Publications by authors named "Angel Amores"

36 Publications

RADSex: A computational workflow to study sex determination using restriction site-associated DNA sequencing data.

Mol Ecol Resour 2021 Jul 9;21(5):1715-1731. Epub 2021 Mar 9.

Physiological Chemistry, Biocenter, University of Wuerzburg, Wuerzburg, Germany.

The study of sex determination and sex chromosome organization in nonmodel species has long been technically challenging, but new sequencing methodologies now enable precise and high-throughput identification of sex-specific genomic sequences. In particular, restriction site-associated DNA sequencing (RAD-Seq) is being extensively applied to explore sex determination systems in many plant and animal species. However, software specifically designed to search for and visualize sex-biased markers using RAD-Seq data is lacking. Here, we present RADSex, a computational analysis workflow designed to study the genetic basis of sex determination using RAD-Seq data. RADSex is simple to use, requires few computational resources, makes no prior assumptions about the type of sex-determination system or structure of the sex locus, and offers convenient visualization through a dedicated R package. To demonstrate the functionality of RADSex, we re-analysed a published data set of Japanese medaka, Oryzias latipes, where we uncovered a previously unknown Y chromosome polymorphism. We then used RADSex to analyse new RAD-Seq data sets from 15 fish species spanning multiple taxonomic orders. We identified the sex determination system and sex-specific markers in six of these species, five of which had no known sex-markers prior to this study. We show that RADSex greatly facilitates the study of sex determination systems in nonmodel species thanks to its speed of analyses, low resource usage, ease of application and visualization options. Furthermore, our analysis of new data sets from 15 species provides new insights on sex determination in fish.
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http://dx.doi.org/10.1111/1755-0998.13360DOI Listing
July 2021

The Developmental and Genetic Architecture of the Sexually Selected Male Ornament of Swordtails.

Curr Biol 2021 Mar 3;31(5):911-922.e4. Epub 2020 Dec 3.

Institute of Neuroscience, University of Oregon, Eugene, OR 97401, USA. Electronic address:

Sexual selection results in sex-specific characters like the conspicuously pigmented extension of the ventral tip of the caudal fin-the "sword"-in males of several species of Xiphophorus fishes. To uncover the genetic architecture underlying sword formation and to identify genes that are associated with its development, we characterized the sword transcriptional profile and combined it with genetic mapping approaches. Results showed that the male ornament of swordtails develops from a sexually non-dimorphic prepattern of transcription factors in the caudal fin. Among genes that constitute the exclusive sword transcriptome and are located in the genomic region associated with this trait we identify the potassium channel, Kcnh8, as a sword development gene. In addition to its neural function kcnh8 performs a known role in fin growth. These findings indicate that during evolution of swordtails a brain gene has been co-opted for an additional novel function in establishing a male ornament.
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http://dx.doi.org/10.1016/j.cub.2020.11.028DOI Listing
March 2021

Chromonomer: A Tool Set for Repairing and Enhancing Assembled Genomes Through Integration of Genetic Maps and Conserved Synteny.

G3 (Bethesda) 2020 11 5;10(11):4115-4128. Epub 2020 Nov 5.

Institute of Ecology and Evolution, University of Oregon, Eugene, OR.

The pace of the sequencing and computational assembly of novel reference genomes is accelerating. Though DNA sequencing technologies and assembly software tools continue to improve, biological features of genomes such as repetitive sequence as well as molecular artifacts that often accompany sequencing library preparation can lead to fragmented or chimeric assemblies. If left uncorrected, defects like these trammel progress on understanding genome structure and function, or worse, positively mislead this research. Fortunately, integration of additional, independent streams of information, such as a marker-dense genetic map and conserved orthologous gene order from related taxa, can be used to scaffold together unlinked, disordered fragments and to restructure a reference genome where it is incorrectly joined. We present a tool set for automating these processes, one that additionally tracks any changes to the assembly and to the genetic map, and which allows the user to scrutinize these changes with the help of web-based, graphical visualizations. Chromonomer takes a user-defined reference genome, a map of genetic markers, and, optionally, conserved synteny information to construct an improved reference genome of chromosome models: a "chromonome". We demonstrate Chromonomer's performance on genome assemblies and genetic maps that have disparate characteristics and levels of quality.
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http://dx.doi.org/10.1534/g3.120.401485DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7642942PMC
November 2020

3D hotspots of marine litter in the Mediterranean: A modeling study.

Mar Pollut Bull 2020 Jun 27;155:111159. Epub 2020 Apr 27.

Spanish Oceanographic Institute - Balearic Oceanographic Centre (IEO-COB), Mallorca, Spain.

The 3D dispersion of marine litter (ML) over the Mediterranean basin has been simulated using the velocity fields from a high resolution circulation model as base to run a 3D Lagrangian model. Three simulations have been performed to mimic the evolution of ML with density lower, similar, or higher than seawater. In all cases a realistic distribution of ML sources was used. Our results show that the accumulation/dispersion areas of the floating and buoyancy neutral particles are practically the same, although the latter are distributed in the water column, 80% of them found in the photic layer (average depth of 35m). Regarding to the densest particles, they rapidly sink and reach the seafloor close to their source. The regions of higher temporal variability mostly coincide with the ML accumulation regions. Weak seasonal variability occurs at a sub-basin scale as a result of the particles redistribution induced by the seasonal variability of the current field.
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http://dx.doi.org/10.1016/j.marpolbul.2020.111159DOI Listing
June 2020

Multiple independent chromosomal fusions accompanied the radiation of the Antarctic teleost genus Trematomus (Notothenioidei:Nototheniidae).

BMC Evol Biol 2020 03 20;20(1):39. Epub 2020 Mar 20.

Sorbonne Université, CNRS, Université des Antilles, Evolution Paris Seine - Institut de Biologie Paris Seine (EPS - IBPS), 75005, Paris, France.

Background: Chromosomal rearrangements are thought to be an important driving force underlying lineage diversification, but their link to speciation continues to be debated. Antarctic teleost fish of the family Nototheniidae (Notothenioidei) diversified in a changing environmental context, which led to ecological, morphological, and genetic differentiation among populations. In addition, extensive chromosomal repatterning accompanied species divergence in several clades. The most striking karyotypic changes involved the recent species radiation (about 10 My) of the genus Trematomus, with chromosomal pair numbers ranging between 29 and 12. These dramatic reductions in chromosome number resulted mostly from large-scale chromosome fusions. Multiple centric and/or tandem fusions have been hypothesized in at least seven of the twelve recognized Trematomus species. To reconstruct their evolutionary history, we employed comparative cytogenomics (BAC-FISH and chromosome painting) to reveal patterns of interspecific chromosomal orthologies across several notothenioid clades.

Results: We defined orthologous chromosomal segments of reference, termed Structural Units (SUs). SUs were identified in a total of 18 notothenioid species. We demonstrated for the first time that SUs were strongly conserved across every specimen examined, with chromosomal syntenies highlighting a paucity of intrachromosomal macro-rearrangements. Multiple independent fusions of these SUs were inferred in the Trematomus species, in contrast to the shared SU fusions in species of the sister lineage Notothenia.

Conclusions: The SU segments were defined units of chromosomal rearrangement in the entire family Nototheiidae, which diverged from the other notothenioid families 20 My ago. Some of the identified chromosomal syntenies within the SUs were even conserved in their closest relatives, the family Eleginopsidae. Comparing the timing of acquisition of the fusions in the closely related genera Notothenia and Trematomus of the nototheniid species family, we conclude that they exhibit distinct chromosomal evolutionary histories, which may be relevant to different speciation scenarios.
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http://dx.doi.org/10.1186/s12862-020-1600-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7082932PMC
March 2020

Tracking a mass mortality outbreak of pen shell Pinna nobilis populations: A collaborative effort of scientists and citizens.

Sci Rep 2019 09 16;9(1):13355. Epub 2019 Sep 16.

Oceanography and Global Change Department, Mediterranean Institute for Advanced Studies (CSIC-UIB), Esporles, Mallorca, Spain.

A mass mortality event is devastating the populations of the endemic bivalve Pinna nobilis in the Mediterranean Sea from early autumn 2016. A newly described Haplosporidian endoparasite (Haplosporidium pinnae) is the most probable cause of this ecological catastrophe placing one of the largest bivalves of the world on the brink of extinction. As a pivotal step towards Pinna nobilis conservation, this contribution combines scientists and citizens' data to address the fast- and vast-dispersion and prevalence outbreaks of the pathogen. Therefore, the potential role of currents on parasite expansion was addressed by means of drift simulations of virtual particles in a high-resolution regional currents model. A generalized additive model was implemented to test if environmental factors could modulate the infection of Pinna nobilis populations. The results strongly suggest that the parasite has probably dispersed regionally by surface currents, and that the disease expression seems to be closely related to temperatures above 13.5 °C and to a salinity range between 36.5-39.7 psu. The most likely spread of the disease along the Mediterranean basin associated with scattered survival spots and very few survivors (potentially resistant individuals), point to a challenging scenario for conservation of the emblematic Pinna nobilis, which will require fast and strategic management measures and should make use of the essential role citizen science projects can play.
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http://dx.doi.org/10.1038/s41598-019-49808-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6746856PMC
September 2019

Epigenetic factors Dnmt1 and Uhrf1 coordinate intestinal development.

Dev Biol 2019 11 5;455(2):473-484. Epub 2019 Aug 5.

Institute of Neuroscience, 1254 University of Oregon, Eugene, OR, 97403, USA. Electronic address:

Intestinal tract development is a coordinated process involving signaling among the progenitors and developing cells from all three germ layers. Development of endoderm-derived intestinal epithelium has been shown to depend on epigenetic modifications, but whether that is also the case for intestinal tract cell types from other germ layers remains unclear. We found that functional loss of a DNA methylation machinery component, ubiquitin-like protein containing PHD and RING finger domains 1 (uhrf1), leads to reduced numbers of ectoderm-derived enteric neurons and severe disruption of mesoderm-derived intestinal smooth muscle. Genetic chimeras revealed that Uhrf1 functions both cell-autonomously in enteric neuron precursors and cell-non-autonomously in surrounding intestinal cells, consistent with what is known about signaling interactions between these cell types that promote one another's development. Uhrf1 recruits the DNA methyltransferase Dnmt1 to unmethylated DNA during replication. Dnmt1 is also expressed in enteric neurons and smooth muscle progenitors. dnmt1 mutants have fewer enteric neurons and disrupted intestinal smooth muscle compared to wildtypes. Because dnmt1;uhrf1 double mutants have a similar phenotype to dnmt1 and uhrf1 single mutants, Dnmt1 and Uhrf1 must function together during enteric neuron and intestinal muscle development. This work shows that genes controlling epigenetic modifications are important to coordinate intestinal tract development, provides the first demonstration that these genes influence development of the ENS, and advances uhrf1 and dnmt1 as potential new Hirschsprung disease candidates.
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http://dx.doi.org/10.1016/j.ydbio.2019.08.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6842436PMC
November 2019

Antarctic blackfin icefish genome reveals adaptations to extreme environments.

Nat Ecol Evol 2019 03 25;3(3):469-478. Epub 2019 Feb 25.

Unit of Polar Genomics, Korea Polar Research Institute, Incheon, Korea.

Icefishes (suborder Notothenioidei; family Channichthyidae) are the only vertebrates that lack functional haemoglobin genes and red blood cells. Here, we report a high-quality genome assembly and linkage map for the Antarctic blackfin icefish Chaenocephalus aceratus, highlighting evolved genomic features for its unique physiology. Phylogenomic analysis revealed that Antarctic fish of the teleost suborder Notothenioidei, including icefishes, diverged from the stickleback lineage about 77 million years ago and subsequently evolved cold-adapted phenotypes as the Southern Ocean cooled to sub-zero temperatures. Our results show that genes involved in protection from ice damage, including genes encoding antifreeze glycoprotein and zona pellucida proteins, are highly expanded in the icefish genome. Furthermore, genes that encode enzymes that help to control cellular redox state, including members of the sod3 and nqo1 gene families, are expanded, probably as evolutionary adaptations to the relatively high concentration of oxygen dissolved in cold Antarctic waters. In contrast, some crucial regulators of circadian homeostasis (cry and per genes) are absent from the icefish genome, suggesting compromised control of biological rhythms in the polar light environment. The availability of the icefish genome sequence will accelerate our understanding of adaptation to extreme Antarctic environments.
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http://dx.doi.org/10.1038/s41559-019-0812-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7307600PMC
March 2019

Comparison of Xiphophorus and human melanoma transcriptomes reveals conserved pathway interactions.

Pigment Cell Melanoma Res 2018 07 29;31(4):496-508. Epub 2018 Jan 29.

The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, San Marcos, TX, USA.

Comparative analysis of human and animal model melanomas can uncover conserved pathways and genetic changes that are relevant for the biology of cancer cells. Spontaneous melanoma in Xiphophorus interspecies backcross hybrid progeny may be informative in identifying genes and functional pathways that are similarly related to melanoma development in all vertebrates, including humans. To assess functional pathways involved in the Xiphophorus melanoma, we performed gene expression profiling of the melanomas produced in interspecies BC and successive backcross generations (i.e., BC ) of the cross: X. hellerii × [X. maculatus Jp 163 A × X. hellerii]. Using RNA-Seq, we identified genes that are transcriptionally co-expressed with the driver oncogene, xmrk. We determined functional pathways in the fish melanoma that are also present in human melanoma cohorts that may be related to dedifferentiation based on the expression levels of pigmentation genes. Shared pathways between human and Xiphophorus melanomas are related to inflammation, cell migration, cell proliferation, pigmentation, cancer development, and metastasis. Our results suggest xmrk co-expressed genes are associated with dedifferentiation and highlight these signaling pathways as playing important roles in melanomagenesis.
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http://dx.doi.org/10.1111/pcmr.12686DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6013346PMC
July 2018

Cold Fusion: Massive Karyotype Evolution in the Antarctic Bullhead Notothen .

G3 (Bethesda) 2017 07 5;7(7):2195-2207. Epub 2017 Jul 5.

Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403

Half of all vertebrate species share a series of chromosome fusions that preceded the teleost genome duplication (TGD), but we do not understand the causative evolutionary mechanisms. The "Robertsonian-translocation hypothesis" suggests a regular fusion of each ancestral acro- or telocentric chromosome to just one other by centromere fusions, thus halving the karyotype. An alternative "genome-stirring hypothesis" posits haphazard and repeated fusions, inversions, and reciprocal and nonreciprocal translocations. To study large-scale karyotype reduction, we investigated the decrease of chromosome numbers in Antarctic notothenioid fish. Most notothenioids have 24 haploid chromosomes, but bullhead notothen () has 11. To understand mechanisms, we made a RAD-tag meiotic map with ∼10,000 polymorphic markers. Comparative genomics aligned about a thousand orthologs of platyfish and stickleback genes along bullhead chromosomes. Results revealed that 9 of 11 bullhead chromosomes arose by fusion of just two ancestral chromosomes and two others by fusion of three ancestral chromosomes. All markers from each ancestral chromosome remained contiguous, implying no inversions across fusion borders. Karyotype comparisons support a history of: (1) Robertsonian fusions of 22 ancestral chromosomes in pairs to yield 11 fused plus two small unfused chromosomes, like ; (2) fusion of one of the remaining two ancestral chromosomes to a preexisting fused pair, giving 12 chromosomes like ; and (3) fusion of the remaining ancestral chromosome to another fused pair, giving 11 chromosomes in These results raise the question of what selective forces promoted the systematic fusion of chromosomes in pairs and the suppression of pericentric inversions in this lineage, and provide a model for chromosome fusions in stem teleosts.
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http://dx.doi.org/10.1534/g3.117.040063DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5498148PMC
July 2017

Molecular genetic analysis of the melanoma regulatory locus in Xiphophorus interspecies hybrids.

Mol Carcinog 2017 08 13;56(8):1935-1944. Epub 2017 Apr 13.

The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, San Marcos, Texas.

Development of spontaneous melanoma in Xiphophorus interspecies backcross hybrid progeny, (X. hellerii × [X. maculatus Jp 163 A × X. hellerii]) is due to Mendelian segregation of a oncogene (xmrk) and a molecularly uncharacterized locus, called R(Diff), on LG5. R(Diff) is thought to suppresses the activity of xmrk in healthy X. maculatus Jp 163 A parental species that rarely develop melanoma. To better understand the molecular genetics of R(Diff), we utilized RNA-Seq to study allele-specific gene expression of spontaneous melanoma tumors and corresponding normal skin samples derived from 15 first generation backcross (BC ) hybrids and 13 fifth generation (BC ) hybrids. Allele-specific expression was determined for all genes and assigned to parental allele inheritance for each backcross hybrid individual. Results showed that genes residing in a 5.81 Mbp region on LG5 were exclusively expressed from the X. hellerii alleles in tumor-bearing BC hybrids. This observation indicates this region is consistently homozygous for X. hellerii alleles in tumor bearing animals, and therefore defines this region to be the R(Diff) locus. The R(Diff) locus harbors 164 gene models and includes the previously characterized R(Diff) candidate, cdkn2x. Twenty-one genes in the R(Diff) region show differential expression in the tumor samples compared to normal skin tissue. These results further characterize the R(Diff) locus and suggest tumor suppression may require a multigenic region rather than a single gene variant. Differences in gene expression between tumor and normal skin tissue in this region may indicate interactions among several genes are required for backcross hybrid melanoma development.
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http://dx.doi.org/10.1002/mc.22651DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5767473PMC
August 2017

The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons.

Nat Genet 2016 Apr 7;48(4):427-37. Epub 2016 Mar 7.

Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.

To connect human biology to fish biomedical models, we sequenced the genome of spotted gar (Lepisosteus oculatus), whose lineage diverged from teleosts before teleost genome duplication (TGD). The slowly evolving gar genome has conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization and development (mediated, for example, by Hox, ParaHox and microRNA genes). Numerous conserved noncoding elements (CNEs; often cis regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles for such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses showed that the sums of expression domains and expression levels for duplicated teleost genes often approximate the patterns and levels of expression for gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes and the function of human regulatory sequences.
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http://dx.doi.org/10.1038/ng.3526DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4817229PMC
April 2016

A Genetic Map for the Only Self-Fertilizing Vertebrate.

G3 (Bethesda) 2016 04 7;6(4):1095-106. Epub 2016 Apr 7.

Graduate School of Fisheries Science and Environmental Studies, Nagasaki University, 852-8521, Japan

The mangrove killifish Kryptolebias marmoratus, and its close relative Kryptolebias hermaphroditus, are the only vertebrate species known to reproduce by self-fertilization due to functional ovotestis development. To improve our understanding of their genomes, we constructed a genetic map. First, a single F1 fish was made by artificial fertilization between K. marmoratus and K. hermaphroditus strains. F2 progeny were then obtained by self-fertilization of the F1 fish. We used RAD-seq to query genomic DNAs from the two parental strains, the F1 individual and 49 F2 progeny. Results identified 9904 polymorphic RAD-tags (DNA markers) that mapped to 24 linkage groups, corresponding to the haploid chromosome number of these species. The total length of the map was 1248 cM, indicating that about one recombination occurred for each of the 24 homologous chromosome pairs in each meiosis. Markers were not evenly distributed along the chromosomes: in all chromosomes, many markers (> 8% of the total markers for each chromosome) mapped to chromosome tips. Centromeres suppress recombination, and this uneven distribution is probably due to the species' acrocentric chromosomes. Mapped marker sequences were compared to genomic sequences of medaka and platyfish, the next most closely related species with sequenced genomes that are anchored to genetic maps. Results showed that each mangrove killifish chromosome corresponds to a single chromosome of both platyfish and medaka, suggesting strong conservation of chromosomes over 100 million years of evolution. Our genetic map provides a framework for the K. marmoratus/K. hermaphroditus genome sequence and an important resource for understanding the biology of hermaphroditism.
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http://dx.doi.org/10.1534/g3.115.022699DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4825644PMC
April 2016

Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains.

Genetics 2014 Nov 18;198(3):1291-308. Epub 2014 Sep 18.

Institute of Neuroscience, University of Oregon, Eugene Oregon 97403

Sex determination can be robustly genetic, strongly environmental, or genetic subject to environmental perturbation. The genetic basis of sex determination is unknown for zebrafish (Danio rerio), a model for development and human health. We used RAD-tag population genomics to identify sex-linked polymorphisms. After verifying this "RAD-sex" method on medaka (Oryzias latipes), we studied two domesticated zebrafish strains (AB and TU), two natural laboratory strains (WIK and EKW), and two recent isolates from nature (NA and CB). All four natural strains had a single sex-linked region at the right tip of chromosome 4, enabling sex genotyping by PCR. Genotypes for the single nucleotide polymorphism (SNP) with the strongest statistical association to sex suggested that wild zebrafish have WZ/ZZ sex chromosomes. In natural strains, "male genotypes" became males and some "female genotypes" also became males, suggesting that the environment or genetic background can cause female-to-male sex reversal. Surprisingly, TU and AB lacked detectable sex-linked loci. Phylogenomics rooted on D. nigrofasciatus verified that all strains are monophyletic. Because AB and TU branched as a monophyletic clade, we could not rule out shared loss of the wild sex locus in a common ancestor despite their independent domestication. Mitochondrial DNA sequences showed that investigated strains represent only one of the three identified zebrafish haplogroups. Results suggest that zebrafish in nature possess a WZ/ZZ sex-determination mechanism with a major determinant lying near the right telomere of chromosome 4 that was modified during domestication. Strains providing the zebrafish reference genome lack key components of the natural sex-determination system but may have evolved variant sex-determining mechanisms during two decades in laboratory culture.
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http://dx.doi.org/10.1534/genetics.114.169284DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4224167PMC
November 2014

A RAD-tag genetic map for the platyfish (Xiphophorus maculatus) reveals mechanisms of karyotype evolution among teleost fish.

Genetics 2014 Jun 2;197(2):625-41. Epub 2014 Apr 2.

Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403

Mammalian genomes can vary substantially in haploid chromosome number even within a small taxon (e.g., 3-40 among deer alone); in contrast, teleost fish genomes are stable (24-25 in 58% of teleosts), but we do not yet understand the mechanisms that account for differences in karyotype stability. Among perciform teleosts, platyfish (Xiphophorus maculatus) and medaka (Oryzias latipes) both have 24 chromosome pairs, but threespine stickleback (Gasterosteus aculeatus) and green pufferfish (Tetraodon nigroviridis) have just 21 pairs. To understand the evolution of teleost genomes, we made a platyfish meiotic map containing 16,114 mapped markers scored on 267 backcross fish. We tiled genomic contigs along the map to create chromosome-length genome assemblies. Genome-wide comparisons of conserved synteny showed that platyfish and medaka karyotypes remained remarkably similar with few interchromosomal translocations but with numerous intrachromosomal rearrangements (transpositions and inversions) since their lineages diverged ∼120 million years ago. Comparative genomics with platyfish shows how reduced chromosome numbers in stickleback and green pufferfish arose by fusion of pairs of ancestral chromosomes after their lineages diverged from platyfish ∼195 million years ago. Zebrafish and human genomes provide outgroups to root observed changes. These studies identify likely genome assembly errors, characterize chromosome fusion events, distinguish lineage-independent chromosome fusions, show that the teleost genome duplication does not appear to have accelerated the rate of translocations, and reveal the stability of syntenies and gene orders in teleost chromosomes over hundreds of millions of years.
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http://dx.doi.org/10.1534/genetics.114.164293DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063920PMC
June 2014

Stacks: an analysis tool set for population genomics.

Mol Ecol 2013 Jun 24;22(11):3124-40. Epub 2013 May 24.

Institute of Ecology and Evolution, University of Oregon, Eugene, OR 97403-5289, USA.

Massively parallel short-read sequencing technologies, coupled with powerful software platforms, are enabling investigators to analyse tens of thousands of genetic markers. This wealth of data is rapidly expanding and allowing biological questions to be addressed with unprecedented scope and precision. The sizes of the data sets are now posing significant data processing and analysis challenges. Here we describe an extension of the Stacks software package to efficiently use genotype-by-sequencing data for studies of populations of organisms. Stacks now produces core population genomic summary statistics and SNP-by-SNP statistical tests. These statistics can be analysed across a reference genome using a smoothed sliding window. Stacks also now provides several output formats for several commonly used downstream analysis packages. The expanded population genomics functions in Stacks will make it a useful tool to harness the newest generation of massively parallel genotyping data for ecological and evolutionary genetics.
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http://dx.doi.org/10.1111/mec.12354DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3936987PMC
June 2013

The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits.

Nat Genet 2013 May 31;45(5):567-72. Epub 2013 Mar 31.

Physiological Chemistry, University of Würzburg, Biozentrum, Am Hubland, Würzburg, Germany.

Several attributes intuitively considered to be typical mammalian features, such as complex behavior, live birth and malignant disease such as cancer, also appeared several times independently in lower vertebrates. The genetic mechanisms underlying the evolution of these elaborate traits are poorly understood. The platyfish, X. maculatus, offers a unique model to better understand the molecular biology of such traits. We report here the sequencing of the platyfish genome. Integrating genome assembly with extensive genetic maps identified an unexpected evolutionary stability of chromosomes in fish, in contrast to in mammals. Genes associated with viviparity show signatures of positive selection, identifying new putative functional domains and rare cases of parallel evolution. We also find that genes implicated in cognition show an unexpectedly high rate of duplicate gene retention after the teleost genome duplication event, suggesting a hypothesis for the evolution of the behavioral complexity in fish, which exceeds that found in amphibians and reptiles.
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http://dx.doi.org/10.1038/ng.2604DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3677569PMC
May 2013

Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics.

PLoS One 2012 9;7(7):e40701. Epub 2012 Jul 9.

Institute of Neuroscience, University of Oregon, Eugene, Oregon, United States of America.

Within vertebrates, major sex determining genes can differ among taxa and even within species. In zebrafish (Danio rerio), neither heteromorphic sex chromosomes nor single sex determination genes of large effect, like Sry in mammals, have yet been identified. Furthermore, environmental factors can influence zebrafish sex determination. Although progress has been made in understanding zebrafish gonad differentiation (e.g. the influence of germ cells on gonad fate), the primary genetic basis of zebrafish sex determination remains poorly understood. To identify genetic loci associated with sex, we analyzed F(2) offspring of reciprocal crosses between Oregon *AB and Nadia (NA) wild-type zebrafish stocks. Genome-wide linkage analysis, using more than 5,000 sequence-based polymorphic restriction site associated (RAD-tag) markers and population genomic analysis of more than 30,000 single nucleotide polymorphisms in our *ABxNA crosses revealed a sex-associated locus on the end of the long arm of chr-4 for both cross families, and an additional locus in the middle of chr-3 in one cross family. Additional sequencing showed that two SNPs in dmrt1 previously suggested to be functional candidates for sex determination in a cross of ABxIndia wild-type zebrafish, are not associated with sex in our AB fish. Our data show that sex determination in zebrafish is polygenic and that different genes may influence sex determination in different strains or that different genes become more important under different environmental conditions. The association of the end of chr-4 with sex is remarkable because, unique in the karyotype, this chromosome arm shares features with known sex chromosomes: it is highly heterochromatic, repetitive, late replicating, and has reduced recombination. Our results reveal that chr-4 has functional and structural properties expected of a sex chromosome.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0040701PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3392230PMC
January 2013

Evolution of the osteoblast: skeletogenesis in gar and zebrafish.

BMC Evol Biol 2012 Mar 5;12:27. Epub 2012 Mar 5.

Institute of Neuroscience, University of Oregon, Eugene, OR 97403-1254, USA.

Background: Although the vertebrate skeleton arose in the sea 500 million years ago, our understanding of the molecular fingerprints of chondrocytes and osteoblasts may be biased because it is informed mainly by research on land animals. In fact, the molecular fingerprint of teleost osteoblasts differs in key ways from that of tetrapods, but we do not know the origin of these novel gene functions. They either arose as neofunctionalization events after the teleost genome duplication (TGD), or they represent preserved ancestral functions that pre-date the TGD. Here, we provide evolutionary perspective to the molecular fingerprints of skeletal cells and assess the role of genome duplication in generating novel gene functions. We compared the molecular fingerprints of skeletogenic cells in two ray-finned fish: zebrafish (Danio rerio)--a teleost--and the spotted gar (Lepisosteus oculatus)--a "living fossil" representative of a lineage that diverged from the teleost lineage prior to the TGD (i.e., the teleost sister group). We analyzed developing embryos for expression of the structural collagen genes col1a2, col2a1, col10a1, and col11a2 in well-formed cartilage and bone, and studied expression of skeletal regulators, including the transcription factor genes sox9 and runx2, during mesenchymal condensation.

Results: Results provided no evidence for the evolution of novel functions among gene duplicates in zebrafish compared to the gar outgroup, but our findings shed light on the evolution of the osteoblast. Zebrafish and gar chondrocytes both expressed col10a1 as they matured, but both species' osteoblasts also expressed col10a1, which tetrapod osteoblasts do not express. This novel finding, along with sox9 and col2a1 expression in developing osteoblasts of both zebrafish and gar, demonstrates that osteoblasts of both a teleost and a basally diverging ray-fin fish express components of the supposed chondrocyte molecular fingerprint.

Conclusions: Our surprising finding that the "chondrogenic" transcription factor sox9 is expressed in developing osteoblasts of both zebrafish and gar can help explain the expression of chondrocyte genes in osteoblasts of ray-finned fish. More broadly, our data suggest that the molecular fingerprint of the osteoblast, which largely is constrained among land animals, was not fixed during early vertebrate evolution.
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http://dx.doi.org/10.1186/1471-2148-12-27DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3314580PMC
March 2012

Stacks: building and genotyping Loci de novo from short-read sequences.

G3 (Bethesda) 2011 Aug 1;1(3):171-82. Epub 2011 Aug 1.

Advances in sequencing technology provide special opportunities for genotyping individuals with speed and thrift, but the lack of software to automate the calling of tens of thousands of genotypes over hundreds of individuals has hindered progress. Stacks is a software system that uses short-read sequence data to identify and genotype loci in a set of individuals either de novo or by comparison to a reference genome. From reduced representation Illumina sequence data, such as RAD-tags, Stacks can recover thousands of single nucleotide polymorphism (SNP) markers useful for the genetic analysis of crosses or populations. Stacks can generate markers for ultra-dense genetic linkage maps, facilitate the examination of population phylogeography, and help in reference genome assembly. We report here the algorithms implemented in Stacks and demonstrate their efficacy by constructing loci from simulated RAD-tags taken from the stickleback reference genome and by recapitulating and improving a genetic map of the zebrafish, Danio rerio.
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http://dx.doi.org/10.1534/g3.111.000240DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3276136PMC
August 2011

Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication.

Genetics 2011 Aug;188(4):799-808

Institute of Neuroscience. University of Oregon, Eugene, Oregon 97403, USA.

Genomic resources for hundreds of species of evolutionary, agricultural, economic, and medical importance are unavailable due to the expense of well-assembled genome sequences and difficulties with multigenerational studies. Teleost fish provide many models for human disease but possess anciently duplicated genomes that sometimes obfuscate connectivity. Genomic information representing a fish lineage that diverged before the teleost genome duplication (TGD) would provide an outgroup for exploring the mechanisms of evolution after whole-genome duplication. We exploited massively parallel DNA sequencing to develop meiotic maps with thrift and speed by genotyping F(1) offspring of a single female and a single male spotted gar (Lepisosteus oculatus) collected directly from nature utilizing only polymorphisms existing in these two wild individuals. Using Stacks, software that automates the calling of genotypes from polymorphisms assayed by Illumina sequencing, we constructed a map containing 8406 markers. RNA-seq on two map-cross larvae provided a reference transcriptome that identified nearly 1000 mapped protein-coding markers and allowed genome-wide analysis of conserved synteny. Results showed that the gar lineage diverged from teleosts before the TGD and its genome is organized more similarly to that of humans than teleosts. Thus, spotted gar provides a critical link between medical models in teleost fish, to which gar is biologically similar, and humans, to which gar is genomically similar. Application of our F(1) dense mapping strategy to species with no prior genome information promises to facilitate comparative genomics and provide a scaffold for ordering the numerous contigs arising from next generation genome sequencing.
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http://dx.doi.org/10.1534/genetics.111.127324DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3176089PMC
August 2011

Identification of transcriptome SNPs between Xiphophorus lines and species for assessing allele specific gene expression within F₁ interspecies hybrids.

Comp Biochem Physiol C Toxicol Pharmacol 2012 Jan 3;155(1):102-8. Epub 2011 Apr 3.

Department of Chemistry and Biochemistry, 419 Centennial Hall, Texas State University, 601 University Drive, San Marcos, TX 78666, USA.

Variations in gene expression are essential for the evolution of novel phenotypes and for speciation. Studying allelic specific gene expression (ASGE) within interspecies hybrids provides a unique opportunity to reveal underlying mechanisms of genetic variation. Using Xiphophorus interspecies hybrid fishes and high-throughput next generation sequencing technology, we were able to assess variations between two closely related vertebrate species, Xiphophorus maculatus and Xiphophorus couchianus, and their F(1) interspecies hybrids. We constructed transcriptome-wide SNP polymorphism sets between two highly inbred X. maculatus lines (JP 163 A and B), and between X. maculatus and a second species, X. couchianus. The X. maculatus JP 163 A and B parental lines have been separated in the laboratory for ≈70 years and we were able to identify SNPs at a resolution of 1 SNP per 49 kb of transcriptome. In contrast, SNP polymorphisms between X. couchianus and X. maculatus species, which diverged ≈5-10 million years ago, were identified about every 700 bp. Using 6524 transcripts with identified SNPs between the two parental species (X. maculatus and X. couchianus), we mapped RNA-seq reads to determine ASGE within F(1) interspecies hybrids. We developed an in silico X. couchianus transcriptome by replacing 90,788 SNP bases for X. maculatus transcriptome with the consensus X. couchianus SNP bases and provide evidence that this procedure overcomes read mapping biases. Employment of the in silico reference transcriptome and tolerating 5 mismatches during read mapping allow direct assessment of ASGE in the F(1) interspecies hybrids. Overall, these results show that Xiphophorus is a tractable vertebrate experimental model to investigate how genetic variations that occur during speciation may affect gene interactions and the regulation of gene expression.
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http://dx.doi.org/10.1016/j.cbpc.2011.03.012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3178741PMC
January 2012

Evolution of developmental regulation in the vertebrate FgfD subfamily.

J Exp Zool B Mol Dev Evol 2010 Jan;314(1):33-56

Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, Oregon, USA.

Fibroblast growth factors (Fgfs) encode small signaling proteins that help regulate embryo patterning. Fgfs fall into seven families, including FgfD. Nonvertebrate chordates have a single FgfD gene; mammals have three (Fgf8, Fgf17, and Fgf18); and teleosts have six (fgf8a, fgf8b, fgf17, fgf18a, fgf18b, and fgf24). What are the evolutionary processes that led to the structural duplication and functional diversification of FgfD genes during vertebrate phylogeny? To study this question, we investigated conserved syntenies, patterns of gene expression, and the distribution of conserved noncoding elements (CNEs) in FgfD genes of stickleback and zebrafish, and compared them with data from cephalochordates, urochordates, and mammals. Genomic analysis suggests that Fgf8, Fgf17, Fgf18, and Fgf24 arose in two rounds of whole genome duplication at the base of the vertebrate radiation; that fgf8 and fgf18 duplications occurred at the base of the teleost radiation; and that Fgf24 is an ohnolog that was lost in the mammalian lineage. Expression analysis suggests that ancestral subfunctions partitioned between gene duplicates and points to the evolution of novel expression domains. Analysis of CNEs, at least some of which are candidate regulatory elements, suggests that ancestral CNEs partitioned between gene duplicates. These results help explain the evolutionary pathways by which the developmentally important family of FgfD molecules arose and the deduced principles that guided FgfD evolution are likely applicable to the evolution of developmental regulation in many vertebrate multigene families.
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http://dx.doi.org/10.1002/jez.b.21307DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3092526PMC
January 2010

Duplication and divergence of fgf8 functions in teleost development and evolution.

J Exp Zool B Mol Dev Evol 2007 Dec;308(6):730-43

Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, USA.

Fibroblast growth factors play critical roles in many aspects of embryo patterning that are conserved across broad phylogenetic distances. To help understand the evolution of fibroblast growth factor functions, we identified members of the Fgf8/17/18-subfamily in the three-spine stickleback Gasterosteus aculeatus, and investigated their evolutionary relationships and expression patterns. We found that fgf17b is the ortholog of tetrapod Fgf17, whereas the teleost genes called fgf8 and fgf17a are duplicates of the tetrapod gene Fgf8, and thus should be called fgf8a and fgf8b. Phylogenetic analysis supports the view that the Fgf8/17/18-subfamily expanded during the ray-fin fish genome duplication. In situ hybridization experiments showed that stickleback fgf8 duplicates exhibited common and unique expression patterns, indicating that tissue specialization followed the gene duplication event. Moreover, direct comparison of stickleback and zebrafish embryonic expression patterns of fgf8 co-orthologs suggested lineage-specific independent subfunction partitioning and the acquisition or the loss of ortholog functions. In tetrapods, Fgf8 plays an important role in the apical ectodermal ridge of the developing pectoral appendage. Surprisingly, differences in the expression of fgf8a in the apical ectodermal ridge of the pectoral fin bud in zebrafish and stickleback, coupled with the role of fgf16 and fgf24 in teleost pectoral appendage show that different Fgf genes may play similar roles in limb development in various vertebrates.
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http://dx.doi.org/10.1002/jez.b.21193DOI Listing
December 2007

Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers.

Genome Res 2007 Feb 22;17(2):240-8. Epub 2006 Dec 22.

Institute for Molecular Biology, University of Oregon, Eugene, Oregon 97403, USA.

Restriction site associated DNA (RAD) tags are a genome-wide representation of every site of a particular restriction enzyme by short DNA tags. Most organisms segregate large numbers of DNA sequence polymorphisms that disrupt restriction sites, which allows RAD tags to serve as genetic markers spread at a high density throughout the genome. Here, we demonstrate the applicability of RAD markers for both individual and bulk-segregant genotyping. First, we show that these markers can be identified and typed on pre-existing microarray formats. Second, we present a method that uses RAD marker DNA to rapidly produce a low-cost microarray genotyping resource that can be used to efficiently identify and type thousands of RAD markers. We demonstrate the utility of the former approach by using a tiling path array for the fruit fly to map a recombination breakpoint, and the latter approach by creating and using an enriched RAD marker array for the threespine stickleback. The high number of RAD markers enabled localization of a previously identified region, as well as a second region also associated with the lateral plate phenotype. Taken together, our results demonstrate that RAD markers, and the method to develop a RAD marker microarray resource, allow high-throughput, high-resolution genotyping in both model and nonmodel systems.
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http://dx.doi.org/10.1101/gr.5681207DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1781356PMC
February 2007

Stereospecificity and PAX6 function direct Hoxd4 neural enhancer activity along the antero-posterior axis.

Dev Biol 2006 Nov 30;299(2):582-93. Epub 2006 Aug 30.

McGill Cancer Centre, McGill University, 3655 Promenade Sir-William-Osler, Montreal, QC, Canada H3G 1Y6.

The antero-posterior (AP) and dorso-ventral (DV) patterning of the neural tube is controlled in part by HOX and PAX transcription factors, respectively. We have reported on a neural enhancer of Hoxd4 that directs expression in the CNS with the correct anterior border in the hindbrain. Comparison to the orthologous enhancer of zebrafish revealed seven conserved footprints including an obligatory retinoic acid response element (RARE), and adjacent sites D, E and F. Whereas enhancer function in the embryonic CNS is destroyed by separation of the RARE from sites D-E-F by a half turn of DNA, it is rescued by one full turn, suggesting stereospecific constraints between DNA-bound retinoid receptors and the factor(s) recognizing sites D-E-F. Alterations in the DV trajectory of the Hoxd4 anterior expression border following mutation of site D or E implicated transcriptional regulators active across the DV axis. We show that PAX6 specifically binds sites D and E in vitro, and use chromatin immunoprecipitation to demonstrate recruitment of PAX6 to the Hoxd4 neural enhancer in mouse embryos. Hoxd4 expression throughout the CNS is reduced in Pax6 mutant Sey(Neu) animals on embryonic day 8. Additionally, stage-matched zebrafish embryos having decreased pax6a and/or pax6b activity display malformed rhombomere boundaries and an anteriorized hoxd4a expression border. These results reveal an evolutionarily conserved role for Pax6 in AP-restricted expression of vertebrate Hoxd4 orthologs.
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http://dx.doi.org/10.1016/j.ydbio.2006.08.061DOI Listing
November 2006

Developmental genetic basis for the evolution of pelvic fin loss in the pufferfish Takifugu rubripes.

Dev Biol 2005 May;281(2):227-39

Institute of Neuroscience, University of Oregon, Eugene, OR 97403, USA.

Paired appendages were a key developmental innovation among vertebrates and they eventually evolved into limbs. Ancient developmental control systems for paired fins and limbs are broadly conserved among gnathostome vertebrates. Some lineages including whales, some salamanders, snakes, and many ray-fin fish, independently lost the pectoral, pelvic, or both appendages over evolutionary time. When different taxa independently evolve similar developmental morphologies, do they use the same molecular genetic mechanisms? To determine the developmental genetic basis for the evolution of pelvis loss in the pufferfish Takifugu rubripes (fugu), we isolated fugu orthologs of genes thought to be essential for limb development in tetrapods, including limb positioning (Hoxc6, Hoxd9), limb bud initiation (Pitx1, Tbx4, Tbx5), and limb bud outgrowth (Shh, Fgf10), and studied their expression patterns during fugu development. Results showed that bud outgrowth and initiation fail to occur in fugu, and that pelvis loss is associated with altered expression of Hoxd9a, which we show to be a marker for pelvic fin position in three-spine stickleback Gasterosteus aculeatus. These results rule out changes in appendage outgrowth and initiation genes as the earliest developmental defect in pufferfish pelvic fin loss and suggest that altered Hoxd9a expression in the lateral mesoderm may account for pelvis loss in fugu. This mechanism appears to be different from the mechanism for pelvic loss in stickleback, showing that different taxa can evolve similar phenotypes by different mechanisms.
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http://dx.doi.org/10.1016/j.ydbio.2005.02.016DOI Listing
May 2005

Subfunction partitioning, the teleost radiation and the annotation of the human genome.

Trends Genet 2004 Oct;20(10):481-90

Institute of Neuroscience, University of Oregon, Eugene, OR 97403, USA.

Half of all vertebrate species are teleost fish. What accounts for this explosion of biodiversity? Recent evidence and advances in evolutionary theory suggest that genomic features could have played a significant role in the teleost radiation. This review examines evidence for an ancient whole-genome duplication (tetraploidization) event that probably occurred just before the teleost radiation. The partitioning of ancestral subfunctions between gene copies arising from this duplication could have contributed to the genetic isolation of populations, to lineage-specific diversification of developmental programs, and ultimately to phenotypic variation among teleost fish. Beyond its importance for understanding mechanisms that generate biodiversity, the partitioning of subfunctions between teleost co-orthologs of human genes can facilitate the identification of tissue-specific conserved noncoding regions and can simplify the analysis of ancestral gene functions obscured by pleiotropy or haploinsufficiency. Applying these principles on a genomic scale can accelerate the functional annotation of the human genome and understanding of the roles of human genes in health and disease.
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http://dx.doi.org/10.1016/j.tig.2004.08.001DOI Listing
October 2004

Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations.

Proc Natl Acad Sci U S A 2004 Apr 6;101(16):6050-5. Epub 2004 Apr 6.

Institute of Neuroscience and Center for Ecology and Evolutionary Biology, University of Oregon, Eugene, OR 97403-1254, USA.

Most adaptation is thought to occur through the fixation of numerous alleles at many different loci. Consequently, the independent evolution of similar phenotypes is predicted to occur through different genetic mechanisms. The genetic basis of adaptation is still largely unknown, however, and it is unclear whether adaptation to new environments utilizes ubiquitous small-effect polygenic variation or large-effect alleles at a small number of loci. To address this question, we examined the genetic basis of bony armor loss in three freshwater populations of Alaskan threespine stickleback, Gasterosteus aculeatus, that evolved from fully armored anadromous populations in the last 14,000 years. Crosses between complete-armor and low-armor populations revealed that a single Mendelian factor governed the formation of all but the most anterior lateral plates, and another independently segregating factor largely determined pelvic armor. Genetic mapping localized the Mendelian genes to different chromosomal regions, and crosses among these same three widely separated populations showed that both bony plates and pelvic armor failed to fully complement, implicating the same Mendelian armor reduction genes. Thus, rapid and repeated armor loss in Alaskan stickleback populations appears to be occurring through the fixation of large-effect variants in the same genes.
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http://dx.doi.org/10.1073/pnas.0308479101DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC395921PMC
April 2004