Rapid and repeatable shifts in life-history timing of Rhagoletis pomonella (Diptera: Tephritidae) following colonization of novel host plants in the Pacific Northwestern United States

Ecol Evol. 2015 Nov 26;5(24):5823-37. doi: 10.1002/ece3.1826. eCollection 2015 Dec.

Abstract

Host shifts of phytophagous insect specialists to novel plants can result in divergent ecological adaptation, generating reproductive isolation and potentially new species. Rhagoletis pomonella fruit flies in eastern North America underwent a host shift ~160 ya from native downy hawthorn (Crataegus mollis) to introduced, domesticated apple (Malus domestica). Divergent selection on diapause phenology related to the earlier fruiting time of apples versus downy hawthorns resulted in partial allochronic reproductive isolation between the fly races. Here, we test for how rapid and repeatable shifts in life-history timing are driving ecological divergence of R. pomonella in the Pacific Northwestern USA. The fly was introduced into the region via larval-infested apples 40-65 ya and now attacks native black hawthorn (Crataegus douglasii) and introduced ornamental hawthorn (Crataegus monogyna), in addition to early- and late-maturing apple varieties in the region. To investigate the life-history timing hypothesis, we used a field-based experiment to characterize the host-associated eclosion and flight activity patterns of adults, and the feeding times of larvae at a field site in Vancouver, Washington. We also assessed the degree to which differences in host-fruiting time generate allochronic isolation among apple-, black hawthorn-, and ornamental hawthorn-associated fly populations. We conclude that host-associated fly populations are temporally offset 24.4% to 92.6% in their seasonal distributions. Our results imply that R. pomonella possesses the capacity for rapid and repeatable shifts in diapause life history to match host-fruiting phenology, which can generate ecologically based reproductive isolation, and potentially biodiversity in the process.

Keywords: Allochronic isolation; apple maggot fly; biodiversity; ecological speciation; hawthorn; host race formation; phytophagous insects.