Demographic histories and genetic diversity across pinnipeds are shaped by human exploitation, ecology and life-history

  1. M. A. Stoffel
  2. E. Humble
  3. A. J. Paijmans
  4. K. Acevedo-Whitehouse
  5. B. L. Chilvers
  6. B. Dickerson
  7. F. Galimberti
  8. N. J. Gemmell
  9. S. D. Goldsworthy
  10. H. J. Nichols
  11. O. Krüger
  12. S. Negro
  13. A. Osborne
  14. T. Pastor
  15. B. C. Robertson
  16. S. Sanvito
  17. J. K. Schultz
  18. A. B. A. Shafer
  19. J. B. W. Wolf
  20. J. I. Hoffman

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Abstract

A central paradigm in conservation biology is that population bottlenecks reduce genetic diversity and population viability. In an era of biodiversity loss and climate change, understanding the determinants and consequences of bottlenecks is therefore an important challenge. However, as most studies focus on single species, the multitude of potential drivers and the consequences of bottlenecks remain elusive. Here, we combined genetic data from over 11,000 individuals of 30 pinniped species with demographic, ecological and life history data to evaluate the consequences of commercial exploitation by 18th and 19th century sealers. We show that around one third of these species exhibit strong signatures of recent population declines. Bottleneck strength is associated with breeding habitat and mating system variation, and together with global abundance explains much of the variation in genetic diversity across species. Overall, bottleneck intensity is unrelated to IUCN status, although the three most heavily bottlenecked species are endangered. Our study reveals an unforeseen interplay between human exploitation, animal biology, demographic declines and genetic diversity.

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  1. Version published to 10.1038/s41467-018-06695-z
  2. PREreview

    This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/7728420.

    PREreview from the OIST Ecology and Evolution Preprint Journal Club

    Recent demographic histories and genetic diversity across pinnipeds are shaped by anthropogenic interactions and mediated by ecology and life-history  Martin Adam Stoffel, Emily Humble, Karina Acevedo-Whitehouse, Barbara L. Chilvers, Bobette Dickerson, Fillipo Galimberti, Neil Gemmell, Simon D. Goldsworthy, Hazel J. Nichols, Oliver Krueger, Sandra Negro, Amy Osborne, Anneke J. Paijmans, Teresa Pastor, Bruce C. Robertson, Simona Sanvito, Jennifer Schultz, Aaron B.A. Shafer, Jochen B.W. Wolf, Joseph I. Hoffman,  April 12, 2018, version 1, bioRxiv doi: https://doi.org/10.1101/293894

    Firstly, we thank the authors for their work and for posting it as a preprint on bioRxiv. This work endeavored to evaluate the occurrence and intensity of population bottlenecks in a large number of pinniped species that have been differentially affected by human exploitation. Population bottlenecks can decrease genetic diversity and adversely affect the ability of a species to adapt to modern habitat loss and climate change. Because historical data is sparse and unreliable, the authors applied population genetics methods to a large, multi-species dataset to detect and evaluate past population bottlenecks and then compared the results to life-history traits and current conservation status for each species. The results indicate that 11 of the species included in the analysis experienced a population bottleneck and that land-breeding pinnipeds are more likely to have experienced a bottleneck than ice-breeding pinnipeds. While there was not an overall relationship between IUCN status and past bottleneck events, bottleneck events were detected for 4 of the 6 endangered species included in the study. The breadth of this study is especially important, as it represents a first effort to apply these methods across 30 species in a single analysis. Our overall impression is that this was a large project using an extensive amount of data from multiple sources, which then had to be standardized in order to be analyzed in a novel way. This paper highlights the benefits of open science and open data, as data from multiple studies was reused and analyzed in a far broader context than any single study on a single population or species.

    This manuscript is exceptionally well-written and uses clear language, making it both easy and enthralling to read. However, there are a few small mistakes that caused some confusion. Particularly, the caption of Figure 4 switches the descriptions for Panels A and B. Additionally, the figures in the main text are numbered 1:4, 6; it appears that Figure 5 may have been moved to the supplemental materials, but the main figure numbering was not adjusted accordingly. 

    All of the figures in the manuscript are very attractive and make good use of consistent coloring. Figure 1 nicely summarizes many of the main findings of the paper. This figure would be even better if Panel A utilized a 2-color scale like Panels B and C. Additionally since Pbot and Pneut are complementary, we suggest that only Pbot needs to be included in Panel C, which will reduce the size of the figure and make it easier to interpret. Figure 2 is very clear and intuitive and nicely illustrates the intensity of population bottlenecks for different species. Additionally, the pinniped drawings are beautiful and the use of original artwork in the paper is commendable. We feel that Figure 4, which displays the expected correlation between global abundance and allelic richness does not necessarily need to be included in the main text. Conversely, we feel that Supplementary Table 1, which contains the sample size, number of microsatellite loci, and citation for each species' dataset, is important for readers to have available in the main text. Overall, the authors did an outstanding job applying population genetics techniques appropriately. In particular, the authors made very good use of the program STRUCTURE. This program was used to detect population substructure and if detected, the largest genetic cluster was selected for inclusion in ensuing analyses. This important step prevents false detection of bottlenecks, which can be a common mistake. It is also appreciated that the authors chose to examine allelic richness rather than allelic frequency. We were left with a few lingering questions about the methods, however. First, we are curious if the authors acquired raw electropherograms or pre-interpreted genotypes for the published datasets used and if there were any measures taken to control for observer bias in interpreting microsatellite genotypes, such as preparing and running samples from other labs and assessing whether similar conclusions were reached. We were also curious about the justification for grouping IUCN categories into "concern" ('near threatened,' 'vulnerable,' and 'endangered') and "least concern" ('least concern'), especially since the IUCN Red List Categories and Criteria groups 'near threatened' with 'least concern' and explicitly distinguishes 'vulnerable,' 'endangered,' and 'critically endangered' as the "threatened" categories. We wonder how the results presented in Figure 6 would be affected by moving the species designated as 'near threatened' out of the "concern" category.

    Lastly, we would have appreciated a more extensive discussion. For example, the authors describe ice-breeding species as experiencing less historical exploitation than the land-breeding species, but ice-breeding species are likely more susceptible to negative impacts from climate change in the recent past and into the future. The implications of the findings of the study combined with change in anthropogenic disturbance patterns and continuing disturbance  in these habitats into the future could be addressed in the discussion. We are also very interested in what the authors perceive as weaknesses in the approaches used, if there may be alternative interpretations of the results, and especially what future studies they would suggest based on their results and conclusions. Again, it was a great pleasure reading this impressive work. We hope that our comments are useful to the authors and we look forward to reading the final version when it is published. 

    Thank you!

    The OIST Ecology and Evolution Preprint Journal Club 

  3. Version published to 10.1101/293894v2 on bioRxiv
  4. Version published to 10.1101/293894v1 on bioRxiv