Publications by authors named "Alexander Nater"

30 Publications

  • Page 1 of 1

Genome sequences reveal global dispersal routes and suggest convergent genetic adaptations in seahorse evolution.

Nat Commun 2021 02 17;12(1):1094. Epub 2021 Feb 17.

CAS Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences, Guangzhou, China.

Seahorses have a circum-global distribution in tropical to temperate coastal waters. Yet, seahorses show many adaptations for a sedentary, cryptic lifestyle: they require specific habitats, such as seagrass, kelp or coral reefs, lack pelvic and caudal fins, and give birth to directly developed offspring without pronounced pelagic larval stage, rendering long-range dispersal by conventional means inefficient. Here we investigate seahorses' worldwide dispersal and biogeographic patterns based on a de novo genome assembly of Hippocampus erectus as well as 358 re-sequenced genomes from 21 species. Seahorses evolved in the late Oligocene and subsequent circum-global colonization routes are identified and linked to changing dynamics in ocean currents and paleo-temporal seaway openings. Furthermore, the genetic basis of the recurring "bony spines" adaptive phenotype is linked to independent substitutions in a key developmental gene. Analyses thus suggest that rafting via ocean currents compensates for poor dispersal and rapid adaptation facilitates colonizing new habitats.
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http://dx.doi.org/10.1038/s41467-021-21379-xDOI Listing
February 2021

The comparative genomic landscape of adaptive radiation in crater lake cichlid fishes.

Mol Ecol 2021 02 6;30(4):955-972. Epub 2021 Jan 6.

Department of Biology, University of Konstanz, Konstanz, Germany.

Factors ranging from ecological opportunity to genome composition might explain why only some lineages form adaptive radiations. While being rare, particular systems can provide natural experiments within an identical ecological setting where species numbers and phenotypic divergence in two closely related lineages are notably different. We investigated one such natural experiment using two de novo assembled and 40 resequenced genomes and asked why two closely related Neotropical cichlid fish lineages, the Amphilophus citrinellus species complex (Midas cichlids; radiating) and Archocentrus centrarchus (Flyer cichlid; nonradiating), have resulted in such disparate evolutionary outcomes. Although both lineages inhabit many of the same Nicaraguan lakes, whole-genome inferred demography suggests that priority effects are not likely to be the cause of the dissimilarities. Also, genome-wide levels of selection, transposable element dynamics, gene family expansion, major chromosomal rearrangements and the number of genes under positive selection were not markedly different between the two lineages. To more finely investigate particular subsets of the genome that have undergone adaptive divergence in Midas cichlids, we also examined if there was evidence for 'molecular pre-adaptation' in regions identified by QTL mapping of repeatedly diverging adaptive traits. Although most of our analyses failed to pinpoint substantial genomic differences, we did identify functional categories containing many genes under positive selection that provide candidates for future studies on the propensity of Midas cichlids to radiate. Our results point to a disproportionate role of local, rather than genome-wide factors underlying the propensity for these cichlid fishes to adaptively radiate.
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http://dx.doi.org/10.1111/mec.15774DOI Listing
February 2021

Contrasting signatures of genomic divergence during sympatric speciation.

Nature 2020 12 28;588(7836):106-111. Epub 2020 Oct 28.

Department of Biology, University of Konstanz, Konstanz, Germany.

The transition from 'well-marked varieties' of a single species into 'well-defined species'-especially in the absence of geographic barriers to gene flow (sympatric speciation)-has puzzled evolutionary biologists ever since Darwin. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.
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http://dx.doi.org/10.1038/s41586-020-2845-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7759464PMC
December 2020

Different Sources of Allelic Variation Drove Repeated Color Pattern Divergence in Cichlid Fishes.

Mol Biol Evol 2021 01;38(2):465-477

Department of Biology, University of Konstanz, Konstanz, Germany.

The adaptive radiations of East African cichlid fish in the Great Lakes Victoria, Malawi, and Tanganyika are well known for their diversity and repeatedly evolved phenotypes. Convergent evolution of melanic horizontal stripes has been linked to a single locus harboring the gene agouti-related peptide 2 (agrp2). However, where and when the causal variants underlying this trait evolved and how they drove phenotypic divergence remained unknown. To test the alternative hypotheses of standing genetic variation versus de novo mutations (independently originating in each radiation), we searched for shared signals of genomic divergence at the agrp2 locus. Although we discovered similar signatures of differentiation at the locus level, the haplotypes associated with stripe patterns are surprisingly different. In Lake Malawi, the highest associated alleles are located within and close to the 5' untranslated region of agrp2 and likely evolved through recent de novo mutations. In the younger Lake Victoria radiation, stripes are associated with two intronic regions overlapping with a previously reported cis-regulatory interval. The origin of these segregating haplotypes predates the Lake Victoria radiation because they are also found in more basal riverine and Lake Kivu species. This suggests that both segregating haplotypes were present as standing genetic variation at the onset of the Lake Victoria adaptive radiation with its more than 500 species and drove phenotypic divergence within the species flock. Therefore, both new (Lake Malawi) and ancient (Lake Victoria) allelic variation at the same locus fueled rapid and convergent phenotypic evolution.
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http://dx.doi.org/10.1093/molbev/msaa237DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7826197PMC
January 2021

Reconstructing the Evolutionary History of Chromosomal Races on Islands: A Genome-Wide Analysis of Natural House Mouse Populations.

Mol Biol Evol 2020 10;37(10):2825-2837

Department of Biology and Biotechnology "Charles Darwin," "La Sapienza" University of Rome, Rome, Italy.

Chromosomal evolution is widely considered to be an important driver of speciation, as karyotypic reorganization can bring about the establishment of reproductive barriers between incipient species. One textbook example for genetic mechanisms of speciation are large-scale chromosomal rearrangements such as Robertsonian (Rb) fusions, a common class of structural variants that can drastically change the recombination landscape by suppressing crossing-over and influence gene expression by altering regulatory networks. Here, we explore the population structure and demographic patterns of a well-known house mouse Rb system in the Aeolian archipelago in Southern Italy using genome-wide data. By analyzing chromosomal regions characterized by different levels of recombination, we trace the evolutionary history of a set of Rb chromosomes occurring in different geographical locations and test whether chromosomal fusions have a single shared origin or occurred multiple times. Using a combination of phylogenetic and population genetic approaches, we find support for multiple, independent origins of three focal Rb chromosomes. The elucidation of the demographic patterns of the mouse populations within the Aeolian archipelago shows that an interplay between fixation of newly formed Rb chromosomes and hybridization events has contributed to shaping their current karyotypic distribution. Overall, our results illustrate that chromosome structure is much more dynamic than anticipated and emphasize the importance of large-scale chromosomal translocations in speciation.
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http://dx.doi.org/10.1093/molbev/msaa118DOI Listing
October 2020

How Linked Selection Shapes the Diversity Landscape in Flycatchers.

Genetics 2019 05 14;212(1):277-285. Epub 2019 Mar 14.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36, Sweden.

There is an increasing awareness that selection affecting linked neutral sites strongly influences on how diversity is distributed across the genome. In particular, linked selection is likely involved in the formation of heterogenous landscapes of genetic diversity, including genomic regions with locally reduced effective population sizes that manifest as dips in diversity, and "islands" of differentiation between closely related populations or species. Linked selection can be in the form of background selection or selective sweeps, and a long-standing quest in population genetics has been to unveil the relative importance of these processes. Here, we analyzed the theoretically expected reduction of diversity caused by linked selection in the collared flycatcher () genome and compared this with population genomic data on the distribution of diversity across the flycatcher genome. By incorporating data on recombination rate variation and the density of target sites for selection (including both protein-coding genes and conserved noncoding elements), we found that background selection can explain most of the observed baseline variation in genetic diversity. However, positive selection was necessary to explain the pronounced local diversity dips in the collared flycatcher genome. We confirmed our analytical findings by comprehensive simulations. Therefore, our study demonstrates that even though both background selection and selective sweeps contribute to the heterogeneous diversity landscape seen in this avian system, they play different roles in shaping it.
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http://dx.doi.org/10.1534/genetics.119.301991DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6499528PMC
May 2019

Genomes reveal marked differences in the adaptive evolution between orangutan species.

Genome Biol 2018 11 15;19(1):193. Epub 2018 Nov 15.

Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057, Zürich, Switzerland.

Background: Integrating demography and adaptive evolution is pivotal to understanding the evolutionary history and conservation of great apes. However, little is known about the adaptive evolution of our closest relatives, in particular if and to what extent adaptions to environmental differences have occurred. Here, we used whole-genome sequencing data from critically endangered orangutans from North Sumatra (Pongo abelii) and Borneo (P. pygmaeus) to investigate adaptive responses of each species to environmental differences during the Pleistocene.

Results: Taking into account the markedly disparate demographic histories of each species after their split ~ 1 Ma ago, we show that persistent environmental differences on each island had a strong impact on the adaptive evolution of the genus Pongo. Across a range of tests for positive selection, we find a consistent pattern of between-island and species differences. In the more productive Sumatran environment, the most notable signals of positive selection involve genes linked to brain and neuronal development, learning, and glucose metabolism. On Borneo, however, positive selection comprised genes involved in lipid metabolism, as well as cardiac and muscle activities.

Conclusions: We find strikingly different sets of genes appearing to have evolved under strong positive selection in each species. In Sumatran orangutans, selection patterns were congruent with well-documented cognitive and behavioral differences between the species, such as a larger and more complex cultural repertoire and higher degrees of sociality. However, in Bornean orangutans, selective responses to fluctuating environmental conditions appear to have produced physiological adaptations to generally lower and temporally more unpredictable food supplies.
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http://dx.doi.org/10.1186/s13059-018-1562-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6237011PMC
November 2018

Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It.

Mol Biol Evol 2018 10;35(10):2475-2486

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

The rate of recombination impacts on rates of protein evolution for at least two reasons: it affects the efficacy of selection due to linkage and influences sequence evolution through the process of GC-biased gene conversion (gBGC). We studied how recombination, via gBGC, affects inferences of selection in gene sequences using comparative genomic and population genomic data from the collared flycatcher (Ficedula albicollis). We separately analyzed different mutation categories ("strong"-to-"weak," "weak-to-strong," and GC-conservative changes) and found that gBGC impacts on the distribution of fitness effects of new mutations, and leads to that the rate of adaptive evolution and the proportion of adaptive mutations among nonsynonymous substitutions are underestimated by 22-33%. It also biases inferences of demographic history based on the site frequency spectrum. In light of this impact, we suggest that inferences of selection (and demography) in lineages with pronounced gBGC should be based on GC-conservative changes only. Doing so, we estimate that 10% of nonsynonymous mutations are effectively neutral and that 27% of nonsynonymous substitutions have been fixed by positive selection in the flycatcher lineage. We also find that gene expression level, sex-bias in expression, and the number of protein-protein interactions, but not Hill-Robertson interference (HRI), are strong determinants of selective constraint and rate of adaptation of collared flycatcher genes. This study therefore illustrates the importance of disentangling the effects of different evolutionary forces and genetic factors in interpretation of sequence data, and from that infer the role of natural selection in DNA sequence evolution.
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http://dx.doi.org/10.1093/molbev/msy149DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6188562PMC
October 2018

Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species.

Curr Biol 2017 Nov 2;27(22):3487-3498.e10. Epub 2017 Nov 2.

Evolutionary Genetics Group, Department of Anthropology, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland. Electronic address:

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cub.2017.09.047DOI Listing
November 2017

Whole-genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine-scale recombination rate variation in birds.

Mol Ecol 2017 Aug 5;26(16):4158-4172. Epub 2017 Jul 5.

Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, Uppsala, Sweden.

Recombination rate is heterogeneous across the genome of various species and so are genetic diversity and differentiation as a consequence of linked selection. However, we still lack a clear picture of the underlying mechanisms for regulating recombination. Here we estimated fine-scale population recombination rate based on the patterns of linkage disequilibrium across the genomes of multiple populations of two closely related flycatcher species (Ficedula albicollis and F. hypoleuca). This revealed an overall conservation of the recombination landscape between these species at the scale of 200 kb, but we also identified differences in the local rate of recombination despite their recent divergence (<1 million years). Genetic diversity and differentiation were associated with recombination rate in a lineage-specific manner, indicating differences in the extent of linked selection between species. We detected 400-3,085 recombination hotspots per population. Location of hotspots was conserved between species, but the intensity of hotspot activity varied between species. Recombination hotspots were primarily associated with CpG islands (CGIs), regardless of whether CGIs were at promoter regions or away from genes. Recombination hotspots were also associated with specific transposable elements (TEs), but this association appears indirect due to shared preferences of the transposition machinery and the recombination machinery for accessible open chromatin regions. Our results suggest that CGIs are a major determinant of the localization of recombination hotspots, and we propose that both the distribution of TEs and fine-scale variation in recombination rate may be associated with the evolution of the epigenetic landscape.
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http://dx.doi.org/10.1111/mec.14197DOI Listing
August 2017

Evidence that the rate of strong selective sweeps increases with population size in the great apes.

Proc Natl Acad Sci U S A 2017 02 30;114(7):1613-1618. Epub 2017 Jan 30.

Bioinformatics Research Centre, Aarhus University, DK-8000 Aarhus C, Denmark;

Quantifying the number of selective sweeps and their combined effects on genomic diversity in humans and other great apes is notoriously difficult. Here we address the question using a comparative approach to contrast diversity patterns according to the distance from genes in all great ape taxa. The extent of diversity reduction near genes compared with the rest of intergenic sequences is greater in a species with larger effective population size. Also, the maximum distance from genes at which the diversity reduction is observed is larger in species with large effective population size. In Sumatran orangutans, the overall genomic diversity is ∼30% smaller than diversity levels far from genes, whereas this reduction is only 9% in humans. We show by simulation that selection against deleterious mutations in the form of background selection is not expected to cause these differences in diversity among species. Instead, selective sweeps caused by positive selection can reduce diversity level more severely in a large population if there is a higher number of selective sweeps per unit time. We discuss what can cause such a correlation, including the possibility that more frequent sweeps in larger populations are due to a shorter waiting time for the right mutations to arise.
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http://dx.doi.org/10.1073/pnas.1605660114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5320968PMC
February 2017

Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome.

Mol Ecol Resour 2017 Jul 14;17(4):586-597. Epub 2016 Nov 14.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36, Uppsala, Sweden.

Properly estimating genetic diversity in populations of nonmodel species requires a basic understanding of how diversity is distributed across the genome and among individuals. To this end, we analysed whole-genome resequencing data from 20 collared flycatchers (genome size ≈1.1 Gb; 10.13 million single nucleotide polymorphisms detected). Genomewide nucleotide diversity was almost identical among individuals (mean = 0.00394, range = 0.00384-0.00401), but diversity levels varied extensively across the genome (95% confidence interval for 200-kb windows = 0.0013-0.0053). Diversity was related to selective constraint such that in comparison with intergenic DNA, diversity at fourfold degenerate sites was reduced to 85%, 3' UTRs to 82%, 5' UTRs to 70% and nondegenerate sites to 12%. There was a strong positive correlation between diversity and chromosome size, probably driven by a higher density of targets for selection on smaller chromosomes increasing the diversity-reducing effect of linked selection. Simulations exploring the ability of sequence data from a small number of genetic markers to capture the observed diversity clearly demonstrated that diversity estimation from finite sampling of such data is bound to be associated with large confidence intervals. Nevertheless, we show that precision in diversity estimation in large outbred population benefits from increasing the number of loci rather than the number of individuals. Simulations mimicking RAD sequencing showed that this approach gives accurate estimates of genomewide diversity. Based on the patterns of observed diversity and the performed simulations, we provide broad recommendations for how genetic diversity should be estimated in natural populations.
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http://dx.doi.org/10.1111/1755-0998.12602DOI Listing
July 2017

Evolution and demography of the great apes.

Curr Opin Genet Dev 2016 Dec 4;41:124-129. Epub 2016 Oct 4.

Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), PRBB, Doctor Aiguader 88, Barcelona, Catalonia 08003, Spain; Institucio Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Catalonia 08010, Spain; CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. Electronic address:

The great apes are the closest living relatives of humans. Chimpanzees and bonobos group together with humans, while gorillas and orangutans are more divergent from humans. Here, we review insights into their evolution pertaining to the topology of species and subspecies and the reconstruction of their demography based on genome-wide variation. These advances have only become possible recently through next-generation sequencing technologies. Given the close relationship to humans, they provide an important evolutionary context for human genetics.
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http://dx.doi.org/10.1016/j.gde.2016.09.005DOI Listing
December 2016

Divergence in gene expression within and between two closely related flycatcher species.

Mol Ecol 2016 05 2;25(9):2015-28. Epub 2016 Apr 2.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden.

Relatively little is known about the character of gene expression evolution as species diverge. It is for instance unclear if gene expression generally evolves in a clock-like manner (by stabilizing selection or neutral evolution) or if there are frequent episodes of directional selection. To gain insights into the evolutionary divergence of gene expression, we sequenced and compared the transcriptomes of multiple organs from population samples of collared (Ficedula albicollis) and pied flycatchers (F. hypoleuca), two species which diverged less than one million years ago. Ordination analysis separated samples by organ rather than by species. Organs differed in their degrees of expression variance within species and expression divergence between species. Variance was negatively correlated with expression breadth and protein interactivity, suggesting that pleiotropic constraints reduce gene expression variance within species. Variance was correlated with between-species divergence, consistent with a pattern expected from stabilizing selection and neutral evolution. Using an expression PST approach, we identified genes differentially expressed between species and found 16 genes uniquely expressed in one of the species. For one of these, DPP7, uniquely expressed in collared flycatcher, the absence of expression in pied flycatcher could be associated with a ≈20-kb deletion including 11 of 13 exons. This study of a young vertebrate speciation model system expands our knowledge of how gene expression evolves as natural populations become reproductively isolated.
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http://dx.doi.org/10.1111/mec.13596DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4879514PMC
May 2016

Recombination Rate Variation Modulates Gene Sequence Evolution Mainly via GC-Biased Gene Conversion, Not Hill-Robertson Interference, in an Avian System.

Mol Biol Evol 2016 Jan 6;33(1):216-27. Epub 2015 Oct 6.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

The ratio of nonsynonymous to synonymous substitution rates (ω) is often used to measure the strength of natural selection. However, ω may be influenced by linkage among different targets of selection, that is, Hill-Robertson interference (HRI), which reduces the efficacy of selection. Recombination modulates the extent of HRI but may also affect ω by means of GC-biased gene conversion (gBGC), a process leading to a preferential fixation of G:C ("strong," S) over A:T ("weak," W) alleles. As HRI and gBGC can have opposing effects on ω, it is essential to understand their relative impact to make proper inferences of ω. We used a model that separately estimated S-to-S, S-to-W, W-to-S, and W-to-W substitution rates in 8,423 avian genes in the Ficedula flycatcher lineage. We found that the W-to-S substitution rate was positively, and the S-to-W rate negatively, correlated with recombination rate, in accordance with gBGC but not predicted by HRI. The W-to-S rate further showed the strongest impact on both dN and dS. However, since the effects were stronger at 4-fold than at 0-fold degenerated sites, likely because the GC content of these sites is farther away from its equilibrium, ω slightly decreases with increasing recombination rate, which could falsely be interpreted as a consequence of HRI. We corroborated this hypothesis analytically and demonstrate that under particular conditions, ω can decrease with increasing recombination rate. Analyses of the site-frequency spectrum showed that W-to-S mutations were skewed toward high, and S-to-W mutations toward low, frequencies, consistent with a prevalent gBGC-driven fixation bias.
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http://dx.doi.org/10.1093/molbev/msv214DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4693978PMC
January 2016

Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers.

Genome Res 2015 Nov 9;25(11):1656-65. Epub 2015 Sep 9.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;

Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(xy) and relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.
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http://dx.doi.org/10.1101/gr.196485.115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4617962PMC
November 2015

Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data.

Syst Biol 2015 Nov 17;64(6):1000-17. Epub 2015 Jul 17.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

Using genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. However, reconstructing the sequence of speciation events, the so-called species tree, in closely related and potentially hybridizing species is very challenging. Processes such as incomplete lineage sorting and interspecific gene flow result in local gene genealogies that differ in their topology from the species tree, and analyses of few loci with a single sequence per species are likely to produce conflicting or even misleading results. To study these phenomena on a full phylogenomic scale, we use whole-genome sequence data from 200 individuals of four black-and-white flycatcher species with so far unresolved phylogenetic relationships to infer gene tree topologies and visualize genome-wide patterns of gene tree incongruence. Using phylogenetic analysis in nonoverlapping 10-kb windows, we show that gene tree topologies are extremely diverse and change on a very small physical scale. Moreover, we find strong evidence for gene flow among flycatcher species, with distinct patterns of reduced introgression on the Z chromosome. To resolve species relationships on the background of widespread gene tree incongruence, we used four complementary coalescent-based methods for species tree reconstruction, including complex modeling approaches that incorporate post-divergence gene flow among species. This allowed us to infer the most likely species tree with high confidence. Based on this finding, we show that regions of reduced effective population size, which have been suggested as particularly useful for species tree inference, can produce positively misleading species tree topologies. Our findings disclose the pitfalls of using loci potentially under selection as phylogenetic markers and highlight the potential of modeling approaches to disentangle species relationships in systems with large effective population sizes and post-divergence gene flow.
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http://dx.doi.org/10.1093/sysbio/syv045DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4604831PMC
November 2015

Evolutionary analysis of the female-specific avian W chromosome.

Nat Commun 2015 Jun 4;6:7330. Epub 2015 Jun 4.

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden.

The typically repetitive nature of the sex-limited chromosome means that it is often excluded from or poorly covered in genome assemblies, hindering studies of evolutionary and population genomic processes in non-recombining chromosomes. Here, we present a draft assembly of the non-recombining region of the collared flycatcher W chromosome, containing 46 genes without evidence of female-specific functional differentiation. Survival of genes during W chromosome degeneration has been highly non-random and expression data suggest that this can be attributed to selection for maintaining gene dose and ancestral expression levels of essential genes. Re-sequencing of large population samples revealed dramatically reduced levels of within-species diversity and elevated rates of between-species differentiation (lineage sorting), consistent with low effective population size. Concordance between W chromosome and mitochondrial DNA phylogenetic trees demonstrates evolutionary stable matrilineal inheritance of this nuclear-cytonuclear pair of chromosomes. Our results show both commonalities and differences between W chromosome and Y chromosome evolution.
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http://dx.doi.org/10.1038/ncomms8330DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4468903PMC
June 2015

Reconstructing the demographic history of orang-utans using Approximate Bayesian Computation.

Mol Ecol 2015 Jan 9;24(2):310-27. Epub 2015 Jan 9.

Anthropological Institute & Museum, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.

Investigating how different evolutionary forces have shaped patterns of DNA variation within and among species requires detailed knowledge of their demographic history. Orang-utans, whose distribution is currently restricted to the South-East Asian islands of Borneo (Pongo pygmaeus) and Sumatra (Pongo abelii), have likely experienced a complex demographic history, influenced by recurrent changes in climate and sea levels, volcanic activities and anthropogenic pressures. Using the most extensive sample set of wild orang-utans to date, we employed an Approximate Bayesian Computation (ABC) approach to test the fit of 12 different demographic scenarios to the observed patterns of variation in autosomal, X-chromosomal, mitochondrial and Y-chromosomal markers. In the best-fitting model, Sumatran orang-utans exhibit a deep split of populations north and south of Lake Toba, probably caused by multiple eruptions of the Toba volcano. In addition, we found signals for a strong decline in all Sumatran populations ~24 ka, probably associated with hunting by human colonizers. In contrast, Bornean orang-utans experienced a severe bottleneck ~135 ka, followed by a population expansion and substructuring starting ~82 ka, which we link to an expansion from a glacial refugium. We showed that orang-utans went through drastic changes in population size and connectedness, caused by recurrent contraction and expansion of rainforest habitat during Pleistocene glaciations and probably hunting by early humans. Our findings emphasize the fact that important aspects of the evolutionary past of species with complex demographic histories might remain obscured when applying overly simplified models.
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http://dx.doi.org/10.1111/mec.13027DOI Listing
January 2015

Generation of SNP datasets for orangutan population genomics using improved reduced-representation sequencing and direct comparisons of SNP calling algorithms.

BMC Genomics 2014 Jan 10;15:16. Epub 2014 Jan 10.

Evolutionary Genetics Group, Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland.

Background: High-throughput sequencing has opened up exciting possibilities in population and conservation genetics by enabling the assessment of genetic variation at genome-wide scales. One approach to reduce genome complexity, i.e. investigating only parts of the genome, is reduced-representation library (RRL) sequencing. Like similar approaches, RRL sequencing reduces ascertainment bias due to simultaneous discovery and genotyping of single-nucleotide polymorphisms (SNPs) and does not require reference genomes. Yet, generating such datasets remains challenging due to laboratory and bioinformatical issues. In the laboratory, current protocols require improvements with regards to sequencing homologous fragments to reduce the number of missing genotypes. From the bioinformatical perspective, the reliance of most studies on a single SNP caller disregards the possibility that different algorithms may produce disparate SNP datasets.

Results: We present an improved RRL (iRRL) protocol that maximizes the generation of homologous DNA sequences, thus achieving improved genotyping-by-sequencing efficiency. Our modifications facilitate generation of single-sample libraries, enabling individual genotype assignments instead of pooled-sample analysis. We sequenced ~1% of the orangutan genome with 41-fold median coverage in 31 wild-born individuals from two populations. SNPs and genotypes were called using three different algorithms. We obtained substantially different SNP datasets depending on the SNP caller. Genotype validations revealed that the Unified Genotyper of the Genome Analysis Toolkit and SAMtools performed significantly better than a caller from CLC Genomics Workbench (CLC). Of all conflicting genotype calls, CLC was only correct in 17% of the cases. Furthermore, conflicting genotypes between two algorithms showed a systematic bias in that one caller almost exclusively assigned heterozygotes, while the other one almost exclusively assigned homozygotes.

Conclusions: Our enhanced iRRL approach greatly facilitates genotyping-by-sequencing and thus direct estimates of allele frequencies. Our direct comparison of three commonly used SNP callers emphasizes the need to question the accuracy of SNP and genotype calling, as we obtained considerably different SNP datasets depending on caller algorithms, sequencing depths and filtering criteria. These differences affected scans for signatures of natural selection, but will also exert undue influences on demographic inferences. This study presents the first effort to generate a population genomic dataset for wild-born orangutans with known population provenance.
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http://dx.doi.org/10.1186/1471-2164-15-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3897891PMC
January 2014

Effective population size dynamics and the demographic collapse of Bornean orang-utans.

PLoS One 2012 15;7(11):e49429. Epub 2012 Nov 15.

Population and Conservation Genetics, Instituto Gulbenkian de Ciência, Oeiras, Portugal.

Bornean orang-utans experienced a major demographic decline and local extirpations during the Pleistocene and Holocene due to climate change, the arrival of modern humans, of farmers and recent commercially-driven habitat loss and fragmentation. The recent loss of habitat and its dramatic fragmentation has affected the patterns of genetic variability and differentiation among the remaining populations and increased the extinction risk of the most isolated ones. However, the contribution of recent demographic events to such genetic patterns is still not fully clear. Indeed, it can be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric demographic events. Here, we investigated the genetic structure and population size dynamics of orang-utans from different sites. Altogether 126 individuals were analyzed and a full-likelihood Bayesian approach was applied. All sites exhibited clear signals of population decline. Population structure is known to generate spurious bottleneck signals and we found that it does indeed contribute to the signals observed. However, population structure alone does not easily explain the observed patterns. The dating of the population decline varied across sites but was always within the 200-2000 years period. This suggests that in some sites at least, orang-utan populations were affected by demographic events that started before the recent anthropogenic effects that occurred in Borneo. These results do not mean that the recent forest exploitation did not leave its genetic mark on orang-utans but suggests that the genetic pool of orang-utans is also impacted by more ancient events. While we cannot identify the main cause for this decline, our results suggests that the decline may be related to the arrival of the first farmers or climatic events, and that more theoretical work is needed to understand how multiple demographic events impact the genome of species and how we can assess their relative contributions.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0049429PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3499548PMC
May 2013

Marked population structure and recent migration in the critically endangered Sumatran orangutan (Pongo abelii).

J Hered 2013 Jan-Feb;104(1):2-13. Epub 2012 Oct 16.

Anthropological Institute & Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

A multitude of factors influence how natural populations are genetically structured, including dispersal barriers, inhomogeneous habitats, and social organization. Such population subdivision is of special concern in endangered species, as it may lead to reduced adaptive potential and inbreeding in local subpopulations, thus increasing the risk of future extinctions. With only 6600 animals left in the wild, Sumatran orangutans (Pongo abelii) are among the most endangered, but also most enigmatic, great ape species. In order to infer the fine-scale population structure and connectivity of Sumatran orangutans, we analyzed the most comprehensive set of samples to date, including mitochondrial hyper-variable region I haplotypes for 123 individuals and genotypes of 27 autosomal microsatellite markers for 109 individuals. For both mitochondrial and autosomal markers, we found a pronounced population structure, caused by major rivers, mountain ridges, and the Toba caldera. We found that genetic diversity and corresponding long-term effective population size estimates vary strongly among sampling regions for mitochondrial DNA, but show remarkable similarity for autosomal markers, hinting at male-driven long-distance gene flow. In support of this, we identified several individuals that were most likely sired by males originating from other genetic clusters. Our results highlight the effect of natural barriers in shaping the genetic structure of great ape populations, but also point toward important dispersal corridors on northern Sumatra that allow for genetic exchange.
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http://dx.doi.org/10.1093/jhered/ess065DOI Listing
June 2013

Call cultures in orang-utans?

PLoS One 2012 7;7(5):e36180. Epub 2012 May 7.

Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland.

Background: Several studies suggested great ape cultures, arguing that human cumulative culture presumably evolved from such a foundation. These focused on conspicuous behaviours, and showed rich geographic variation, which could not be attributed to known ecological or genetic differences. Although geographic variation within call types (accents) has previously been reported for orang-utans and other primate species, we examine geographic variation in the presence/absence of discrete call types (dialects). Because orang-utans have been shown to have geographic variation that is not completely explicable by genetic or ecological factors we hypothesized that this will be similar in the call domain and predict that discrete call type variation between populations will be found.

Methodology/principal Findings: We examined long-term behavioural data from five orang-utan populations and collected fecal samples for genetic analyses. We show that there is geographic variation in the presence of discrete types of calls. In exactly the same behavioural context (nest building and infant retrieval), individuals in different wild populations customarily emit either qualitatively different calls or calls in some but not in others. By comparing patterns in call-type and genetic similarity, we suggest that the observed variation is not likely to be explained by genetic or ecological differences.

Conclusion/significance: These results are consistent with the potential presence of 'call cultures' and suggest that wild orang-utans possess the ability to invent arbitrary calls, which spread through social learning. These findings differ substantially from those that have been reported for primates before. First, the results reported here are on dialect and not on accent. Second, this study presents cases of production learning whereas most primate studies on vocal learning were cases of contextual learning. We conclude with speculating on how these findings might assist in bridging the gap between vocal communication in non-human primates and human speech.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0036180PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3346723PMC
September 2012

Heavily male-biased long-distance dispersal of orang-utans (genus: Pongo), as revealed by Y-chromosomal and mitochondrial genetic markers.

Mol Ecol 2012 Jul 30;21(13):3173-86. Epub 2012 Mar 30.

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

Mating systems are thought to be an important determinant of dispersal strategies in most animals, including the great apes. As the most basal taxon of all great apes, orang-utans can provide information about the evolution of mating systems and their consequences for population structure in this Family. To assess the sex-specific population structure in orang-utans, we used a combination of paternally transmitted Y-chromosomal genetic markers and maternally transmitted mitochondrial DNA sequences. Markers transmitted through the more philopatric sex are expected to show stronger differentiation among populations than the ones transmitted through the dispersing sex. We studied these patterns using 70 genetic samples from wild orang-utans from seven Bornean and two Sumatran populations. We found pronounced population structure in haplotype networks of mitochondrial sequence data, but much less so for male-specific markers. Similarly, mitochondrial genetic differentiation was twice as high among populations compared to Y-chromosomal variation. We also found that genetic distance increased faster with geographic distance for mitochondrial than for Y-linked markers, leading to estimates of male dispersal distances that are several-fold higher than those of females. These findings provide evidence for strong male-biased dispersal in orang-utans. The transition to predominantly female-biased dispersal in the great ape lineage appears to be correlated with life in multimale groups and may reflect the associated fitness benefits of reliable male coalitions with relatives or known partners, a feature that is absent in orang-utans.
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http://dx.doi.org/10.1111/j.1365-294X.2012.05539.xDOI Listing
July 2012

Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant Orangutans (genus: Pongo).

Mol Biol Evol 2011 Aug 18;28(8):2275-88. Epub 2011 Feb 18.

Anthropological Institute & Museum, University of Zurich, Zurich, Switzerland.

The Southeast Asian Sunda archipelago harbors a rich biodiversity with a substantial proportion of endemic species. The evolutionary history of these species has been drastically influenced by environmental forces, such as fluctuating sea levels, climatic changes, and severe volcanic activities. Orangutans (genus: Pongo), the only Asian great apes, are well suited to study the relative impact of these forces due to their well-documented behavioral ecology, strict habitat requirements, and exceptionally slow life history. We investigated the phylogeographic patterns and evolutionary history of orangutans in the light of the complex geological and climatic history of the Sunda archipelago. Our study is based on the most extensive genetic sampling to date, covering the entire range of extant orangutan populations. Using data from three mitochondrial DNA (mtDNA) genes from 112 wild orangutans, we show that Sumatran orangutans, Pongo abelii, are paraphyletic with respect to Bornean orangutans (P. pygmaeus), the only other currently recognized species within this genus. The deepest split in the mtDNA phylogeny of orangutans occurs across the Toba caldera in northern Sumatra and, not as expected, between both islands. Until the recent past, the Toba region has experienced extensive volcanic activity, which has shaped the current phylogeographic patterns. Like their Bornean counterparts, Sumatran orangutans exhibit a strong, yet previously undocumented structuring into four geographical clusters. However, with 3.50 Ma, the Sumatran haplotypes have a much older coalescence than their Bornean counterparts (178 kya). In sharp contrast to the mtDNA data, 18 Y-chromosomal polymorphisms show a much more recent coalescence within Sumatra compared with Borneo. Moreover, the deep geographic structure evident in mtDNA is not reflected in the male population history, strongly suggesting male-biased dispersal. We conclude that volcanic activities have played an important role in the evolutionary history of orangutans and potentially of many other forest-dwelling Sundaland species. Furthermore, we demonstrate that a strong sex bias in dispersal can lead to conflicting patterns in uniparentally inherited markers even at a genus-wide scale, highlighting the need for a combined usage of maternally and paternally inherited marker systems in phylogenetic studies.
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http://dx.doi.org/10.1093/molbev/msr042DOI Listing
August 2011

Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus).

Proc Natl Acad Sci U S A 2010 Dec 22;107(50):21376-81. Epub 2010 Nov 22.

Anthropological Institute and Museum, University of Zurich, 8057 Zurich, Switzerland.

Sundaland, a tropical hotspot of biodiversity comprising Borneo and Sumatra among other islands, the Malay Peninsula, and a shallow sea, has been subject to dramatic environmental processes. Thus, it presents an ideal opportunity to investigate the role of environmental mechanisms in shaping species distribution and diversity. We investigated the population structure and underlying mechanisms of an insular endemic, the Bornean orangutan (Pongo pygmaeus). Phylogenetic reconstructions based on mtDNA sequences from 211 wild orangutans covering the entire range of the species indicate an unexpectedly recent common ancestor of Bornean orangutans 176 ka (95% highest posterior density, 72-322 ka), pointing to a Pleistocene refugium. High mtDNA differentiation among populations and rare haplotype sharing is consistent with a pattern of strong female philopatry. This is corroborated by isolation by distance tests, which show a significant correlation between mtDNA divergence and distance and a strong effect of rivers as barriers for female movement. Both frequency-based and Bayesian clustering analyses using as many as 25 nuclear microsatellite loci revealed a significant separation among all populations, as well as a small degree of male-mediated gene flow. This study highlights the unique effects of environmental and biological features on the evolutionary history of Bornean orangutans, a highly endangered species particularly vulnerable to future climate and anthropogenic change as an insular endemic.
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http://dx.doi.org/10.1073/pnas.1010169107DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3003094PMC
December 2010

Development of polymorphic microsatellite markers for the dung fly (Sepsis cynipsea).

Mol Ecol Resour 2009 Nov 25;9(6):1554-6. Epub 2009 Jun 25.

Anthropological Institute & Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland Zoological Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

The polyandrous fly Sepsis cynipsea has been used extensively in studies of sexual selection and local adaptation. We isolated and characterized 11 novel microsatellite markers for S. cynipsea from a genomic library and screened 32 flies for polymorphism. All microsatellite markers show high allelic diversity with an average of 9.64 alleles per locus. Two microsatellites were found likely to be X-linked. These novel markers will significantly advance studies of sexual selection and evolutionary genetics of S. cynipsea and related species, especially given the low numbers of markers currently available in this family.
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http://dx.doi.org/10.1111/j.1755-0998.2009.02736.xDOI Listing
November 2009

New polymorphic tetranucleotide microsatellites improve scoring accuracy in the bottlenose dolphin Tursiops aduncus.

Mol Ecol Resour 2009 Mar 20;9(2):531-4. Epub 2009 Jan 20.

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland.

We isolated and characterized 19 novel tetranucleotide microsatellite markers in the Indo-Pacific bottlenose dolphin (Tursiops aduncus) in order to improve genotyping accuracy in applications like large-scale population-wide paternity and relatedness assessments. One hundred T. aduncus from Shark Bay, Western Australia, were screened for polymorphism. Cross-amplification was tested on four other small odontocete species. The new tetranucleotide microsatellite loci showed a more than fourfold higher scoring accuracy and significantly lower stutter formation compared to eight dinucleotide loci, although overall allelic diversity was significantly reduced.
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http://dx.doi.org/10.1111/j.1755-0998.2008.02246.xDOI Listing
March 2009

Development of polymorphic microsatellite markers for the livebearing fish Poecilia parae.

Mol Ecol Resour 2008 Jul;8(4):857-60

Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland, Zoological Institute, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland.

We developed 16 novel polymorphic tetranucleotide microsatellite markers for Poecilia parae, a livebearing fish used in evolutionary studies because of its Y-linked colour and size polymorphism. A set of 199 clones was sequenced out of an enriched genomic library, and we achieved an enrichment efficiency of nearly 80%. Primers were designed for 16 pure repeats, and 59 P. parae were screened for polymorphism. Cross-amplification was tested on Poecilia picta and Poecilia reticulata, the guppy. The new microsatellite markers showed an exceptionally high allelic diversity and low stutter formation, proving their suitability for a broad range of applications in these species.
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http://dx.doi.org/10.1111/j.1755-0998.2008.02090.xDOI Listing
July 2008