The last days of Aporia crataegi (L.) in Britain: evaluating genomic erosion in an extirpated butterfly
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Abstract
Current rates of habitat degradation and climate change are causing unprecedented declines in global biodiversity. Studies on vertebrates highlight how conservation genomics can be an effective tool to identify and manage threatened populations, but it is unclear how vertebrate derived metrics of genomic erosion translate to invertebrate species, with their markedly different population sizes and life histories. The Black-veined White butterfly ( Aporia crataegi) was extirpated from Britain in the 1920s. Here, we sequenced historical DNA from 17 museum specimens collected between 1854-1924 to reconstruct demography and determine levels of genomic erosion in the species as it approached extirpation. We compare these results to those from the Common Blue butterfly ( Polyommatus icarus ); a species with relatively stable demographic trends in Great Britain. We provide evidence for bottlenecks in both these species around the period of post-glacial colonisation of the British Isles. Our results reveal different demographic histories and N e for both species, consistent with their fates in Britain, likely driven by differences in life history, ecology, genome lengths and body size. Despite a difference, by an order of magnitude, in historical effective population sizes ( N e ), reduction in genetic diversity in A. crataegi was comparable to that in P. icarus . Symptomatic of A. crataegi ’s disappearance were marked increases in runs-of-homozygosity (RoH), consistent with recent inbreeding, and accumulation of putatively mildly and weakly deleterious variants. Our results support the idea that metrics of inbreeding and accumulation of deleterious mutations could be more informative markers of population or species in decline.
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This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/10779381.
The study used conservation genomics methods to investigate genetic erosion in a butterfly extirpated from Britain in the 1920s (Aporia crataegi). The authors extracted DNA from A. crataegi museum specimens and compared it to DNA from a stable butterfly species, Polyommatus icarus. They also compared A. crataegi from the British Isles to specimens from the European mainland. The authors examine and report metrics of genomic erosion including historical effective population sizes, genetic diversity, and runs-of-homozygosity in each species. Their results reveal differences in demographic histories and effective population sizes but similar reductions in genetic diversity for both species. …
This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/10779381.
The study used conservation genomics methods to investigate genetic erosion in a butterfly extirpated from Britain in the 1920s (Aporia crataegi). The authors extracted DNA from A. crataegi museum specimens and compared it to DNA from a stable butterfly species, Polyommatus icarus. They also compared A. crataegi from the British Isles to specimens from the European mainland. The authors examine and report metrics of genomic erosion including historical effective population sizes, genetic diversity, and runs-of-homozygosity in each species. Their results reveal differences in demographic histories and effective population sizes but similar reductions in genetic diversity for both species. Overall, the authors conclude that A. crataegi likely suffered a severe bottleneck during the colonization of the British Isles, with low effective population size, recent inbreeding, and accumulation of weak or mild deleterious mutations.
The manuscript is well-written and details an important study on the conservation genomics of both extirpated and stable butterfly species. The authors effectively articulate the significance of their research, contextualizing it within the realm of butterfly conservation. They also address the study's limitations and explore potential applications for other species. The reviewer found the article to be interesting and novel as well as accessible to a range of audiences. I would recommend this article for publication pending the major and minor revisions detailed below.
Major Edits
· Abstract: The reviewer suggests adding a sentence to describe the comparison between the British Isles and continental A. crataegi populations (it is described within the text but not mentioned in the abstract).
· In the Abstract, Introduction, and Methods, it would be very helpful to clarify the time period being referenced. It is important to note that the A. crataegi data are compared to contemporary P. icarus populations (if that is the case). Collection dates for P. icarus are not specified in the methods. The reviewer would also find it helpful to include a description of why you chose to use contemporary P. icarus specimens rather than those from the same time period as A. crataegi.
· Upon reading initially, it was unclear to the reviewer whether P. icarus specimens were sourced from museums or collected in the field by the authors. The methods section, 'Sampling Modern specimens of P. icarus' would benefit from the inclusion of additional details such as the dates in which the specimens were collected and how far apart the collection locations were for the British Isles and France samples.
· In the last paragraph of the Introduction, it is mentioned that the study specifically addressed whether the British A. crataegi were distinct from continental Europe based on genetic structuring and demographic history prior to 10 Kya. The reviewer suggests including additional information about how genetic structuring and demographic history data were generated for that time period. Providing additional details in both the Introduction and Methods sections to describe this process would enhance clarity and understanding.
· Methods, paragraph 1: This paragraph would benefit from additional information, including the number of specimens collected from each of the three locations listed and whether each specimen came from different 'sites' (latitude/longitude) or if there was overlap in the sites in which specimens were collected. How close or how far apart were the sites? Were the collection dates similar among locations sampled (mainland vs Isles)?
· Methods – "Historical Demography Reconstruction", paragraph 2: The authors should consider adding additional context to explain the validity of using mutation rate estimates from Heliconius melpomene.
· Methods – "Genetic Diversity": The reviewer recommends adding additional information about why LD pruning was not performed.
· Methods – "Statistical Analysis": The reviewer recommends revising this section to include important missing details. Providing a clear description of how the linear models were constructed, including identification of response and predictor variables, would enhance clarity. It would also be beneficial to specify whether multiple linear models were constructed or just one.
· Results: Several descriptions of statistical tests and their corresponding results are missing statistics. For instance, in the second paragraph, the authors mention a significant positive correlation between mean fragment length and the age of the sample; however, the specific statistical values are not provided.
· Results, paragraph 5: The authors mention a sample with unknown origins (K05L). It would be beneficial to also include this information in the Methods section, providing more detailed descriptions of the locations and specimens with unknown origins.
Minor Edits
· The reviewer suggests that future preprints include line numbers to streamline the review process.
· In the last sentence of the abstract, it would be beneficial to clarify what specific metrics of inbreeding and accumulation of deleterious mutations are being compared to for their informativeness regarding population or species decline.
· Introduction, paragraph 3: Adding a definition of genomic erosion might be helpful to set the context for the rest of the paper.
· Intro, paragraph 3: Which of the metrics described rely on genome-wide, putatively neutral genetic markers? The reviewer recommends adding an example in parentheses here.
· Additionally, the reviewer finds it unclear what comparison is being made in the statement: "For comparison, we only used museum samples of continental populations to avoid any potential bias stemming from comparing degraded historical DNA with modern DNA." Is this referring to a comparison between mainland and island populations? If so, explicitly framing it as such could improve clarity for the reader.
· In the first sentence of the Discussion, it may not be necessary to mention that the extractions were contaminant-free. The paragraph could be enhanced by providing additional details on the specific types of groups to which this approach could be applied (e.g., is it applicable to only certain orders/types of insects with similar sex determination mechanisms?).
· Discussion, paragraph 5: The authors should consider expanding on the influence that captive bred specimens may have on their results - what are some implications of this?
Competing interests
The author declares that they have no competing interests.
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