1. Evolutionary Biology
  2. Genetics and Genomics
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Demographic reconstruction from ancient DNA supports rapid extinction of the great auk

  1. Jessica E Thomas  Is a corresponding author
  2. Gary R Carvalho
  3. James Haile
  4. Nicolas J Rawlence
  5. Michael D Martin
  6. Simon YW Ho
  7. Arnór Þ Sigfússon
  8. Vigfús A Jósefsson
  9. Morten Frederiksen
  10. Jannie F Linnebjerg
  11. Jose A Samaniego Castruita
  12. Jonas Niemann
  13. Mikkel-Holger S Sinding
  14. Marcela Sandoval-Velasco
  15. André ER Soares
  16. Robert Lacy
  17. Christina Barilaro
  18. Juila Best
  19. Dirk Brandis
  20. Chiara Cavallo
  21. Mikelo Elorza
  22. Kimball L Garrett
  23. Maaike Groot
  24. Friederike Johansson
  25. Jan T Lifjeld
  26. Göran Nilson
  27. Dale Serjeanston
  28. Paul Sweet
  29. Errol Fuller
  30. Anne Karin Hufthammer
  31. Morten Meldgaard
  32. Jon Fjeldså
  33. Beth Shapiro
  34. Michael Hofreiter
  35. John R Stewart
  36. M Thomas P Gilbert
  37. Michael Knapp  Is a corresponding author
  1. Bangor University, United Kingdom
  2. University of Copenhagen, Denmark
  3. University of Otago, New Zealand
  4. Norwegian University of Science and Technology, Norway
  5. University of Sydney, Australia
  6. Verkís Consulting Engineers, Iceland
  7. Aarhus University, Denmark
  8. Greenland Institute of Natural Resources, Greenland
  9. University of California Santa Cruz, United States
  10. Chicago Zoological Society, United States
  11. Landesmuseum Natur und Mensch Oldenburg, Germany
  12. Bournemouth University, United Kingdom
  13. Cardiff University, United Kingdom
  14. University of Kiel, Germany
  15. University of Amsterdam, Netherlands
  16. Sociedad de Ciencias Aranzadi, Spain
  17. Natural History Museum of Los Angeles County, United States
  18. Freie Universität Berlin, Germany
  19. Gothenburg Museum of Natural History, Sweden
  20. University of Oslo, Norway
  21. University of Southampton, United Kingdom
  22. American Museum of Natural History, United States
  23. Independent researcher, United Kingdom
  24. University Museum of Bergen, Norway
  25. University of Greenland, Greenland
  26. University of Potsdam, Germany
Research Article
Cite this article as: eLife 2019;8:e47509 doi: 10.7554/eLife.47509
12 figures, 4 tables and 4 additional files

Figures

The great auk and its former distribution in the North Atlantic.

Red shading indicates the geographic distribution of the great auk, as defined by BirdLife International/IUCN (BirdLife International, 2016a). Sites marked with blue dots represent samples used in our analyses. Black dots denote other sites from which material was obtained, but for which samples were not sequenced or for which sequences did not pass filtering settings. Numbers associated with blue dots correspond to the following sites: 1: Funk Island (n = 14), 2: Qeqertarsuatsiaat (n = 1), 3: Eldey Island (n = 2), 4: Iceland (n = 5), 5: Tofts Ness (n = 2), 6: Bornais (n = 1), 7: Cladh Hallan (n = 1), 8: Portland (n = 1), 9: Santa Catalina (n = 2), 10: Schipluiden (n = 1), 11: Velsen (n = 1), 12: Sotenkanalen (n = 2), 13: Skalbank Otterön (n = 2), 14: Kirkehlleren (n = 1), 15: Storbåthelleren (n = 1), 16: Iversfjord (n = 1), 17: Vardø (n = 2), and 18: Nyelv (n = 1).

Statistical parsimony network showing haplotype diversity of great auk mitogenomes through time.

In each age category observed haplotypes are shown in colour, absent haplotypes are shown as empty circles, and mutations between haplotypes are marked as black dots. All samples have been included in this figure.

Median-joining network of great auk mitogenomes.

The network was inferred in PopART18 and shows a lack of phylogeographic structure among the dated and undated samples of great auks. Haplotypes are coloured according to sampling location.

Routes taken by GPS capsules in the North Atlantic.

The map shows GPS data from two capsules (green and yellow lines). These tracks show possible routes that the great auk might have used to move between colonies, aided by ocean currents, waves, and wind. Legend: Red Star: Known breeding sites of the great auk (Funk Island, New Newfoundland; Eldey Island, Iceland; St Kilda, Scotland). Green line: GPS capsule 1. Yellow line: GPS capsule 2. Pink arrows: Warm sea currents (Gulf Stream and North Atlantic Drift). Dark blue arrows: Cold sea currents (East Greenland Current and Labrador Current).

Great auk humeri following sampling.

Great auk humeri, collected from Funk Island, following sampling to collect bone powder for use in DNA extraction. Bones part of the collection at the American Museum of Natural History (Credit: J. Thomas).

Appendix 1—figure 1
Phylogenetic tree showing the relationships among dated mitogenomes from the great auk.

This maximum-clade-credibility tree was inferred by Bayesian analysis in BEAST. Nodes are labelled with posterior probabilities. The tree is drawn to a timescale, as indicated by the horizontal scale bar. Samples included in the analysis are those with associated date information (see Supplementary file 1e). For samples with a stratigraphically assigned date the median age has been used. Tip labels give the sample names, sampling locations, and sample ages (years before present, with the exception of mounted specimens labelled YA- years ago).

Appendix 1—figure 2
Phylogenetic tree showing the relationships among dated and undated mitogenomes from the great auk.

This maximum-clade-credibility tree was inferred by Bayesian analysis in BEAST. Nodes are labelled with posterior probabilities. The tree is drawn to a timescale, as indicated by the horizontal scale bar. Samples included in the analysis are those with and without associated date information (Supplementary file 1e). For samples with a stratigraphically assigned date the median age has been used. Tip labels give the sample names, sampling locations, and sample ages (years before present, with the exception of mounted specimens labelled YA- years ago).

Appendix 3—figure 1
Date-randomisation test for temporal structure in dated mitogenome sequences.

The filled circle indicates the median posterior estimate of the mutation rate from the original data set, whereas the empty circles show the median posterior estimates from 20 date-randomised replicate data sets. The 95% credibility intervals (vertical black lines) of the estimates from the date-randomised replicates do not overlap with the median estimate from the original data set, providing some evidence of temporal structure in the data set (criterion CR1). However, the 95% credibility intervals of the estimates from the date-randomised replicates overlap with the 95% credibility interval of the estimate from the original data set, indicating that the data set does not meet the more stringent criterion CR2.

Appendix 4—figure 1
Hybrid reference mitogenome used for bait design.

Illustration of the hybrid reference mitogenome constructed using the killdeer (Charadrius vociferous) mitogenome, with orthologous gene regions replaced by those of the great auk (Pinguinus impennis), or razorbill (Alca torda), when great auk data were unavailable. Annotations correspond to the various regions of the mitogenome: those in blue show where great auk or razorbill genes have been used; yellow corresponds to coding regions; green shows all gene regions; the D-loop is shown in gold; rRNA regions are in red; tRNA regions are in pink; and any miscellaneous features are in grey. The numbers on the outer black circle correspond to the base position of the mitogenome.

Appendix 9—figure 1
Section of the presence/absence matrix showing coverage of 30/495 captured genes (listed on the right-hand side) for each sample sent for sequencing.

Presence is defined as coverage >= 3, indicated by a red square, absence is indicated by a blue square.

Appendix 10—figure 1
Phylogenetic tree showing the relationship between all samples that passed filtering criteria, plus additional Spanish samples previously excluded from analysis.

The evolutionary history was inferred using the Neighbor-Joining method (Saitou and Nei, 1987) in MEGAX (Kumar et al., 2018). The optimal tree with the sum of branch length = 0.01164144 is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches (Felsenstein, 1985). The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the p-distance method (Nei and Kumar, 2000) and are in the units of the number of base differences per site. This analysis involved 43 nucleotide sequences. All positions containing gaps and missing data were eliminated (complete deletion option). There were a total of 859 positions in the final dataset. Tip labels give the sample names and sampling locations.

Author response image 1
The evolutionary history was inferred using the Neighbor-Joining method [Saitou and Nei, 1987].

The optimal tree with the sum of branch length = 0.01164144 is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches [Felsenstein, 1985]. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the p-distance method [Nei and Kumar, 2000] and are in the units of the number of base differences per site. This analysis involved 43 nucleotide sequences. All positions containing gaps and missing data were eliminated (complete deletion option). There were a total of 859 positions in the final dataset. Evolutionary analyses were conducted in MEGA X [Kumar et al., 2018].

Tables

Table 1
Population viability analysis.

Extinction is defined as ‘only one sex remains’. The number of mature individuals was estimated in Vortex 10.2.8.0, assuming a stable age distribution and given our fixed mortality rates. ‘Maximum- number of eggs’ refers to the number of eggs that would be produced if all mature individuals were breeding. ‘Harvest rate’ describes the percentage of the population that is harvested annually, with egg harvest rate calculated from the maximum number of eggs in parentheses. ‘DD’ refers to density-dependent reduction of mortality. ‘Number of birds’ is the total number of birds killed annually, which was split between the age cohorts (see Appendix 8). ‘Number of eggs’ is total number of eggs harvested annually.

Conservative settings
Population size
(total)
Mature birds
(>4 years)
Maximum number of eggsHarvest rate
(% of starting population size)
DDNumber of birdsNumber of eggsProbability of extinction within 350 years
2,000,0001,027,532513,7669 (5)No180,00025,6880.00
2,000,0001,027,532513,76610 (5)No200,00025,6880.79
2,000,0001,027,532513,76610 (5)Yes200,00025,6880.22
2,000,0001,027,532513,76610.5 (5)Yes210,00025,6881.00
2,000,0001,027,532513,76610.5 (0)No210,00000.71
2,000,0001,027,532513,76610.5 (0)Yes210,00000.19
6,000,0003,082,5941,541,2979 (5)No540,00077,0650.00
6,000,0003,082,5941,541,29710 (5)No600,00077,0650.86
6,000,0003,082,5941,541,29710 (5)Yes600,00077,0650.33
6,000,0003,082,5941,541,29710.5 (5)Yes630,00077,0651.00
6,000,0003,082,5941,541,29710.5 (0)No600,00000.81
6,000,0003,082,5941,541,29710.5 (0)Yes630,00000.15
‘Realistic’ settings
Population size
(total)
Mature birds
(>5 years)
Maximum number of eggsHarvest rate
(% of starting population size)
DDNumber of birdsNumber of eggsProbability of extinction within 350 years
2,000,0001,027,532513,7662 (0)Yes40,00000.19–0.33
(range across multiple repeat simulations)
Appendix 6—table 1
Marginal likelihoods of six partitioning schemes and two tree priors for the 25 dated mitogenomes.
Partitioning schemeaMarginal likelihoodb
Constant sizeExponential growth
Unpartitioned−24,151.6−24,143.6
two subsets: (CR rRNA tRNA) (PC1 PC2 PC3)−24,222.3−24,212.4
three subsets: (CR) (rRNA tRNA) (PC1 PC2 PC3)−24,162.4−24,150.1
four subsets: (CR) (rRNA tRNA) (PC1 PC2) (PC3)−23,659.7−23,647.5
five subsets: (CR) (rRNA tRNA) (PC1) (PC2) (PC3)−23,248.7−23,235.9
six subsets: (CR) (rRNA) (tRNA) (PC1) (PC2) (PC3)−23,229.1−23,217.5
  1. aComponents of the mitogenome are the ribosomal RNA genes (rRNA), transfer RNA genes (tRNA), three codon positions of the protein-coding genes (PC1, PC2, and PC3), and the control region (CR). bMarginal likelihoods were estimated by stepping-stone sampling with 25 path steps, each with a chain length of 2,000,000 steps.

Appendix 9—table 1
Estimated coverage information from the twelve sequenced samples.

The estimated coverage of the 495 targeted genes and estimated coverage of the reads that mapped to the razorbill genome is reported.

SampleCountryEstimated coverage of razorbill genomeEstimated coverage of targeted genes
MK49Norway0.01010.0152
MK50Iceland0.01900.0155
MK78Funk Island0.00220.0018
MK83Funk Island0.000060.0071
MK103Funk Island0.00110.0150
MK106Sweden0.01720.0105
MK115Norway0.00120.0021
MK131Iceland0.00900.0423
MK133Skin Mystery0.01900.0154
MK134Skin Mystery0.01791.2592
MK135Skin Mystery0.00730.0106
MK136Skin Mystery0.00210.0128
Appendix 9—table 2
Coverage range of captured markers.

Numbers in square brackets represent the number of markers which have 0 coverage. Genes with the highest coverage are shown in brackets.

SampleCountryCoverage range
of captured markers
MK49Norway0 [125] – 0.4898 (Fam174b)
MK50Iceland0 [157] – 0.2204 (Isca2)
MK78Funk Island0 [379] – 0.1087 (Mrp130)
MK83Funk Island0 [223] – 0.2960 (Nipbl)
MK103Funk Island0 [164] – 0.7049 (Glrx5)
MK106Sweden0 [190] – 0.2403 (Pcp4)
MK115Norway0 [366] – 0.2263 (Tmem60)
MK131Iceland0[78] – 1.5238 (Ssna1)
MK133Skin mystery0 [129] – 0.3061 (Fam174b)
MK134Skin mystery0.0628 (TPK1) – 17.7232 (Ssna1)
MK135Skin mystery0 [172] – 0.2580 (myct1)
MK136Skin mystery0 [142] – 0.4067 (myct1)

Additional files

Source data 1

Nuclear SNP bait design.

https://cdn.elifesciences.org/articles/47509/elife-47509-data1-v1.zip
Supplementary file 1

Sample Information.

Supplementary file 1a Sample information for all samples collected. Information listed shows institution name and number where sample was sourced, the site location and country where sample was discovered (if known), and any associated date/age information, if known. Those highlighted indicate samples that ultimately passed the filtering settings and were used in the final analysis. Asterisks indicate samples from Thomas et al. (2017). Supplementary file 1b Lab process table for all samples collected. Table includes information on sample type, weight used in extraction, which library build method was used, if hybridization capture was used, and which type of sequencing was performed. Those highlighted indicate samples that ultimately passed the filtering settings and were used in the final analysis. Asterisks indicate samples from Thomas et al. (2017). Supplementary file 1c PALEOMIX summary data for mitogenome samples. Summary statistics table from all great auk samples sent for sequencing. Library type: PE = Paired end, SE = Single end, *=both. Samples highlighted were used in final analysis. Supplementary file 1d GenBank accession numbers. GenBank accession numbers for samples used in analysis. Supplementary file 1e Age information for samples used in analysis. Age information for samples used in the BEAST and TempNet analyses.

https://cdn.elifesciences.org/articles/47509/elife-47509-supp1-v1.xlsx
Supplementary file 2

Population Viability Analysis Settings.

Supplementary file 2a Settings used in Population Viability Analysis. Details of the settings used for Population Viability Analysis performed in Vortex 10.2.8.0. Information displayed corresponds to the various setting sections in the software and the variables that were changed. Further details on justification for these settings can be found in Appendix 8. Supplementary file 2b Details of mortality rates used in Population Viability Analysis. Details of the mortality rate settings used in Population Viability Analysis performed in Vortex 10.2.8.0, showing formula information for including density-dependent change and additional justification. Supplementary file 2c Harvest rate calculations. Example of how harvest rates of birds and eggs were calculated for the Population Viability Analysis.

https://cdn.elifesciences.org/articles/47509/elife-47509-supp2-v1.xlsx
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https://cdn.elifesciences.org/articles/47509/elife-47509-transrepform-v1.pdf

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