Whole-genomes from the extinct Xerces Blue butterfly reveal low diversity and long-term population decline

The Xerces Blue (Glaucopsyche xerces) (Boisduval 1852) is considered the first known butterfly to become globally extinct in historical times and was notable for its iridescent blue colour with white spots in the ventral wings. The last specimens were collected in their restricted habitat, in the dunes near the Presidio military base in San Francisco, in 1941 (Downey and Lange 1956). To explore the phylogenetic relationships and demographic history of this iconic butterfly, we have sequenced at medium coverage four 80 to 100-year-old Xerces Blue and seven historic Silvery Blue (G. lygdamus) specimens, its closest living relative. We have subsequently compared their genomes to a novel assembled and annotated genome of the Green-Underside Blue (G. alexis). The phylogenetic relationships assessed with complete mitochondrial (mtDNA) genomes indicate that Xerces Blue diverged from the Silvery Blue lineage at least 850,000 years ago. We used the nuclear genomes to explore their past demographic history and found that while both species experienced a population growth during the Eemian interglacial period, Xerces Blue decreased to a very low effective population size in post glacial periods, a trend opposite to that observed in the Silvery Blue. The patterns of runs of homozygosity in the Xerces Blue reveal signs of background inbreeding in this species to a much greater extent than the Silvery Blue, while global heterozygosity shows an opposite trend. In addition, Xerces Blue carried a higher proportion of derived, putatively deleterious amino acid-changing alleles than the Silvery Blue. We conclude that Xerces Blue experienced a long population decline process prior to its final extinction.