Genetic diversity loss in a biodiversity hotspot: ancient DNA quantifies genetic decline and former connectivity in a critically endangered marsupial.
The extent of genetic diversity loss and former connectivity between fragmented populations are often unknown factors when studying endangered species. While genetic techniques are commonly applied in extant populations to assess temporal and spatial demographic changes, it is no substitute for directly measuring past diversity using ancient DNA (aDNA). We analysed both mitochondrial DNA (mtDNA) and nuclear microsatellite loci from 64 historical fossil and skin samples of the critically endangered Western Australian woylie (Bettongia penicillata ogilbyi), and compared them with 231 (n = 152 for mtDNA) modern samples. In modern woylie populations 15 mitochondrial control region (CR) haplotypes were identified. Interestingly, mtDNA CR data from only 29 historical samples demonstrated 15 previously unknown haplotypes and detected an extinct divergent clade. Through modelling, we estimated the loss of CR mtDNA diversity to be between 46% and 91% and estimated this to have occurred in the past 2000-4000 years in association with a dramatic population decline. In addition, we obtained near-complete 11-loci microsatellite profiles from 21 historical samples. In agreement with the mtDNA data, a number of 'new' microsatellite alleles was only detected in the historical populations despite extensive modern sampling, indicating a nuclear genetic diversity loss >20%. Calculations of genetic diversity (heterozygosity and allelic rarefaction) showed that these were significantly higher in the past and that there was a high degree of gene flow across the woylie's historical range. These findings have an immediate impact on how the extant populations are managed and we recommend the implementation of an assisted migration programme to prevent further loss of genetic diversity. Our study demonstrates the value of integrating aDNA data into current-day conservation strategies.
Ancient DNA Laboratory, School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, 6150, Australia.
Carlo
C
Pacioni
Ancient DNA Laboratory, School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, 6150, Australia.
Helen
H
Hunt
Ancient DNA Laboratory, School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, 6150, Australia.|Centre for GeoGenetics, Natural History Museum, University of Copenhagen, Øster Voldgade 5-7, 1350, Copenhagen K, Denmark.
Morten E
ME
Allentoft
Department of Computer Science, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand.
Timothy G
TG
Vaughan
Department of Parks and Wildlife, Manjimup, WA, 6258, Australia.
Adrian F
AF
Wayne
Western Australian Museum, Locked Bag 49, Welshpool DC, WA, 6986, Australia.
Alexander
A
Baynes
Ancient DNA Laboratory, School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, 6150, Australia.
Dalal
D
Haouchar
Archaeology, M257, The University of Western Australia, 35 Stirling Highway, Nedlands, WA, 6009, Australia.
Joe
J
Dortch
Ancient DNA Laboratory, School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, 6150, Australia.|Department of Environment and Agriculture, Trace and Environmental DNA Laboratory, Kent Street, Bentley, Perth, WA, 6845, Australia.
Michael
M
Bunce
D000818:Animals; D001315:Australia; D003247:Conservation of Natural Resources; D004272:DNA, Mitochondrial / Q000235:genetics; D056727:Endangered Species; D005580:Fossils; D051456:Gene Flow; D005819:Genetic Markers; D014644:Genetic Variation; D005828:Genetics, Population; D006239:Haplotypes; D008394:Marsupialia / Q000235:genetics*; D018895:Microsatellite Repeats; D008969:Molecular Sequence Data; D017422:Sequence Analysis, DNA
D004272:DNA, Mitochondrial; D005819:Genetic Markers
Bettongia; ancient DNA; biodiversity loss; genetic diversity; population bottleneck