Ancient and modern colonization of North America by hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia

Hemlock woolly adelgid, Adelges tsugae, is an invasive pest of hemlock
trees (Tsuga) in eastern North America. We used 14 microsatellites and
mitochondrial COI sequences to assess its worldwide genetic structure and
reconstruct its colonization history. The resulting information about its
life cycle, biogeography and host specialization could help predict
invasion by insect herbivores. We identified eight endemic lineages of
hemlock adelgids in central China, western China, Ulleung Island (South
Korea), western North America, and two each in Taiwan and Japan, with the
Japanese lineages specializing on different Tsuga species. Adelgid life
cycles varied at local and continental scales with different sexual,
obligately asexual and facultatively asexual lineages. Adelgids in western
North America exhibited very high microsatellite heterozygosity, which
suggests ancient asexuality. The earliest lineages diverged in Asia during
Pleistocene glacial periods, as estimated using approximate Bayesian
computation. Colonization of western North America was estimated to have
occurred prior to the last glacial period by adelgids directly ancestral
to those in southern Japan, perhaps carried by birds. The modern invasion
from southern Japan to eastern North America caused an extreme genetic
bottleneck with just two closely related clones detected throughout the
introduced range. Both colonization events to North America involved host
shifts to unrelated hemlock species. These results suggest that genetic
diversity, host specialization and host phylogeny are not predictive of
adelgid invasion. Monitoring non-native sentinel host trees and focusing
on invasion pathways might be more effective methods of preventing
invasion than making predictions using species traits or evolutionary
history.