Whole-genomes from the extinct Xerces Blue butterfly can help identify declining insect species

  1. Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), 08003 Barcelona, Spain
  2. Institute of Genomics, University of Tartu, Riia 23B, 51010 Tartu, Estonia
  3. Section for Evolutionary Genomics, The Globe Institute, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen K, Denmark, Centre for Biodiversity Genomics, University of Copenhagen, DK-2100, Denmark
  4. Wellcome Sanger Institute, Hinxton, Saffron Walden CB10 1RQ, UK
  5. Departament of Genetics, Microbiology and Statistics-Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona 08028, Spain
  6. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Barcelona, Spain
  7. Museu de Ciències Naturals de Barcelona, 08019, Barcelona, Spain
  8. Catalan Institution of Research and Advanced Studies (ICREA), 08010 Barcelona, Spain
  9. Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA
  10. CNAG-CRG, Centre for Genomic Regulation, Barcelona Institute of Science and Technology (BIST), 08036 Barcelona, Spain

Peer review process

Not revised: This Reviewed Preprint includes the authors’ original preprint (without revision), an eLife assessment, public reviews, and a response from the authors (if available).

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Editors

  • Reviewing Editor
    George Perry
    Pennsylvania State University, University Park, United States of America
  • Senior Editor
    George Perry
    Pennsylvania State University, University Park, United States of America

Reviewer #1 (Public Review):

The authors report a study, where they have sequenced whole genomes of four individuals of an extinct species of butterfly from western North America (Glaucopsyche xerces), along with seven genomes of a closely related species (Glaucopsyche lygdamus), mainly from museum specimens, several to many decades old. They then compare these fragmented genomes to a high-quality, chromosome-level assembly of a genome of a European species in the same genus (Glaucopsyche alexis). They find that the extinct species shows clear signs of declining population sizes since the last glacial period and an increase in inbreeding, perhaps exacerbating the low viability of the populations and contributing to the extinction of the species.

The study really highlights how museum specimens can be used to understand the genetic variability of populations and species in the past, up to a century or more ago. This is an incredibly valuable tool, and can potentially help us to quickly identify whether current populations of rare and declining species are in danger due to inbreeding, or whether at least their genetic integrity is in good condition and other factors need to be prioritised in their conservation. In the case of extinct species, sequencing museum specimens is really our only window into the dynamics of genomic variability prior to extinction, and such information can help us understand how genetic variation is related to extinction.

I think the authors have achieved their goal admirably, they have used a careful approach to mapping their genomic reads to a related species with a high-quality genome assembly. They might miss out on some interesting genetic information in the unmapped reads, but by and large, they have captured the essential information on genetic variability within their mapped reads. Their conclusions on the lower genetic variability in the extinct species are sound, and they convincingly show that Glaucopyche xerces is a separate species to Glaucopsyche lygdamus (this has been debated in the past).

Reviewer #2 (Public Review):

The Xerces Blue is an iconic species, now extinct, that is a symbol for invertebrate conservation. Using genomic sequencing of century-old specimens of the Xerces Blue and its closest living relatives, the authors hypothesize about possible genetic indicators of the species' demise. Although the limited range and habitat destruction are the most likely culprits, it is possible that some natural reasons have been brewing to bring this species closer to extinction.

The importance of this study is in its generality and applicability to any other invertebrate species. The authors find that low effective population size, high inbreeding (for tens of thousands of years), and higher fraction of deleterious alleles characterize the Xerces colonies prior to extinction. These signatures can be captured from comparative genomic analysis of any target species to evaluate its population health.

It should be noted that it remains unclear if these genomic signatures are indeed predictive of extinction, or populations can bounce back given certain conditions and increase their genetic diversity somehow.

Methods are detailed and explained well, and the study could be replicated. I think this is a solid piece of work. Interested researchers can apply these methods to their chosen species and eventually, we will assemble datasets to study extinction process in many species to learn some general rules.

Several small questions/suggestions:

  1. The authors reference a study concluding that Shijimiaeoides is Glaucopsyche. Their tree shows the same, confirming previous publications. And yet they still use Shijimiaeoides, which is confusing. Why not use Glaucopsyche for all these blues?

  2. Plebejus argus is a species much more distant from P. melissa than Plebejus anna (anna and melissa are really very close to each other), and yet their tree shows the opposite. What is the problem? Misidentification? Errors in phylogenetic analyses?

  3. Wouldn't it be nicer to show the underside of butterfly pictures that reveals the differences between xerces and others? Now, they all look blue and like one species, no real difference.

  4. The authors stated that one of five xerces specimens failed to sequence, and yet they show 5 specimens in the tree. Was the extra specimen taken from GenBank?

  1. Howard Hughes Medical Institute
  2. Wellcome Trust
  3. Max-Planck-Gesellschaft
  4. Knut and Alice Wallenberg Foundation