Lepidoptera genomics based on 88 chromosomal reference sequences informs population genetic parameters for conservation

Abstract

Butterflies and moths (Lepidoptera) are one of the most ecologically diverse and speciose insect orders, with more than 157,000 described species. However, the abundance and diversity of Lepidoptera are declining worldwide at an alarming rate. As few Lepidoptera are explicitly recognised as at risk globally, the need for conservation is neither mandated nor well-evidenced. Large-scale biodiversity genomics projects that take advantage of the latest developments in long-read sequencing technologies offer a valuable source of information. We here present a comprehensive, reference-free, whole-genome, multiple sequence alignment of 88 species of Lepidoptera. We show that the accuracy and quality of the alignment is influenced by the contiguity of the reference genomes analysed. We explored genomic signatures that might indicate conservation concern in these species. In our dataset, which is largely from Britain, many species, in particular moths, display low heterozygosity and a high level of inbreeding, reflected in medium (0.1 - 1 Mb) and long (> 1 Mb) runs of homozygosity. Many species with low inbreeding display a higher masked load, estimated from the sum of rejected substitution scores at heterozygous sites. Our study shows that the analysis of a single diploid genome in a comparative phylogenetic context can provide relevant genetic information to prioritise species for future conservation investigation, particularly for those with an unknown conservation status.

The last days ofAporia crataegi(L.) in Britain: evaluating genomic erosion in an extirpated butterfly

“…2) and the exact timing of the colonisation of the British Isles by these species may also result from bias in the PSMC method. Simulations by Bortoluzzi et al . (2023) suggest, that PSMC reconstructions for species with small genomes and a high ratio of recombination to mutation rate, may reflect linked selection rather than true demographic history.…”

“…Isolated populations on islands, including the British Isles, offer an excellent system to study the genomics of populations with contrasting or unknown fates (e.g. Bortoluzzi et al ., 2023; Kyriazis et al ., 2023).…”

“…Recent advances in resequencing of museum samples (Korlević et al ., 2021, Mullin et al ., 2023), bioinformatic tools (e.g., Korneliussen et al ., 2014, Kutschera et al, 2022) and the availability of high-quality genomes with annotations (Rhie et al ., 2021; Formenti et al, 2022; DToL, 2022) are providing much needed resources for such work. Although challenges remain, for example, evaluating and interpreting fitness effects of deleterious mutations (de Valles-Ibáñez et al ., 2016; Robinson et al ., 2023), we expect museomics in combination with contemporary samples will expand our understanding of the genomics of extinction but also improve feasibility to monitor and manage threatened insect populations (Díez-del-Molino et al, 2018; Jensen et al ., 2022; Bortoluzzi et al ., 2023).…”

“…This approach should be applicable to other insect species using both museum and contemporary specimens. Comparative data on genomic erosion in threatened, stable and expanding species, but also those with different life histories could improve the predictive capacity for using metrics of genome erosion for identifying and managing threatened populations and species (Bortoluzzi et al ., 2023; Kyriazis et al ., 2023; Webster et al ., 2023).…”

Wisent genome assembly uncovers extended runs of homozygosity and a large deletion that inactivates the thyroid hormone responsive gene

“…We constructed a phylogenetic tree from complete single copy orthologs identified by compleasm v0.2 (Bortoluzzi et al, 2023). We ran compleasm using the mammalia_odb10 database on an additional set of eleven cetartiodactyla species ( Supplementary Table 3 ).…”