The deme-formation hypothesis states that selection can produce adapti
ve genetic variation within and among phytophagous insect populations.
We conducted three field experiments and tested this prediction by tr
ansferring eggs and measuring performance of a mobile leafmining insec
t, Stilbosis quadricustatella. In Experiment 1, we compared the rate o
f mine initiation of leafminers transferred to natal and novel sites.
In Experiment 2, we compared mine-initiation rate of leafminers transf
erred to natal and novel host-plant species. In Experiment 3, we compa
red the mine-initiation rate, mine-completion rate, and sources of mor
tality of miners transferred to neighboring natal and novel Quercus ge
minata trees. In the first, second, and third experiments, leafminer l
arvae initiated significantly more mines at the natal site, on the nat
al plant species, and on the natal e. geminata tree, evidence for adap
tive differentiation. Furthermore, plant-mediated mortality was signif
icantly lower among miners transferred to natal Q. geminata trees. Thi
s result supports a key assumption of the deme-formation hypothesis: i
nsects adapt to the defensive phenotypes of individual trees. However,
natural-enemy mortality was significantly higher among miners transfe
rred to natal trees, essentially reversing the plant effect. Therefore
, rates of successful mine completion were similar on natal (19%) and
novel (17%) trees. This experiment suggests that host plants and natur
al enemies may represent opposing forces of selection. Leafminers adap
ted to individual trees may realize a selective advantage only when na
tural-enemy densities are low.