estimating the strength of selection against domestic offspring in the wild to predict the long-term impact of farmed salmon escape events on wild populations.
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http://dx.doi.org/10.1111/eva.12746DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6439497PMC
April 2019

Temporal dynamics of genetic clines of invasive European green crab () in eastern North America.

Evol Appl 2018 Oct 28;11(9):1656-1670. Epub 2018 Jun 28.

Northwest Atlantic Fisheries Centre Fisheries and Oceans Canada St. John's Newfoundland Canada.

Two genetically distinct lineages of European green crabs () were independently introduced to eastern North America, the first in the early 19th century and the second in the late 20th century. These lineages first came into secondary contact in southeastern Nova Scotia, Canada (NS), where they hybridized, producing latitudinal genetic clines. Previous studies have documented a persistent southward shift in the clines of different marker types, consistent with existing dispersal and recruitment pathways. We evaluated current clinal structure by quantifying the distribution of lineages and fine-scale hybridization patterns across the eastern North American range (25 locations, ~39 to 49°N) using informative single nucleotide polymorphisms (SNPs;  = 96). In addition, temporal changes in the genetic clines were evaluated using mitochondrial DNA and microsatellite loci ( = 9-11) over a 15-year period (2000-2015). Clinal structure was consistent with prior work demonstrating the existence of both northern and southern lineages with a hybrid zone occurring between southern New Brunswick (NB) and southern NS. Extensive later generation hybrids were detected in this region and in southeastern Newfoundland. Temporal genetic analysis confirmed the southward progression of clines over time; however, the rate of this progression was slower than predicted by forecasting models, and current clines for all marker types deviated significantly from these predictions. Our results suggest that neutral and selective processes contribute to cline dynamics, and ultimately, highlight how selection, hybridization, and dispersal can collectively influence invasion success.
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http://dx.doi.org/10.1111/eva.12657DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6183463PMC
October 2018

Extensive hybridization following a large escape of domesticated Atlantic salmon in the Northwest Atlantic.

Commun Biol 2018 9;1:108. Epub 2018 Aug 9.

Science Branch, Fisheries and Oceans Canada, 80 East White Hills Road, St. John's, Newfoundland, A1C 5X1, Canada.

Domestication is rife with episodes of interbreeding between cultured and wild populations, potentially challenging adaptive variation in the wild. In Atlantic salmon, , the number of domesticated individuals far exceeds wild individuals, and escape events occur regularly, yet evidence of the magnitude and geographic scale of interbreeding resulting from individual escape events is lacking. We screened juvenile Atlantic salmon using 95 single nucleotide polymorphisms following a single, large aquaculture escape in the Northwest Atlantic and report the landscape-scale detection of hybrid and feral salmon (27.1%, 17/18 rivers). Hybrids were reproductively viable, and observed at higher frequency in smaller wild populations. Repeated annual sampling of this cohort revealed decreases in the presence of hybrid and feral offspring over time. These results link previous observations of escaped salmon in rivers with reports of population genetic change, and demonstrate the potential negative consequences of escapes from net-pen aquaculture on wild populations.
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http://dx.doi.org/10.1038/s42003-018-0112-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6123692PMC
August 2018

Genotyping-by-sequencing of genome-wide microsatellite loci reveals fine-scale harvest composition in a coastal Atlantic salmon fishery.

Evol Appl 2018 Jul 11;11(6):918-930. Epub 2018 Mar 11.

Department of Biology Dalhousie University Halifax NS Canada.

Individual assignment and genetic mixture analysis are commonly utilized in contemporary wildlife and fisheries management. Although microsatellite loci provide unparalleled numbers of alleles per locus, their use in assignment applications is increasingly limited. However, next-generation sequencing, in conjunction with novel bioinformatic tools, allows large numbers of microsatellite loci to be simultaneously genotyped, presenting new opportunities for individual assignment and genetic mixture analysis. Here, we scanned the published Atlantic salmon genome to identify 706 microsatellite loci, from which we developed a final panel of 101 microsatellites distributed across the genome (average 3.4 loci per chromosome). Using samples from 35 Atlantic salmon populations ( = 1,485 individuals) from coastal Labrador, Canada, a region characterized by low levels of differentiation in this species, this panel identified 844 alleles (average of 8.4 alleles per locus). Simulation-based evaluations of assignment and mixture identification accuracy revealed unprecedented resolution, clearly identifying 26 rivers or groups of rivers spanning 500 km of coastline. This baseline was used to examine the stock composition of 696 individuals harvested in the Labrador Atlantic salmon fishery and revealed that coastal fisheries largely targeted regional groups (<300 km). This work suggests that the development and application of large sequenced microsatellite panels presents great potential for stock resolution in Atlantic salmon and more broadly in other exploited anadromous and marine species.
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http://dx.doi.org/10.1111/eva.12606DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5999200PMC
July 2018

Genomewide evidence of environmentally mediated secondary contact of European green crab () lineages in eastern North America.

Evol Appl 2018 Jul 23;11(6):869-882. Epub 2018 Feb 23.

Fisheries and Oceans Canada Bedford Institute of Oceanography Dartmouth NS Canada.

Genetic-environment associations are increasingly revealed through population genomic data and can occur through a number of processes, including secondary contact, divergent natural selection, or isolation by distance. Here, we investigate the influence of the environment, including seasonal temperature and salinity, on the population structure of the invasive European green crab () in eastern North America. Green crab populations in eastern North America are associated with two independent invasions, previously shown to consist of distinct northern and southern ecotypes, with a contact zone in southern Nova Scotia, Canada. Using a RAD-seq panel of 9,137 genomewide SNPs, we detected 41 SNPs (0.49%) whose allele frequencies were highly correlated with environmental data. A principal components analysis of 25 environmental variables differentiated populations into northern, southern, and admixed sites in concordance with the observed genomic spatial structure. Furthermore, a spatial principal components analysis conducted on genomic and geographic data revealed a high degree of global structure ( < .0001) partitioning a northern and southern ecotype. Redundancy and partial redundancy analyses revealed that among the environmental variables tested, winter sea surface temperature had the strongest association with spatial structuring, suggesting that it is an important factor defining range and expansion limits of each ecotype. Understanding environmental thresholds associated with intraspecific diversity will facilitate the ability to manage current and predict future distributions of this aquatic invasive species.
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http://dx.doi.org/10.1111/eva.12601DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5999199PMC
July 2018

Fine-scale temperature-associated genetic structure between inshore and offshore populations of sea scallop (Placopecten magellanicus).

Heredity (Edinb) 2019 01 17;122(1):69-80. Epub 2018 May 17.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St. John's, NL, A1C 5X1, Canada.

In the northwest Atlantic Ocean, sea scallop (Placopecten magellanicus) has been characterized by a latitudinal genetic cline with a breakpoint between northern and southern genetic clusters occurring at ~45°N along eastern Nova Scotia, Canada. Using 96 diagnostic single-nucleotide polymorphisms (SNPs) capable of discriminating between northern and southern clusters, we examined fine-scale genetic structure of scallops among 27 sample locations, spanning the largest geographic range evaluated in this species to date (~37-51°N). Here, we confirmed previous observations of northern and southern groups, but we show that the boundary between northern and southern clusters is not a discrete latitudinal break. Instead, at latitudes near the previously described boundary, we found unexpected patterns of fine-scale genetic structure occurring between inshore and offshore sites. Scallops from offshore sites, including St. Pierre Bank and the eastern Scotian Shelf, clustered with southern stocks, whereas inshore sites at similar latitudes clustered with northern stocks. Our analyses revealed significant genetic divergence across small spatial scales (i.e., 129-221 km distances), and that spatial structure over large and fine scales was strongly associated with temperature during seasonal periods of thermal minima. Clear temperature differences between inshore and offshore locations may explain the fine-scale structuring observed, such as why southern lineages of scallop occur at higher latitudes in deeper, warmer offshore waters. Our study supports growing evidence that fine-scale population structure in marine species is common, often environmentally associated, and that consideration of environmental and genomic data can significantly enhance the identification of marine diversity and management units.
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http://dx.doi.org/10.1038/s41437-018-0087-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6288113PMC
January 2019

A climate-associated multispecies cryptic cline in the northwest Atlantic.

Sci Adv 2018 03 28;4(3):eaaq0929. Epub 2018 Mar 28.

Department of Computer Science, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.

The spatial genetic structure of most species in the open marine environment remains largely unresolved. This information gap creates uncertainty in the sustainable management, recovery, and associated resilience of marine communities and our capacity to extrapolate beyond the few species for which such information exists. We document a previously unidentified multispecies biogeographic break aligned with a steep climatic gradient and driven by seasonal temperature minima in the northwest Atlantic. The coherence of this genetic break across our five study species with contrasting life histories suggests a pervasive macroecological phenomenon. The integration of this genetic structure with habitat suitability models and climate forecasts predicts significant variation in northward distributional shifts among populations and availability of suitable habitat in future oceans. The results of our integrated approach provide new perspective on how cryptic intraspecific diversity associated with climatic variation influences species and community response to climate change beyond simple poleward shifts.
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http://dx.doi.org/10.1126/sciadv.aaq0929DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5873842PMC
March 2018

A novel sperm adaptation to evolutionary constraints on reproduction: Pre-ejaculatory sperm activation in the beach spawning capelin (Osmeridae).

Ecol Evol 2018 02 29;8(4):2343-2349. Epub 2018 Jan 29.

Department of Biology Memorial University St. John's NL Canada.

Reproduction of external fertilizing vertebrates is typically constrained to either fresh or salt water, not both. For all studied amphibians and fishes, this constraint includes immotile sperm that are activated after ejaculation only by the specific chemistry of the fertilizing medium in which the species evolved (fresh, brackish, or salt water). No amphibians can reproduce in the sea. Although diadromous fishes may migrate between salt and fresh water, they are shackled to their natal environment for spawning in part because of sperm activation. Here, we report for the first time among all documented external fertilizing vertebrates, that in the absence of any external media, sperm are motile at ejaculation in a marine spawning fish (Osmeridae, capelin, ). To illuminate why, we evaluated sperm behavior at different salinities in as well as the related freshwater spawning anadromous rainbow smelt (). Surprisingly, sperm performance was superior in fresh water for both species. spend their entire life at sea but our results show that their sperm are deactivated by sea water, suggesting a freshwater ancestry. By circumventing constraining water chemistry, we interpret the unique pre-ejaculatory sperm activation in this species as a novel adaptation that enables fertilization in the marine environment. These findings also contribute to understanding the persistence of anadromy, despite great energetic costs to adult fishes.
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http://dx.doi.org/10.1002/ece3.3783DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5817138PMC
February 2018

Range-wide parallel climate-associated genomic clines in Atlantic salmon.

R Soc Open Sci 2017 Nov 15;4(11):171394. Epub 2017 Nov 15.

Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, St John's, Newfoundland and Labrador, CanadaA1C 5X1.

Clinal variation across replicated environmental gradients can reveal evidence of local adaptation, providing insight into the demographic and evolutionary processes that shape intraspecific diversity. Using 1773 genome-wide single nucleotide polymorphisms we evaluated latitudinal variation in allele frequency for 134 populations of North American and European Atlantic salmon (). We detected 84 (4.74%) and 195 (11%) loci showing clinal patterns in North America and Europe, respectively, with 12 clinal loci in common between continents. Clinal single nucleotide polymorphisms were evenly distributed across the salmon genome and logistic regression revealed significant associations with latitude and seasonal temperatures, particularly average spring temperature in both continents. Loci displaying parallel clines were associated with several metabolic and immune functions, suggesting a potential basis for climate-associated adaptive differentiation. These climate-based clines collectively suggest evidence of large-scale environmental associated differences on either side of the North Atlantic. Our results support patterns of parallel evolution on both sides of the North Atlantic, with evidence of both similar and divergent underlying genetic architecture. The identification of climate-associated genomic clines illuminates the role of selection and demographic processes on intraspecific diversity in this species and provides a context in which to evaluate the impacts of climate change.
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http://dx.doi.org/10.1098/rsos.171394DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5717698PMC
November 2017

hybriddetective: A workflow and package to facilitate the detection of hybridization using genomic data in r.

Mol Ecol Resour 2017 Nov 18;17(6):e275-e284. Epub 2017 Sep 18.

Salmonids Section, Northwest Atlantic Fisheries Centre, Fisheries and Oceans Canada, St. John's, NL, Canada.

The ability to detect and characterize hybridization in nature has long been of interest to many fields of biology and often has direct implications for wildlife management and conservation. The capacity to identify the presence of hybridization, and quantify the numbers of individuals belonging to different hybrid classes, permits inference on the magnitude of, and timescale over which, hybridization has been or is occurring. Here, we present an r package and associated workflow developed for the detection, with estimates of efficiency and accuracy, of multigenerational hybrid individuals using genetic or genomic data in conjunction with the program newhybrids. This package includes functions for the identification and testing of diagnostic panels of markers, the simulation of multigenerational hybrids, and the quantification and visualization of the efficiency and accuracy with which hybrids can be detected. Overall, this package delivers a streamlined hybrid analysis platform, providing improvements in speed, ease of use and repeatability over current ad hoc approaches. The latest version of the package and associated documentation are available on GitHub (https://github.com/bwringe/hybriddetective).
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http://dx.doi.org/10.1111/1755-0998.12704DOI Listing
November 2017

parallelnewhybrid: an R package for the parallelization of hybrid detection using newhybrids.

Mol Ecol Resour 2017 Jan 1;17(1):91-95. Epub 2016 Oct 1.

Fisheries and Oceans Canada, Salmonids Section, 80 East White Hills Road, St. John's, Newfoundland and Labrador, Canada, A1C 5X1.

Hybridization among populations and species is a central theme in many areas of biology, and the study of hybridization has direct applicability to testing hypotheses about evolution, speciation and genetic recombination, as well as having conservation, legal and regulatory implications. Yet, despite being a topic of considerable interest, the identification of hybrid individuals, and quantification of the (un)certainty surrounding the identifications, remains difficult. Unlike other programs that exist to identify hybrids based on genotypic information, newhybrids is able to assign individuals to specific hybrid classes (e.g. F , F ) because it makes use of patterns of gene inheritance within each locus, rather than just the proportions of gene inheritance within each individual. For each comparison and set of markers, multiple independent runs of each data set should be used to develop an estimate of the hybrid class assignment accuracy. The necessity of analysing multiple simulated data sets, constructed from large genomewide data sets, presents significant computational challenges. To address these challenges, we present parallelnewhybrid, an r package designed to decrease user burden when undertaking multiple newhybrids analyses. parallelnewhybrid does so by taking advantage of the parallel computational capabilities inherent in modern computers to efficiently and automatically execute separate newhybrids runs in parallel. We show that parallelization of analyses using this package affords users several-fold reductions in time over a traditional serial analysis. parallelnewhybrid consists of an example data set, a readme and three operating system-specific functions to execute parallel newhybrids analyses on each of a computer's c cores. parallelnewhybrid is freely available on the long-term software hosting site github (www.github.com/bwringe/parallelnewhybrid).
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http://dx.doi.org/10.1111/1755-0998.12597DOI Listing
January 2017

genepopedit: a simple and flexible tool for manipulating multilocus molecular data in R.

Mol Ecol Resour 2017 Jan 11;17(1):12-18. Epub 2016 Aug 11.

Northwest Atlantic Fisheries Science Centre, St. John's, Newfoundland, Canada.

Advances in genetic sequencing technologies and techniques have made large, genome-wide data sets comprised of hundreds or even thousands of individuals and loci the norm rather than the exception even for nonmodel organisms. While such data present new opportunities for evaluating population structure and demographic processes, the large size of these genomic data sets brings new computational challenges for researchers needing to parse, convert and manipulate data often into a variety of software-specific formats required of genomic analyses. We developed genepopedit as a flexible tool for the manipulation of multilocus molecular data sets. Functionality can be divided among diagnostic-, manipulation-, sampling-, simulation-, and transformation-based tools. Metadata from large genomic data sets can be efficiently extracted, without the need to view data in a text-editing program. genepopedit provides tools to manipulate loci, individual samples and populations included in genomic data sets, in addition to the ability to convert directly to a variety of software formats. Functions are compiled as an R package, which can integrate into existing analysis workflows. Importantly, genepopedit provides a simple yet robust code-based tool for repeatable genomic data manipulation, which has been proven to be stable for data sets in excess of 200 000 SNPs. The latest version of the package and associated documentation are available on Github (github.com/rystanley/genepopedit).
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http://dx.doi.org/10.1111/1755-0998.12569DOI Listing
January 2017

Growth-related quantitative trait loci in domestic and wild rainbow trout (Oncorhynchus mykiss).

BMC Genet 2010 Jul 7;11:63. Epub 2010 Jul 7.

Department of Integrative Biology, 50 Stone Road East, University of Guelph, Guelph, ON N1G 2W1 Canada.

Background: Somatic growth is a complex process that involves the action and interaction of genes and environment. A number of quantitative trait loci (QTL) previously identified for body weight and condition factor in rainbow trout (Oncorhynchus mykiss), and two other salmonid species, were used to further investigate the genetic architecture of growth-influencing genes in this species. Relationships among previously mapped candidate genes for growth and their co-localization to identified QTL regions are reported. Furthermore, using a comparative genomic analysis of syntenic rainbow trout linkage group clusters to their homologous regions within model teleost species such as zebrafish, stickleback and medaka, inferences were made regarding additional possible candidate genes underlying identified QTL regions.

Results: Body weight (BW) QTL were detected on the majority of rainbow trout linkage groups across 10 parents from 3 strains. However, only 10 linkage groups (i.e., RT-3, -6, -8, -9, -10, -12, -13, -22, -24, -27) possessed QTL regions with chromosome-wide or genome-wide effects across multiple parents. Fewer QTL for condition factor (K) were identified and only six instances of co-localization across families were detected (i.e. RT-9, -15, -16, -23, -27, -31 and RT-2/9 homeologs). Of note, both BW and K QTL co-localize on RT-9 and RT-27. The incidence of epistatic interaction across genomic regions within different female backgrounds was also examined, and although evidence for interaction effects within certain QTL regions were evident, these interactions were few in number and statistically weak. Of interest, however, was the fact that these predominantly occurred within K QTL regions. Currently mapped growth candidate genes are largely congruent with the identified QTL regions. More QTL were detected in male, compared to female parents, with the greatest number evident in an F1 male parent derived from an intercross between domesticated and wild strain of rainbow trout which differed strongly in growth rate.

Conclusions: Strain background influences the degree to which QTL effects are evident for growth-related genes. The process of domestication (which primarily selects faster growing fish) may largely reduce the genetic influences on growth-specific phenotypic variation. Although heritabilities have been reported to be relatively high for both BW and K growth traits, the genetic architecture of K phenotypic variation appears less defined (i.e., fewer major contributing QTL regions were identified compared with BW QTL regions).
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http://dx.doi.org/10.1186/1471-2156-11-63DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2914766PMC
July 2010