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The evolutionary history of grey wolf Y chromosomes
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-8415-9259
Nat Resources Inst Finland Luke, Rovaniemi, Finland.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-5035-1736
2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 9, p. 2173-2191Article in journal (Refereed) Published
Abstract [en]

Analyses of Y chromosome haplotypes uniquely provide a paternal picture of evolutionary histories and offer a very useful contrast to studies based on maternally inherited mitochondrial DNA (mtDNA). Here we used a bioinformatic approach based on comparison of male and female sequence coverage to identify 4.7 Mb from the grey wolf (Canis lupis) Y chromosome, probably representing most of the male-specific, nonampliconic sequence from the euchromatic part of the chromosome. We characterized this sequence and then identified approximate to 1,500 Y-linked single nucleotide polymorphisms in a sample of 145 resequenced male wolves, including 75 Finnish wolf genomes newly sequenced in this study, and in 24 dogs and eight other canids. We found 53 Y chromosome haplotypes, of which 26 were seen in grey wolves, that clustered in four major haplogroups. All four haplogroups were represented in samples of Finnish wolves, showing that haplogroup lineages were not partitioned on a continental scale. However, regional population structure was indicated because individual haplotypes were never shared between geographically distant areas, and genetically similar haplotypes were only found within the same geographical region. The deepest split between grey wolf haplogroups was estimated to have occurred 125,000 years ago, which is considerably older than recent estimates of the time of divergence of wolf populations. The distribution of dogs in a phylogenetic tree of Y chromosome haplotypes supports multiple domestication events, or wolf paternal introgression, starting 29,000 years ago. We also addressed the disputed origin of a recently founded population of Scandinavian wolves and observed that founding as well as most recent immigrant haplotypes were present in the neighbouring Finnish population, but not in sequenced wolves from elsewhere in the world, or in dogs.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019. Vol. 28, no 9, p. 2173-2191
Keywords [en]
bioinfomatics, phyloinfomatics, conservation genetics, haplotypes, population genomics, Y chromosome
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-389874DOI: 10.1111/mec.15054ISI: 000471073000005PubMedID: 30788868OAI: oai:DiVA.org:uu-389874DiVA, id: diva2:1339867
Funder
Swedish Research CouncilKnut and Alice Wallenberg FoundationAvailable from: 2019-07-31 Created: 2019-07-31 Last updated: 2023-12-15Bibliographically approved
In thesis
1. Conservation genomics in inbred Scandinavian wolves using bioinformatic methods
Open this publication in new window or tab >>Conservation genomics in inbred Scandinavian wolves using bioinformatic methods
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

With the recent and unprecedented progress in retrieving DNA sequence information from a large number of individuals of any species, conservation genetic research has entered a new phase. Specifically, it has become possible to study how genomes of endangered species respond to reductions in population size. Using genomic and bioinformatic approaches, in this thesis I investigate the contemporary Scandinavian wolf population founded 40 years ago by only three individuals, after the original population had been extirpated some decades earlier. The origin of the founders has been the subject of controversy, so I aimed to trace their origin using first male-specific Y chromosome sequences, and then whole-genome sequence data. I compared Scandinavian wolves to wolves from the nearby Finnish-Russian population as well as to publicly available wolf and dog samples from around the northern hemisphere, and found that the Scandinavian founders shared Y-haplotypes only with Finnish wolves. Consistent with this observation, when assessing population structure on the genomic scale, founders clustered with Finnish and Russian wolves, and an admixture analysis showed no other ancestries, nor traces of introgression from dogs. 

Small populations tend to have less genetic variation than larger populations, which might reduce their adaptive potential and increase the risk for extinction. A common measure used to investigate the genetic health of small populations is the genetic load, which is the fitness reduction of individuals due to accumulation of deleterious variants. I assessed the genetic load in Scandinavian wolves, divided into the components masked load (comprised of deleterious mutations in heterozygous state) and realized load (comprised of deleterious mutations in homozygous state), using both putatively deleterious single nucleotides and structural variants. I found that the realized load increased with every generation of inbreeding but was alleviated after genetic rescue events when new immigrants entered the population. Finally, I searched for the genetic basis of cryptorchidism, a testis condition that results in lowered fertility and is thought to be related to inbreeding depression. The trait is likely highly polygenic and the fact that only one significant association (to a region on the X chromosome) was found can be explained by that the number of available samples was very low, as is inevitable for small populations. 

In conclusion, this thesis explores the origin and the genetic health status of a small and recently founded natural population, and gives insights into how patterns of genetic load are affected by inbreeding and genetic rescue.  

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2024. p. 65
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2351
Keywords
conservation genomics, Canis lupus, bioinformatics, Y chromosome, admixture, genetic load, structural variation, GWAS
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-517653 (URN)978-91-513-1998-8 (ISBN)
Public defence
2024-02-16, Zootissalen, EBC, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2024-01-24 Created: 2023-12-15 Last updated: 2024-01-24

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Smeds, LinneaEllegren, Hans

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