R.P.M.A. Crooijmans

Wageningen University, Wageningen, Gelderland, Netherlands

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Publications (276)732.62 Total impact

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    ABSTRACT: Early pig farmers in Europe imported Asian pigs to cross with their local breeds in order to improve traits of commercial interest. Current genomics techniques enabled genome-wide identification of these Asian introgressed haplotypes in modern European pig breeds. We propose that the Asian variants are still present because they affect phenotypes that were important for ancient traditional, as well as recent, commercial pig breeding. Genome-wide introgression levels were only weakly correlated with gene content and recombination frequency. However, regions with an excess or absence of Asian haplotypes (AS) contained genes that were previously identified as phenotypically important such as FASN, ME1, and KIT. Therefore, the Asian alleles are thought to have an effect on phenotypes that were historically under selection. We aimed to estimate the effect of AS in introgressed regions in Large White pigs on the traits of backfat (BF) and litter size. The majority of regions we tested that retained Asian deoxyribonucleic acid (DNA) showed significantly increased BF from the Asian alleles. Our results suggest that the introgression in Large White pigs has been strongly determined by the selective pressure acting upon the introgressed AS. We therefore conclude that human-driven hybridization and selection contributed to the genomic architecture of these commercial pigs.
    Preview · Article · Dec 2015 · Proceedings of the Royal Society B: Biological Sciences
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    Full-text · Dataset · Oct 2015
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    Full-text · Dataset · Oct 2015
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    ABSTRACT: Traditionally, the process of domestication is assumed to be initiated by humans, involve few individuals and rely on reproductive isolation between wild and domestic forms. We analyzed pig domestication using over 100 genome sequences and tested whether pig domestication followed a traditional linear model or a more complex, reticulate model. We found that the assumptions of traditional models, such as reproductive isolation and strong domestication bottlenecks, are incompatible with the genetic data. In addition, our results show that, despite gene flow, the genomes of domestic pigs have strong signatures of selection at loci that affect behavior and morphology. We argue that recurrent selection for domestic traits likely counteracted the homogenizing effect of gene flow from wild boars and created 'islands of domestication' in the genome. Our results have major ramifications for the understanding of animal domestication and suggest that future studies should employ models that do not assume reproductive isolation.
    No preview · Article · Aug 2015 · Nature Genetics
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    ABSTRACT: The advent of high-throughput genomic technologies is enabling analyses on thousands or even millions of single-nucleotide polymorphisms (SNPs). At the same time, the selection of a minimum number of SNPs with the maximum information content is becoming increasingly problematic. Available locus ranking programs have been accused of providing upwardly biased results (concerning the predicted accuracy of the chosen set of markers for population assignment), cannot handle high-dimensional datasets, and some of them are computationally intensive. The toolbox for ranking and evaluation of SNPs (TRES) is a collection of algorithms built in a user-friendly and computationally efficient software that can manipulate and analyze datasets even in the order of millions of genotypes in a matter of seconds. It offers a variety of established methods for evaluating and ranking SNPs on user defined groups of populations and produces a set of predefined number of top ranked loci. Moreover, dataset manipulation algorithms enable users to convert datasets in different file formats, split the initial datasets into train and test sets, and finally create datasets containing only selected SNPs occurring from the SNP selection analysis for later on evaluation in dedicated software such as GENECLASS. This application can aid biologists to select loci with maximum power for optimization of cost-effective panels with applications related to e.g. species identification, wildlife management, and forensic problems. TRES is available for all operating systems at http://mlkd.csd.auth.gr/bio/tres. © The American Genetic Association 2015. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
    No preview · Article · Jul 2015 · The Journal of heredity
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    ABSTRACT: Conservation and breeding programs aim at maintaining the most diversity, thereby avoiding deleterious effects of inbreeding while maintaining enough variation from which traits of interest can be selected. Theoretically, the most diversity is maintained using optimal contributions based on many markers to calculate coancestries, but this can decrease fitness by maintaining linked deleterious variants. The heterogeneous patterns of coancestry displayed in pigs make them an excellent model to test these predictions. We propose methods to measure coancestry and fitness from resequencing data and use them in population management. We analyzed the resequencing data of Sus cebifrons, a highly endangered porcine species from the Philippines, and genotype data from the Pietrain domestic breed. By analyzing the demographic history of Sus cebifrons, we inferred two past bottlenecks that resulted in some inbreeding load. In Pietrain, we analyzed signatures of selection possibly associated with commercial traits. We also simulated the management of each population to assess the performance of different optimal contribution methods to maintain diversity, fitness, and selection signatures. Maximum genetic diversity was maintained using marker-by-marker coancestry, and least using genealogical coancestry. Using a measure of coancestry based on shared segments of the genome achieved the best results in terms of diversity and fitness. However, this segment-based management eliminated signatures of selection. We demonstrate that maintaining both diversity and fitness depends on the genomic distribution of deleterious variants, which is shaped by demographic and selection histories. Our findings show the importance of genomic and next-generation sequencing information in the optimal design of breeding or conservation programs. © 2015 Bosse et al.; Published by Cold Spring Harbor Laboratory Press.
    Full-text · Article · Jun 2015 · Genome Research
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    ABSTRACT: Unraveling the genetic mechanisms associated with reduced gene flow between genetically differentiated populations is key to understand speciation. Different types of structural variations (SVs) have been found as a source of genetic diversity in a wide range of species. Previous studies provided detailed knowledge on the potential evolutionary role of SVs, especially copy number variations (CNVs), between well diverged species of e.g. primates. However, our understanding of their significance during ongoing speciation processes is limited due to the lack of CNV data from closely related species. The genus Sus (pig and its close relatives) which started to diverge ~4 Mya presents an excellent model for studying the role of CNVs during ongoing speciation. In this study, we identified 1408 CNV regions (CNVRs) across the genus Sus. These CNVRs encompass 624 genes and were found to evolve ~2.5 times faster than single nucleotide polymorphisms (SNPs). The majority of these copy number variable genes are olfactory receptors (ORs) known to play a prominent role in food foraging and mate recognition in Sus. Phylogenetic analyses, including novel Bayesian analysis, based on CNVRs that overlap ORs retain the well-accepted topology of the genus Sus whereas CNVRs overlapping genes other than ORs show evidence for random drift and/or admixture. We hypothesize that inter-specific variation in copy number of ORs provided the means for rapid adaptation to different environments during the diversification of the genus Sus in the Pliocene. Furthermore, these regions might have acted as barriers preventing massive gene flow between these species during the multiple hybridization events that took place later in the Pleistocene suggesting a possible prominent role of ORs in the ongoing Sus speciation.
    Preview · Article · Apr 2015 · BMC Genomics
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    No preview · Conference Paper · Mar 2015

  • No preview · Article · Feb 2015 · Nature Genetics
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    ABSTRACT: The most significant challenge in the post-genomic era is connecting genotype to quantitative phenotype in basic and applied biology - the Genome to Phenome challenge. ENCODE (ENCyclopedia Of DNA Elements) projects have shown that a coordinated genome-wide identification of functional elements in multiple species is an invaluable resource for the dissection of genotype to phenotype relationships. The phenotypic diversity in domesticated animals provides unique opportunities to study such relationships. The FAANG consortium (www.animalgenome.org/community/FAANG) aims to promote and coordinate an international project to identify all functional elements in these species. This project is expected to provide critical information to enable the application of molecular phenotypes to prediction of complex phenotypes, and as such to have an important impact on studies and applications in agriculture, biomedical science, evolution and environment. Several groups worldwide are starting pilot projects. Common aims are to improve the functional annotation of the genomes of major domesticated species, and to develop the analytic framework needed for the FAANG initiative. “WUR-pigENCODE” (on pig) is an ongoing Dutch pilot project (Wageningen University). The INRA project “FR-AgENCODE” (on cattle, goat, pig, chicken; in collaboration with EMBL-EBI, University of Edinburgh and Wageningen University) and a USDA-NIFA project by UC Davis (on chicken, cattle, and pig; in collaboration with three US Species Genome Coordinators, UCSC, and EMBL-EBI) will start in January 2015. This presentation will provide an overview of the FAANG initiative (see poster by Clarke, L. et al.) and illustrate these pilot projects, including the implications for adequate coordination among parallel initiatives.
    No preview · Conference Paper · Jan 2015
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    ABSTRACT: The evolution of island populations in natural systems is driven by local adaptation and genetic drift. However, evolutionary pathways may be altered by humans in several ways. The wild boar (WB) (Sus scrofa) is an iconic game species occurring in several islands, where it has been strongly managed since prehistoric times. We examined genomic diversity at 49 803 single-nucleotide polymorphisms in 99 Sardinian WBs and compared them with 196 wild specimens from mainland Europe and 105 domestic pigs (DP; 11 breeds). High levels of genetic variation were observed in Sardinia (80.9% of the total number of polymorphisms), which can be only in part associated to recent genetic introgression. Both Principal Component Analysis and Bayesian clustering approach revealed that the Sardinian WB population is highly differentiated from the other European populations (F ST = 0.126–0.138), and from DP (F ST = 0.169). Such evidences were mostly unaffected by an uneven sample size, although clustering results in reference populations changed when the number of individuals was standardized. Runs of homozygosity (ROHs) pattern and distribution in Sardinian WB are consistent with a past expansion following a bottleneck (small ROHs) and recent population substructuring (highly homozygous individuals). The observed effect of a non-random selection of Sardinian individuals on diversity, F ST and ROH estimates, stressed the importance of sampling design in the study of structured or introgressed populations. Our results support the heterogeneity and distinctiveness of the Sardinian population and prompt further investigations on its origins and conservation status.
    Full-text · Article · Jan 2015 · Heredity
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    K Ngeno · E H Van Der Waaij · H J Megens · A K Kahi · J A M Van Arendonk · R P M A Crooijmans
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    ABSTRACT: The study investigated the genetic make-up of different ecotypes of indigenous chickens (ICs) in Kenya based on major histocompatibility complex (MHC)-linked and non-MHC microsatellite markers. Blood samples were collected from eight regions (48 birds per region) of Kenya: Kakamega (KK), Siaya (BN), West Pokot (WP), Turkana (TK), Bomet (BM), Narok (NR), Lamu (LM) and Taita-Taveta (TT) and genotyped using two MHC-linked and ten non-MHC markers. All MHC-linked and non-MHC markers were polymorphic with a total of 140 alleles, of which 56 were identified in MHC-linked markers. Mean number of alleles (Na and Ne), private alleles, heterozygosity and genetic distances were higher for MHC-linked markers compared with non-MHC markers. The ad hoc statistic ΔK detected the true numbers of clusters to be three for MHC-linked markers and two in non-MHC markers. In conclusion, Kenyan ICs belong into two to three genetically distinct groups. Different markers systems have different clustering system. MHC-linked markers divided ICs into three mixed clusters, composing of individuals from the different ecotypes whereas non-MHC markers grouped ICs into two groups. These IC ecotypes host many and highly diverse MHC-linked alleles. Higher allelic diversity indicated a huge amount of genetic variation in the MHC region of ICs and supported their reputation of being hardy and resistant to diseases.
    Full-text · Article · Dec 2014
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    ABSTRACT: Background The domestic turkey (Meleagris gallopavo) is an important agricultural species that is largely used as a meat-type bird. Characterizing genetic variation in populations of domesticated species and associating these variation patterns with the evolution, domestication, and selective breeding is critical for understanding the dynamics of genomic change in these species. Intense selective breeding and population bottlenecks are expected to leave signatures in the genome of domesticated species, such as unusually low nucleotide diversity or the presence of exceptionally extended haplotype homozygosity. These patterns of variation in selected populations are highly useful to not only understand the consequences of selective breeding and population dynamics, but also to provide insights into biological mechanisms that may affect physiological processes important to bring changes in phenotype of interest.ResultsWe observed 54 genomic regions in heritage and commercial turkey populations on 14 different chromosomes that showed statistically significant (P¿<¿0.05) reduction in genomic variation indicating candidate selective sweeps. Areas with evidence of selective sweeps varied from 1.5 Mb to 13.8 Mb in length. Out of these 54 sweeps, 23 overlapped at least partially between two or more populations. Overlapping sweeps were found on 13 different chromosomes. The remaining 31 sweeps were population-specific and were observed on 12 different chromosomes, with 26 of these regions present only in commercial populations. Genes that are known to affect growth were enriched in the sweep regions.Conclusion The turkey genome showed large sweep regions. The relatively high number of sweep regions in commercial turkey populations compared to heritage varieties and the enrichment of genes important to growth in these regions, suggest that these sweeps are the result of intense selection in these commercial lines, moving specific haplotypes towards fixation.
    Full-text · Article · Nov 2014 · BMC Genetics
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    ABSTRACT: Abstract Text: In 2010 an abnormally large number of German Longhaired Pointers (GLP) was offered for treatment of thyroid cancer. Pedigree analysis revealed a potential monogenic background. Histo-pathological examination revealed a variety of sub-types of thyroid cancer. In total 20 cases, ranging from 4.5 to 13 years old, and 28 controls were genotyped with the >170K CanineHD BeadChip. A GWAS resulted in a number of, and not in a single, genome-wide suggestive peaks. This lead to the hypothesis that there are two types of thyroid cancer in the GLP of which only one is highly heritable. When only affected dogs younger than 7 years were included in the GWAS, a single region with 5 SNP in complete LD between cases and controls was detected. This suggests the presence of a major gene that explains the onset of thyroid cancer in the German Longhaired Pointer. Keywords: Thyroid cancer Dogs Major gene
    No preview · Conference Paper · Aug 2014
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    ABSTRACT: The independent domestication of local wild boar populations in Asia and Europe about 10,000 years ago led to distinct European and Asian pig breeds, each with very different phenotypic characteristics. During the Industrial Revolution, Chinese breeds were imported to Europe to improve commercial traits in European breeds. Here we demonstrate the presence of introgressed Asian haplotypes in European domestic pigs and selection signatures on some loci in these regions, using whole genome sequence data. The introgression signatures are widespread and the Asian haplotypes are rarely fixed. The Asian introgressed haplotypes are associated with regions harbouring genes involved in meat quality, development and fertility. We identify Asian-derived non-synonymous mutations in the AHR gene that associate with increased litter size in multiple European commercial lines. These findings demonstrate that increased fertility was an important breeding goal for early nineteenth century pig farmers, and that Asian variants of genes related to this trait were preferentially selected during the development of modern European pig breeds.
    Full-text · Article · Jul 2014 · Nature Communications
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    ABSTRACT: The merging of populations after an extended period of isolation and divergence is a common phenomenon, in natural settings as well as due to human interference. Individuals with such hybrid origins contain genomes that essentially form a mosaic of different histories and demographies. Pigs are an excellent model species to study hybridization because European and Asian wild boars diverged ~1.2 Mya and pigs were domesticated independently in Europe and Asia. During the Industrial Revolution in England, pigs were imported from China to improve the local pigs. This study utilizes the latest genomics tools to identify the origin of haplotypes in European domesticated pigs that are descendant from Asian and European populations. Our results reveal fine-scale haplotype structure representing different ancient demographic events, as well as a mosaic composition of those distinct histories due to recently introgressed haplotypes in the pig genome. As a consequence, nucleotide diversity in the genome of European domesticated pigs is higher when at least one haplotype of Asian origin is present, and haplotype length correlates negatively with recombination frequency and nucleotide diversity. Another consequence is that the inference of past effective population size is influenced by the background of the haplotypes in an individual, but we demonstrate that by careful sorting based on the origin of haplotypes both distinct demographic histories can be reconstructed. Future detailed mapping of the genomic distribution of variation will enable a targeted approach to increase genetic diversity of captive and wild populations, thus facilitating conservation efforts in the near future.This article is protected by copyright. All rights reserved.
    No preview · Article · May 2014 · Molecular Ecology
  • J. Abernathy · X. Li · X. Jia · W. Chou · S. J. Lamont · R. Crooijmans · H. Zhou
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    ABSTRACT: Copy number variation refers to regions along chromosomes that harbor a type of structural variation, such as duplications or deletions. Copy number variants (CNVs) play a role in many important traits as well as in genetic diversity. Previous analyses of chickens using array comparative genomic hybridizations or single-nucleotide polymorphism chip assays have been performed on various breeds and genetic lines to discover CNVs. In this study, we assessed individuals from two highly inbred (inbreeding coefficiency > 99.99%) lines, Leghorn G-B2 and Fayoumi M15.2, to discover novel CNVs in chickens. These lines have been previously studied for disease resistance, and to our knowledge, this represents the first global assessment of CNVs in the Fayoumi breed. Genomic DNA from individuals was examined using the Agilent chicken 244 K comparative genomic hybridization array and quantitative PCR. We identified a total of 273 CNVs overall, with 112 CNVs being novel and not previously reported. Quantitative PCR using the standard curve method validated a subset of our array data. Through enrichment analysis of genes within CNV regions, we observed multiple chromosomes, terms and pathways that were significantly enriched, largely dealing with the major histocompatibility complex and immune responsiveness. Using an additional round of computational and statistical analysis with a different bioinformatic pipeline, we identified 43 CNVs among these as high-confidence regions, 14 of which were found to be novel. We further compared and contrasted individuals of the two inbred lines to discover regions that have a significant difference in copy number between lines. A total of 40 regions had significant deletions or duplications between the lines. Gene Ontology analysis of genomic regions containing CNVs between lines also was performed. This between-line candidate CNV list will be useful in studies with these two unique genetic lines, which may harbor variations that underlie quantitative trait loci for disease resistance and other important traits. Through the global discovery of novel CNVs in chicken, these data also provide resources for further genetic and functional genomics studies.
    No preview · Article · Mar 2014 · Animal Genetics
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    ABSTRACT: The success of Genome Wide Association Studies in the discovery of sequence variation linked to complex traits in humans has increased interest in high throughput SNP genotyping assays in livestock species. Primary goals are QTL detection and genomic selection. The purpose here was design of a 50-60,000 SNP chip for goats. The success of a moderate density SNP assay depends on reliable bioinformatic SNP detection procedures, the technological success rate of the SNP design, even spacing of SNPs on the genome and selection of Minor Allele Frequencies (MAF) suitable to use in diverse breeds. Through the federation of three SNP discovery projects consolidated as the International Goat Genome Consortium, we have identified approximately twelve million high quality SNP variants in the goat genome stored in a database together with their biological and technical characteristics. These SNPs were identified within and between six breeds (meat, milk and mixed): Alpine, Boer, Creole, Katjang, Saanen and Savanna, comprising a total of 97 animals. Whole genome and Reduced Representation Library sequences were aligned on >10 kb scaffolds of the de novo goat genome assembly. The 60,000 selected SNPs, evenly spaced on the goat genome, were submitted for oligo manufacturing (Illumina, Inc) and published in dbSNP along with flanking sequences and map position on goat assemblies (i.e. scaffolds and pseudo-chromosomes), sheep genome V2 and cattle UMD3.1 assembly. Ten breeds were then used to validate the SNP content and 52,295 loci could be successfully genotyped and used to generate a final cluster file. The combined strategy of using mainly whole genome Next Generation Sequencing and mapping on a contig genome assembly, complemented with Illumina design tools proved to be efficient in producing this GoatSNP50 chip. Advances in use of molecular markers are expected to accelerate goat genomic studies in coming years.
    Full-text · Article · Jan 2014 · PLoS ONE
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    ABSTRACT: Although all farm animals have an original source of domestication, a large variety of modern breeds exist that are phenotypically highly distinct from the ancestral wild population. This phenomenon can be the result of artificial selection or gene flow from other sources into the domesticated population. The Eurasian wild boar (Sus scrofa) has been domesticated at least twice in two geographically distinct regions during the Neolithic revolution when hunting shifted to farming. Prior to the establishment of the commercial European pig breeds we know today, some 200 years ago Chinese pigs were imported into Europe to improve local European pigs. Commercial European domesticated pigs are genetically more diverse than European wild boars, although historically the latter represents the source population for domestication. In this study we examine the cause of the higher diversity within the genomes of European commercial pigs compared to their wild ancestors by testing two different hypotheses. In the first hypothesis we consider that European commercial pigs are a mix of different European wild populations as a result of movement throughout Europe, hereby acquiring haplotypes from all over the European continent. As an alternative hypothesis, we examine whether the introgression of Asian haplotypes into European breeds during the Industrial Revolution caused the observed increase in diversity. By using re-sequence data for chromosome 1 of 136 pigs and wild boars, we show that an Asian introgression of about 20% into the genome of European commercial pigs explains the majority of the increase in genetic diversity. These findings confirm that the Asian hybridization, that was used to improve production traits of local breeds, left its signature in the genome of the commercial pigs we know today.
    Full-text · Article · Jan 2014 · Frontiers in Genetics
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    ABSTRACT: The pig, Sus scrofa, is a foreign species to the American continent. Although pigs originally introduced in the Americas should be related to those from the Iberian Peninsula and Canary islands, the phylogeny of current creole pigs that now populate the continent is likely to be very complex. Because of the extreme climates that America harbors, these populations also provide a unique example of a fast evolutionary phenomenon of adaptation. Here, we provide a genome wide study of these issues by genotyping, with a 60k SNP chip, 206 village pigs sampled across 14 countries and 183 pigs from outgroup breeds that are potential founders of the American populations, including wild boar, Iberian, international and Chinese breeds. Results show that American village pigs are primarily of European ancestry, although the observed genetic landscape is that of a complex conglomerate. There was no correlation between genetic and geographical distances, neither continent wide nor when analyzing specific areas. Most populations showed a clear admixed structure where the Iberian pig was not necessarily the main component, illustrating how international breeds, but also Chinese pigs, have contributed to extant genetic composition of American village pigs. We also observe that many genes related to the cardiovascular system show an increased differentiation between altiplano and genetically related pigs living near sea level.Heredity advance online publication, 19 December 2012; doi:10.1038/hdy.2012.109.
    Full-text · Article · Dec 2013 · Heredity

Publication Stats

7k Citations
732.62 Total Impact Points

Institutions

  • 1993-2015
    • Wageningen University
      • • Animal Breeding and Genomics Centre
      • • Division of Fokkerij & Genetica
      Wageningen, Gelderland, Netherlands
  • 2010
    • Wageningen UR
      Wageningen, Gelderland, Netherlands
  • 2000
    • University of Wuerzburg
      Würzburg, Bavaria, Germany