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Genomics of chicken domestication and feralisation
Linköping University, Department of Physics, Chemistry and Biology, Biology. Linköping University, Faculty of Science & Engineering.ORCID iD: 0000-0003-1262-4585
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Domestication can serve as a study system of rapid evolutionary change with wide-ranging effects on traits in animals. The chicken was domesticated from the Red Junglefowl and has diverged in behaviour, morphology and life history traits. Conversely, feralisation is a more recent process when domestic animals are again exposed and respond to an environment outside of human husbandry. Linkage-based quantitative trait locus (QTL) mapping has been used to localise genetic variants that affect domestication traits in the chicken genome. Because of the limited resolution of linkage mapping, the QTL regions associated with domestication traits are often broad and contain many genes. One approach to help sort out potential causative genes is to measure gene expression as an intermediary molecular phenotype. In this dissertation, expression quantitative trait locus (eQTL) mapping of gene expression traits is used to search for potential causative genes for domestication traits in the chicken. Expression quantitative trait loci were mapped across the whole genome in bone and hypothalamus samples, and targeted at QTL regions in the base of the comb. These studies have resulted in candidate quantitative trait genes, supported by genetic and gene expression evidence, for relative comb mass, bone allocation, egg production and fearful behaviour as measured in an open field test. Secondly, a population genomics approach was used to study the molecular basis of feralisation in a free-range feral chicken population from the Pacific island of Kauai. Mitochondrial DNA sequences and phenotypic observations establish the hybrid origin of this population as a mixture of wild and domestic chickens. Genome-wide mapping of pooled heterozygosity highlight regions that may be involved in adaptation to the feral environment. The expression QTL results bring us closer to knowledge about the molecular basis of domestication traits in the chicken, suggesting plausible candidate genes and opening up for functional studies of individual loci. The population genomic study shows that feralisation has a mostly different genomic architecture than domestication, and suggests phenotypic effects, based on overlap with domestication QTL regions, for some of the identified regions.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2015. , 28 p.
Series
Linköping Studies in Science and Technology. Dissertations, ISSN 0345-7524 ; 1708
National Category
Genetics
Identifiers
URN: urn:nbn:se:liu:diva-122280DOI: 10.3384/diss.diva-122280ISBN: 978-91-7685-932-2 (print)OAI: oai:DiVA.org:liu-122280DiVA: diva2:865193
Public defence
2015-12-18, Planck, Fysikhuset, Campus Valla, Linköping, 10:15 (English)
Opponent
Supervisors
Available from: 2015-11-02 Created: 2015-10-27 Last updated: 2017-01-03Bibliographically approved
List of papers
1. A Sexual Ornament in Chickens Is Affected bu Pleiotropic Alleles at HAO1 and BMP2, Selected during Domestication
Open this publication in new window or tab >>A Sexual Ornament in Chickens Is Affected bu Pleiotropic Alleles at HAO1 and BMP2, Selected during Domestication
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2012 (English)In: PLOS Genetics, ISSN 1553-7390, Vol. 8, no 8, e10002914- p.Article in journal (Refereed) Published
Abstract [en]

Domestication is one of the strongest forms of short-term, directional selection. Although selection is typically only exerted on one or a few target traits, domestication can lead to numerous changes in many seemingly unrelated phenotypes. It is unknown whether such correlated responses are due to pleiotropy or linkage between separate genetic architectures. Using three separate intercrosses between wild and domestic chickens, a locus affecting comb mass (a sexual ornament in the chicken) and several fitness traits (primarily medullary bone allocation and fecundity) was identified. This locus contains two tightly-linked genes, BMP2 and HAO1, which together produce the range of pleiotropic effects seen. This study demonstrates the importance of pleiotropy (or extremely close linkage) in domestication. The nature of this pleiotropy also provides insights into how this sexual ornament could be maintained in wild populations.

National Category
Natural Sciences
Identifiers
urn:nbn:se:liu:diva-80901 (URN)10.1371/journal.pgen.1002914 (DOI)000308529300066 ()
Note

funding agencies|Foundation for Strategic Environmental Research||Swedish Research Council for Environmental, Agricultural Sciences, and Spatial Planning||FORMAS (Swedish Environment, Agricultural Sciences and Spatial Planning)||VR (Swedish Research Council)||

Available from: 2012-09-03 Created: 2012-09-03 Last updated: 2015-11-02
2. The role of pleiotropy and linkage in genes affecting a sexual ornament and bone allocation in the chicken
Open this publication in new window or tab >>The role of pleiotropy and linkage in genes affecting a sexual ornament and bone allocation in the chicken
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2014 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 9, 2275-2286 p.Article in journal (Refereed) Published
Abstract [en]

Sexual selection and the ornaments that inform such choices have been extensively studied, particularly from a phenotypic perspective. Although more is being revealed about the genetic architecture of sexual ornaments, much still remains to be discovered. The comb of the chicken is one of the most widely recognized sexual ornaments, which has been shown to be correlated with both fecundity and bone allocation. In this study, we use a combination of multiple intercrosses between White Leghorn populations and wild-derived Red Junglefowl to, first, map quantitative trait loci (QTL) for bone allocation and, second, to identify expression QTL that correlate and colocalize with comb mass. These candidate quantitative genes were then assessed for potential pleiotropic effects on bone tissue and fecundity traits. We identify genes that correlate with both relative comb mass and bone traits suggesting a combination of both pleiotropy and linkage mediates gene regulatory variation in these traits.

Place, publisher, year, edition, pages
John Wiley & Sons, 2014
Keyword
bone allocation, domestication, QTG, QTL, sexual selection
National Category
Natural Sciences
Identifiers
urn:nbn:se:liu:diva-105936 (URN)10.1111/mec.12723 (DOI)000334908100013 ()
Available from: 2014-04-15 Created: 2014-04-15 Last updated: 2017-12-05
3. Genetic Regulation of Bone Metabolism in the Chicken: Similarities and Differences to Mammalian Systems
Open this publication in new window or tab >>Genetic Regulation of Bone Metabolism in the Chicken: Similarities and Differences to Mammalian Systems
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2015 (English)In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 11, no 5, e1005250Article in journal (Refereed) Published
Abstract [en]

Birds have a unique bone physiology, due to the demands placed on them through egg production. In particular their medullary bone serves as a source of calcium for eggshell production during lay and undergoes continuous and rapid remodelling. We take advantage of the fact that bone traits have diverged massively during chicken domestication to map the genetic basis of bone metabolism in the chicken. We performed a quantitative trait locus (QTL) and expression QTL (eQTL) mapping study in an advanced intercross based on Red Junglefowl (the wild progenitor of the modern domestic chicken) and White Leghorn chickens. We measured femoral bone traits in 456 chickens by peripheral computerised tomography and femoral gene expression in a subset of 125 females from the cross with microarrays. This resulted in 25 loci for female bone traits, 26 loci for male bone traits and 6318 local eQTL loci. We then overlapped bone and gene expression loci, before checking for an association between gene expression and trait values to identify candidate quantitative trait genes for bone traits. A handful of our candidates have been previously associated with bone traits in mice, but our results also implicate unexpected and largely unknown genes in bone metabolism. In summary, by utilising the unique bone metabolism of an avian species, we have identified a number of candidate genes affecting bone allocation and metabolism. These findings can have ramifications not only for the understanding of bone metabolism genetics in general, but could also be used as a potential model for osteoporosis as well as revealing new aspects of vertebrate bone regulation or features that distinguish avian and mammalian bone.

National Category
Genetics
Identifiers
urn:nbn:se:liu:diva-118579 (URN)10.1371/journal.pgen.1005250 (DOI)000355305200057 ()26023928 (PubMedID)
Available from: 2015-06-01 Created: 2015-06-01 Last updated: 2017-12-04
4. Genetical Genomics of Behavior: A novel chicken genomic model for anxiety behavior
Open this publication in new window or tab >>Genetical Genomics of Behavior: A novel chicken genomic model for anxiety behavior
2016 (English)In: Genetics, ISSN 0016-6731, Vol. 202, no 1, 327+- p.Article in journal (Refereed) Published
Abstract [en]

The identification of genetic variants responsible for behavioral variation is an enduring goal in biology, with wide-scale ramifications, ranging from medical research to evolutionary theory on personality syndromes. Here, we use for the first time a large-scale genetical genomics analysis in the brain of the chicken to identify genes affecting anxiety as measured by an open field test. We combine quantitative trait locus (QTL) analysis in 572 individuals and expression QTL (eQTL) analysis in 129 individuals from an advanced intercross between domestic chickens and Red Junglefowl. We identify ten putative quantitative trait genes affecting anxiety behavior. These genes were tested for an association in the mouse Heterogenous Stock anxiety (open field) dataset and human GWAS datasets for bipolar disorder, major depressive disorder and schizophrenia. Although comparisons between species are complex, associations were observed for four of the candidate genes in mouse, and three of the candidate genes in humans. Using a multi-model approach we have therefore identified a number of putative quantitative trait genes affecting anxiety behavior, principally in the chicken but also with some potentially translational effects as well. This study demonstrates that the chicken is an excellent model organism for the genetic dissection of behavior.

Place, publisher, year, edition, pages
The Genetics Society, 2016
Keyword
Anxiety, behavioral genes, eQTL, QTL, causal genes, personality
National Category
Genetics
Identifiers
urn:nbn:se:liu:diva-122276 (URN)10.1534/genetics.115.179010 (DOI)000367718100026 ()26733665 (PubMedID)
Note

Funding agencies: Swedish Research Council; Swedish Research Council for Environment; Agricultural Sciences and Spatial Planning; European Research Council [GENEWELL 322206]

Available from: 2015-10-27 Created: 2015-10-27 Last updated: 2016-02-01Bibliographically approved
5. Quantitative trait locus and genetical genomics analysis identifies putatively causal genes for fecundity and brooding in the chicken
Open this publication in new window or tab >>Quantitative trait locus and genetical genomics analysis identifies putatively causal genes for fecundity and brooding in the chicken
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2016 (English)In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 6, no 2, 311-319 p.Article in journal (Refereed) Published
Abstract [en]

Life history traits such as fecundity are important to evolution because they make up components of lifetime fitness. Due to their polygenic architectures, such traits are difficult to investigate with genetic mapping. Therefore, little is known about their molecular basis. One possible way toward finding the underlying genes is to map intermediary molecular phenotypes, such as gene expression traits. We set out to map candidate quantitative trait genes for egg fecundity in the chicken by combining quantitative trait locus mapping in an advanced intercross of wild by domestic chickens with expression quantitative trait locus mapping in the same birds. We measured individual egg fecundity in 232 intercross chickens in two consecutive trials, the second one aimed at measuring brooding. We found 12 loci for different aspects of egg fecundity. We then combined the genomic confidence intervals of these loci with expression quantitative trait loci from bone and hypothalamus in the same intercross. Overlaps between egg loci and expression loci, and trait–gene expression correlations identify 29 candidates from bone and five from hypothalamus. The candidate quantitative trait genes include fibroblast growth factor 1, and mitochondrial ribosomal proteins L42 and L32. In summary, we found putative quantitative trait genes for egg traits in the chicken that may have been affected by regulatory variants under chicken domestication. These represent, to the best of our knowledge, some of the first candidate genes identified by genome-wide mapping for life history traits in an avian species.

Place, publisher, year, edition, pages
Bethesda, MD, United States: Genetics Society of America, 2016
National Category
Genetics
Identifiers
urn:nbn:se:liu:diva-124211 (URN)10.1534/g3.115.024299 (DOI)000369595300008 ()26637433 (PubMedID)
Note

At the time for thesis presentation publication was in status: Manuscript

At the time for thesis presentation manuscript was named: Quantitative trait locus and genetical genomics analysis identifies putatively causal genes for fecundity and brooding behavior in the chicken

Funding agencies: Swedish Research Council (VR); Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS); European Research Council

Available from: 2016-01-22 Created: 2016-01-22 Last updated: 2017-11-30Bibliographically approved
6. Mixed ancestry and admixture in Kauai's feral chickens: invasion of domestic genes into ancient Red Junglefowl reserviors
Open this publication in new window or tab >>Mixed ancestry and admixture in Kauai's feral chickens: invasion of domestic genes into ancient Red Junglefowl reserviors
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2015 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 24, no 9, 2112-2124 p.Article in journal (Refereed) Published
Abstract [en]

A major goal of invasion genetics is to determine how establishment histories shape non-native organisms' genotypes and phenotypes. While domesticated species commonly escape cultivation to invade feral habitats, few studies have examined how this process shapes feral gene pools and traits. We collected genomic and phenotypic data from feral chickens (Gallus gallus) on the Hawaiian island of Kauai to (i) ascertain their origins and (ii) measure standing variation in feral genomes, morphology and behaviour. Mitochondrial phylogenies (D-loop & whole Mt genome) revealed two divergent clades within our samples. The rare clade also contains sequences from Red Junglefowl (the domestic chicken's progenitor) and ancient DNA sequences from Kauai that predate European contact. This lineage appears to have been dispersed into the east Pacific by ancient Polynesian colonists. The more prevalent MtDNA clade occurs worldwide and includes domesticated breeds developed recently in Europe that are farmed within Hawaii. We hypothesize this lineage originates from recently feralized livestock and found supporting evidence for increased G. gallus density on Kauai within the last few decades. SNPs obtained from whole-genome sequencing were consistent with historic admixture between Kauai's divergent (G. gallus) lineages. Additionally, analyses of plumage, skin colour and vocalizations revealed that Kauai birds' behaviours and morphologies overlap with those of domestic chickens and Red Junglefowl, suggesting hybrid origins. Together, our data support the hypotheses that (i) Kauai's feral G. gallus descend from recent invasion(s) of domestic chickens into an ancient Red Junglefowl reservoir and (ii) feral chickens exhibit greater phenotypic diversity than candidate source populations. These findings complicate management objectives for Pacific feral chickens, while highlighting the potential of this and other feral systems for evolutionary studies of invasions.

Place, publisher, year, edition, pages
John Wiley & Sons, 2015
Keyword
conservation genetics, Gallius gallus, hybridization, invasive species
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:liu:diva-117160 (URN)10.1111/mec.13096 (DOI)000353928200014 ()25655399 (PubMedID)
Available from: 2015-04-20 Created: 2015-04-20 Last updated: 2017-12-04
7. Feralisation targets different genomic loci to domestication in the chicken.
Open this publication in new window or tab >>Feralisation targets different genomic loci to domestication in the chicken.
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2016 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 7, 12950Article in journal (Refereed) Published
Abstract [en]

Feralisation occurs when a domestic population recolonizes the wild, escaping its previous restricted environment, and has been considered as the reverse of domestication. We have previously shown that Kauai Island's feral chickens are a highly variable and admixed population. Here we map selective sweeps in feral Kauai chickens using whole-genome sequencing. The detected sweeps were mostly unique to feralisation and distinct to those selected for during domestication. To ascribe potential phenotypic functions to these genes we utilize a laboratory-controlled equivalent to the Kauai population-an advanced intercross between Red Junglefowl and domestic layer birds that has been used previously for both QTL and expression QTL studies. Certain sweep genes exhibit significant correlations with comb mass, maternal brooding behaviour and fecundity. Our analyses indicate that adaptations to feral and domestic environments involve different genomic regions and feral chickens show some evidence of adaptation at genes associated with sexual selection and reproduction.

Place, publisher, year, edition, pages
London: Nature Publishing Group, 2016
National Category
Genetics
Identifiers
urn:nbn:se:liu:diva-122279 (URN)10.1038/ncomms12950 (DOI)000385444300002 ()27686863 (PubMedID)
Note

The prevous status of this article was Manuscript and the title was The genomic signals of feralisation: Not just domestication in reverse?

Funding agencies: We thank Tony Lydgate and the Steelgrass Institute for invaluable assistance and accommodation on Kauai. The research was carried out within the framework of the Linkoping University Neuro-network. WGS was performed by the Uppsala Genome Center as part of NGI Sweden. Computations were performed at UPPMAX as part of SNIC Sweden. The project was supported by grants from the Swedish Research Council (VR), the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS), the Carl Trygers Stiftelse and by the National Science Foundation under Cooperative Agreement No. DBI-0939454. S.L. is supported by BBSRC (grant number BB/L009382/1). L.V.D. is supported by CoMPLEX via EPSRC (grant number EP/F500351/1). G.H. is supported by a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society (grant number 098386/Z/12/Z) and supported by the National Institute for Health Research University College London Hospitals Biomedical Research Centre. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Available from: 2015-10-27 Created: 2015-10-27 Last updated: 2017-12-01Bibliographically approved

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