Genetic Evidence for the Introduction of Rhagoletis pomonella (Diptera: Tephritidae) into the Northwestern United States.

The apple maggot fly, Rhagoletis pomonella Walsh (Diptera: Tephritidae), is a serious quarantine pest in the apple-growing regions of central Washington and Oregon. The fly is believed to have been introduced into the Pacific Northwest via the transport of larval-infested apples near Portland, Oregon, within the last 40 yr. However, R. pomonella also attacks native black hawthorn, Crataegus douglasii Lindley (Rosales: Rosaceae), and introduced ornamental hawthorn, Crataegus monogyna Jacquin, in the region. It is, therefore, possible that R. pomonella was not introduced but has always been present on black hawthorn. If true, then the fly may have independently shifted from hawthorn onto apple in the Pacific Northwest within the last 40 yr after apples were introduced. Here, we test the introduction hypothesis through a microsatellite genetic survey of 10 R. pomonella sites in Washington and 5 in the eastern United States, as well as a comparison to patterns of genetic variation between populations of Rhagoletis cingulata Loew and Rhagoletis indifferens Curran, two sister species of cherry-infesting flies known to be native to the eastern and western United States, respectively. We report results based on genetic distance networks, patterns of allelic variation, and estimated times of population divergence that are consistent with the introduction hypothesis for R. pomonella. The results have important implications for R. pomonella management, suggesting that black hawthorn-infesting flies near commercial apple-growing regions of central Washington may harbor sufficient variation to utilize apple as an alternate host, urging careful monitoring, and possible removal of hawthorn trees near orchards.

Hybridization and the spread of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae), in the northwestern United States.

Hybridization may be an important process interjecting variation into insect populations enabling host plant shifts and the origin of new economic pests. Here, we examine whether hybridization between the native snowberry-infesting fruit fly Rhagoletis zephyria (Snow) and the introduced quarantine pest R. pomonella (Walsh) is occurring and may aid the spread of the latter into more arid commercial apple-growing regions of central Washington state, USA. Results for 19 microsatellites implied hybridization occurring at a rate of 1.44% per generation between the species. However, there was no evidence for increased hybridization in central Washington. Allele frequencies for seven microsatellites in R. pomonella were more 'R. zephyria-like' in central Washington, suggesting that genes conferring resistance to desiccation may be adaptively introgressing from R. zephyria. However, in only one case was the putatively introgressing allele from R. zephyria not found in R. pomonella in the eastern USA. Thus, many of the alleles changing in frequency may have been prestanding in the introduced R. pomonella population. The dynamics of hybridization are therefore complex and nuanced for R. pomonella, with various causes and factors, including introgression for a portion, but not all of the genome, potentially contributing to the pest insect's spread.

Molecular species identification of cryptic apple and snowberry maggots (Diptera: Tephritidae) in western and central Washington.

In Washington state, identification of the quarantine apple pest Rhagoletis pomonella (Walsh) is complicated by the presence of the cryptic species Rhagoletis zephyria Snow (Diptera: Tephritidae). Distinguishing the two flies is important because there is a zero tolerance policy for R. pomonella in apple production for export. Here, we attempt to distinguish the two species by scoring R. pomonella and R. zephyria populations from western and south-central Washington for a set of 11 nuclear markers, including four single nucleotide polymorphisms (SNPs) developed for rapid and inexpensive genotyping using Taqman real-time quantitative-polymerase chain reaction. We show that the four SNPs may be adequate in most cases for distinguishing whether a fly originated from apple or black hawthorn (the two major host plants for R. pomonella representing an economic risk) versus snowberry (the major host for R. zephyria, and not a commercial threat). However, directional introgression of R. zephyria alleles into R. pomonella can complicate the identification of flies of mixed ancestry based only on the four SNPs. Moreover, this problem is more acute in the sensitive apple-growing regions of central Washington where our results imply hybridization is common. Consequently, application of the four SNP quantitative-polymerase chain reaction assay can immediately assist ongoing apple maggot monitoring, while the development of additional genetic markers through next-generation sequencing would be valuable for increasing confidence in species identification and for assessing the threat posed by hybridization as R. pomonella further spreads into the more arid apple-growing regions of central Washington.