title: Ancient and modern colonization of North America by hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia.
abstract: 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.
authors.affiliation: Northern Research Station, USDA Forest Service, Hamden, Connecticut 06514, USA.
authors.forename: Nathan P
authors.initials: NP
authors.lastname: Havill
authors.affiliation: Osaka Museum of Natural History, Osaka 546-0034, Japan.
authors.forename: Shigehiko
authors.initials: S
authors.lastname: Shiyake
authors.affiliation: Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA.
authors.forename: Ashley
authors.initials: A
authors.lastname: Lamb Galloway
authors.affiliation: Canadian National Collection of Insects, Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada.
authors.forename: Robert G
authors.initials: RG
authors.lastname: Foottit
authors.affiliation: Institute of Plant & Environmental Protection, Beijing Academy of Agricultural & Forestry Science, Beijing 100097, China.
authors.forename: Guoyue
authors.initials: G
authors.lastname: Yu
authors.affiliation: Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003, USA.
authors.forename: Annie
authors.initials: A
authors.lastname: Paradis
authors.affiliation: Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003, USA.
authors.forename: Joseph
authors.initials: J
authors.lastname: Elkinton
authors.affiliation: Northern Research Station, USDA Forest Service, Hamden, Connecticut 06514, USA.
authors.forename: Michael E
authors.initials: ME
authors.lastname: Montgomery
authors.affiliation: Systematic Entomology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Hokkaido, Japan.
authors.forename: Masakazu
authors.initials: M
authors.lastname: Sano
authors.affiliation: Department of Ecology & Evolutionary Biology, Yale University, New Haven, Connecticut 06520, USA.
authors.forename: Adalgisa
authors.initials: A
authors.lastname: Caccone
mesh_terms: D000818:Animals; D001499:Bayes Theorem; D004272:DNA, Mitochondrial / Q000235:genetics; D005202:Asia, Eastern; D005828:Genetics, Population; D005838:Genotype; D006430:Hemiptera / Q000235:genetics*; D018652:Hemlock; D060434:Herbivory; D058865:Introduced Species; D018895:Microsatellite Repeats; D009656:North America; D017422:Sequence Analysis, DNA
chemical_list: D004272:DNA, Mitochondrial
keywords: complex life cycle; cyclical parthenogenesis; host range; invasive species