Unraveling the genetic legacy of commercial whaling in bowhead whales and narwhals

  1. Evelien de Greef
  2. Claudio Müller
  3. Matt J. Thorstensen
  4. Steven H. Ferguson
  5. Cortney A. Watt
  6. Marianne Marcoux
  7. Stephen D. Petersen
  8. Colin J. Garroway

Reviewed by

Read the full article See related articles

Listed in

Log in to save this article

Abstract

Commercial whaling decimated many whale populations over several centuries. Bowhead whales ( Balaena mysticetus ) and narwhal ( Monodon monoceros ) have similar habitat requirements and are often seen together in the Canadian Arctic. Although their ranges overlap extensively, bowhead whales experienced significantly greater whaling pressure than narwhals. The different harvest histories but similar habitat requirements of these two species provide an opportunity to examine the demographic and genetic consequences of commercial whaling. We whole-genome resequenced Canadian Arctic bowhead whales and narwhals to delineate population structure and reconstruct demographic history. Bowhead whale effective population size sharply declined contemporaneously with the intense commercial whaling period. Narwhals instead exhibited recent growth in effective population size, reflecting limited opportunistic commercial harvest. Although the genetic diversity of bowhead whales and narwhals was similar, bowhead whales had more genetic diversity prior to commercial whaling and will likely continue to experience significant genetic drift in the future. In contrast, narwhals appear to have had long-term low genetic diversity and may not be at imminent risk of the consequences of the erosion of genetic diversity. This work highlights the importance of considering population trajectories in addition to genetic diversity when assessing the genetics of populations for conservation and management purposes.

Article activity feed

  1. PREreview

    This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/11455529.

    Commercial whaling created intense pressure on many whale populations and brought many close to extinction. While commercial whaling was halted due to its dangerous environmental impact, whale populations today are still recovering. The paper aimed to investigate the effects of commercial whaling on bowhead whales (Balaena mysticetus) and narwhals (Monodon monoceros) through assessments of each species' current genetic diversity and demographic history. Bowhead whales and narwhals experience differences in whaling pressure with bowhead whales being majorly pursued by whalers while narwhals were typically caught opportunistically. By comparing these two species, this study seeks to illustrate how the differences in whaling practices may impact current populations.

    Overall, the paper is addressing a major issue in conservation biology and displaying how genomic technologies can be incorporated to address major challenges when assessing management success like determining inbreeding evasion and population estimates. The authors found evidence that bowhead whales, which were the main target for whaling, experienced a sharp decline in population size which led to the evidence of a bottleneck (longer runs of homozygosity versus higher genetic diversity) resulting in inbreeding in today's individuals. The main area of concern for this paper is the power of the analyses presented to support the authors' claims. I particularly noticed the differences in reference quality and reliance on linkage disequilibrium-based methods for inferring recent population size. Reviewing the power of used methods and either adding different analyses that a less sensitive to demographic information, filtering, and recombination rate or adding justification for use of these sensitive methods may provide stronger support for their conclusions.

    Major point:

    ·      The researchers use recently developed methods that leverage the relationship between Ne, recombination rate, and linkage disequilibrium to estimate population size in the recent past. However, this approach for estimating Ne requires additional information for accurate estimation of demographic history that can be difficult to gather for non-model species. Moreover, the method is sensitive to certain demographic and filtering conditions (e.g. MAF thresholds) and biological variation in recombination rate. The paper did not provide information on how these challenges were addressed, which impacts confidence in their estimates of recent population size. A related issue is that the reference assemblies used for the basis of these analyses had quality differences in scaffold size. The bowhead whale genome consisted of many, small scaffolds versus the larger scaffolds in the narwhal genome. The authors could use simulation-based approaches to show that scaffold size does not impact their estimates of Ne or ROH to address this concern.  

    ·      The genome assemblies for each species differed dramatically in quality (regarding scaffold number, coverage, and assembly method) which resulted in different choices for filtering and made me concerned that this could impact the results and conclusions regarding genetic diversity, potentially ROH, and PSMC. More explicit details on how the authors overcame or evaluated these challenges would be beneficial for addressing these concerns. 

    ·      Authors pulled abundance measures from outside resources but might want to explain if measurements were single measures or coming from multiple estimates.

    ·      Shorter ROH is found for the narwhal compared to the bowhead whale but no information regarding the significance of the difference in size within the figure. It would be helpful for the authors to address the possibility that this may be driven by reference quality differences.

    ·      PSMC was used to assess historic demographic history, but this program relies on SNP density within genome fragments to generate population estimates. There is concern that the genome quality (shorter, disjointed scaffolds) could influence the findings. It would be helpful to have information on how this sensitivity was considered when generating results to provide confidence in results. Furthermore, bootstraps are missing in PSMC figures within the main text. Bootstrap results should be moved to main figures for proper assessment when reading. 

    Minor point:

    ·      The introduction of the paper explored several motivating topics including addressing consequences of whaling, importance of both species, and climate change. While all points are helpful to provide better understanding of the use of this study, points like climate change could be used more efficiently later in the conclusion to support the significance of the study versus provide motivation for this work.

    ·      Brief mention of Canada ban on whaling that can be expanded upon by giving information on the duration of whaling in Canada and effects of this practice in the introduction for added historical context and understanding of why this study is significant.

    ·      Figures are often referenced as the entire figure instead of referencing the independent components which can be difficult for a reader to follow.

    ·      Genome size for narwhal and bowhead reference genomes should be mentioned under genome information.

    ·      The colors in Figure 3a and 3c are a bit too subtle and hard to distinguish between the shades of blue. Changing the colors would help viewers more easily interpret the figure.

    ·      Line 212 mentions greatest latitudinal difference between sampling locations but seems to be greater longitudinal difference by sample map. Author can make a quick word change from latitudinal to "longitudinal".

    Competing interests

    The authors declare that they have no competing interests.

  2. Version published to 10.1101/2024.01.04.574243v2 on bioRxiv
  3. Version published to 10.1101/2024.01.04.574243v1 on bioRxiv