The chromosome-scale genome of the pine bark adelgid reveals conserved macrosynteny across Adelgidae

Abstract

Chromosome evolution varies widely across Aphidomorpha: several aphid lineages exhibit extensive interautosomal reshuffling, whereas comparisons involving grape phylloxera and Adelges suggest greater chromosome conservation outside Aphididae. However, all published adelgid genomes represent the genus Adelges, leaving conservation across deeper adelgid divergences unresolved. Here, we report a chromosome-scale genome for the pine bark adelgid, Pineus strobi, providing the first genome for the genus Pineus and extending genomic sampling to an early-diverging adelgid lineage. Synteny analyses revealed broad conservation of major linkage groups between Pineus and Adelges across approximately 90 million years. The five grape phylloxera chromosomes also showed broad correspondence to the ten adelgid chromosomes, consistent with a limited number of chromosomal fusions or fissions and relatively little exchange among major linkage groups. These findings strengthen evidence that such extensive interautosomal reshuffling is not characteristic of Aphidomorpha as a whole. We also recovered a complete 25.3 kb mitochondrial genome with expanded, repeat-rich noncoding regions and complete circular genomes for the obligate nutritional symbionts "Candidatus Annandia pinicola" and "Candidatus Hartigia pinicola." Comparisons with Pineus similis symbionts revealed conserved coding capacity and genome-wide synteny, supporting conservation of this dual nutritional symbiosis in pine-associated adelgids. Finally, we recovered the first complete Wolbachia genome reported from an adelgid. Because Wolbachia can induce parthenogenesis, its presence in P. strobi raises the possibility that it contributes to the maintenance or reinforcement of parthenogenesis in a species lacking a viable sexual generation. Together, these genomes provide an integrated resource for aphidomorph evolution and symbiosis. Significance statementSeveral aphid lineages exhibit extensive reshuffling among autosomes, whereas previous comparisons with grape phylloxera and Adelges cooleyi suggested greater chromosome conservation outside Aphididae; however, all published adelgid genomes have represented Adelges, leaving the long-term stability of chromosome organization across Adelgidae unresolved. The first chromosome-scale genome from Pineus reveals broad conservation of major linkage groups across approximately 90 million years of adelgid evolution and clear correspondence with the five chromosomes of the grape phylloxera, supporting chromosome conservation outside Aphididae. The accompanying mitochondrial and symbiont genomes provide an integrated resource for studying aphidomorph genome evolution and symbiosis.