Mitogenomic analysis of a 50-generation chicken pedigree reveals a rapid rate of mitochondrial evolution and evidence for paternal mtDNA inheritance.
Mitochondrial genomes represent a valuable source of data for evolutionary research, but studies of their short-term evolution have typically been limited to invertebrates, humans and laboratory organisms. Here we present a detailed study of 12 mitochondrial genomes that span a total of 385 transmissions in a well-documented 50-generation pedigree in which two lineages of chickens were selected for low and high juvenile body weight. These data allowed us to test the hypothesis of time-dependent evolutionary rates and the assumption of strict maternal mitochondrial transmission, and to investigate the role of mitochondrial mutations in determining phenotype. The identification of a non-synonymous mutation in ND4L and a synonymous mutation in CYTB, both novel mutations in Gallus, allowed us to estimate a molecular rate of 3.13 × 10(-7) mutations/site/year (95% confidence interval 3.75 × 10(-8)-1.12 × 10(-6)). This is substantially higher than avian rate estimates based upon fossil calibrations. Ascertaining which of the two novel mutations was present in an additional 49 individuals also revealed an instance of paternal inheritance of mtDNA. Lastly, an association analysis demonstrated that neither of the point mutations was strongly associated with the phenotypic differences between the two selection lines. Together, these observations reveal the highly dynamic nature of mitochondrial evolution over short time periods.
BioArCh Biology S Block, University of York, Wentworth Way, Heslington, York YO10 5DD, UK Department of Archaeology, School of Geosciences, University of Aberdeen, St. Mary's, Elphinstone Road, AB24 3UF, UK.
Michelle
http://orcid.org/0000-0001-8000-3639
M
Alexander
School of Biological Sciences, University of Sydney, Sydney, New South Wales 2006, Australia.
Simon Y W
http://orcid.org/0000-0002-0361-2307
SY
Ho
Museum and Institute of Zoology, Polish Academy of Sciences, Warsaw 00-679, Poland.
Martyna
http://orcid.org/0000-0001-5068-8649
M
Molak
Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK.
Ross
R
Barnett
Department of Clinical Sciences, Swedish University of Agricultural Sciences, PO Box 7078, 75007 Uppsala, Sweden.
Örjan
Ö
Carlborg
Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, PO Box 582, 75123 Uppsala, Sweden Department of Animal and Poultry Sciences, Virginia Tech, Blacksburg, VA 24061, USA.
Ben
B
Dorshorst
Department of Animal and Poultry Sciences, Virginia Tech, Blacksburg, VA 24061, USA.
Christa
C
Honaker
Section of Population Genetics, Institute of Marine Research, Nordnes 5817, Bergen, Norway.
Francois
F
Besnier
Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, PO Box 582, 75123 Uppsala, Sweden.
Per
P
Wahlberg
Department of Archaeology, School of Geosciences, University of Aberdeen, St. Mary's, Elphinstone Road, AB24 3UF, UK.
Keith
K
Dobney
Department of Animal and Poultry Sciences, Virginia Tech, Blacksburg, VA 24061, USA.
Paul
P
Siegel
Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, PO Box 582, 75123 Uppsala, Sweden Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, PO Box 7023, 75007 Uppsala, Sweden.
Leif
L
Andersson
Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK greger.larson@arch.ox.ac.uk.
Greger
G
Larson
D000818:Animals; D000831:Animals, Newborn; D005075:Biological Evolution; D001835:Body Weight; D002645:Chickens / Q000235:genetics*; D004272:DNA, Mitochondrial / Q000235:genetics*; D005260:Female; D054629:Genome, Mitochondrial; D008297:Male; D008928:Mitochondria / Q000235:genetics*; D059645:Mutation Rate; D010375:Pedigree; D013997:Time Factors
D004272:DNA, Mitochondrial
association analysis; mitochondrial genome; mutation rates; paternal leakage; pedigree