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

Abstract

The Xerces Blue (Glaucopsyche xerces) is considered to be the first butterfly to become extinct at global scale in historical times. It was notable for its chalky lavender wings with conspicuous white spots on the ventral wings. The last individuals were collected in their restricted habitat, in the dunes near the Presidio military base in San Francisco, in 1941. To explore the demographic history of this iconic butterfly and to better understand why it went extinct, we sequenced at medium coverage the genomes of four 80 to 100-year-old Xerces Blue specimens and seven historic specimens of its closest relative, the Silvery Blue (G. lygdamus). We compared these to a novel annotated genome of the Green-Underside Blue (G. alexis). Phylogenetic relationships inferred from complete mitochondrial genomes indicate that Xerces Blue was a distinct species that diverged from the Silvery Blue lineage at least 850,000 years ago. Using nuclear genomes, we show that both species experienced population growth during the MIS 7 interglacial period, but the Xerces Blue decreased to a very low effective population size subsequently, a trend opposite to that observed in the Silvery Blue. Runs of homozygosity in the Xerces Blue were significantly greater than in the Silvery Blue, suggesting a higher incidence of inbreeding. In addition, the Xerces Blue carried a higher proportion of derived, putatively deleterious amino acid-changing alleles than the Silvery Blue. These results demonstrate that the Xerces Blue experienced more than 100 thousand years of population decline, prior to its human-induced final extinction.

Another ghost of Gondwana—Progradungula barringtonensis Michalik & Smith, sp. nov., a new species of the relict spider genus Progradungula (Araneae: Gradungulidae) from a temperate rainforest in eastern Australia

“…This may also apply to rainforest communities, which are not considered to be resilient to fire (Bowman 2000; Lee, Cornwell, & Kingsford 2022), and can be assumed for Progradungula spiders. Finally, significant habitat loss could be the ultimate threat driving a local endemic such as P. barringtonensis to extinction as was recently demonstrated for the extinct Xerces blue butterfly (de‐Dios et al 2023).…”

Incorporating genomics into insect conservation: Butterflies as a model group

“…Demographic inference using genome-wide data corroborated that G. xerces has likely had a small range as a result of a gradual population contraction and putatively deleterious alleles were already present prior to its human-driven extinction (de-Dios et al, 2021).…”

“…Such a species had a small historical range near San Francisco, USA, and succumbed due to urban development in the 1940s. Demographic inference using genome‐wide data corroborated that G. xerces has likely had a small range as a result of a gradual population contraction and putatively deleterious alleles were already present prior to its human‐driven extinction (de‐Dios et al, 2021). Therefore, by re‐assessing its taxonomic status, it became clear that G. xerces reintroduction is not possible anymore.…”

Population genetics for insect conservation and control

“…Using these methods, it is possible to determine whether populations have suffered the deleterious effects of population declines and to assess the need for and feasibility of specific measures to restore their level of diversity, for example, using genetic rescue (Frankham, 2015). These methods have also been used to investigate the genomic signals of population decline leading to the extinction of the Xerces Blue butterfly, Glaucopsyche xerces (De‐Dios et al, 2023). Screening for such signals might be very useful to detect and prevent future extinctions.…”