Ke. Filchak et al., A field test for host-plant dependent selection on larvae of the apple maggot fly, Rhagoletis pomonella, EVOLUTION, 53(1), 1999, pp. 187-200
Host-plant dependent fitness trade-offs refer to traits that enhance the pe
rformance of an insect on one plant species to its detriment on others. Suc
h trade-offs are central to models of sympatric speciation via host shifts,
but have proven difficult to empirically demonstrate.
Here, we test for host-plant dependent selection on larvae of apple (Malus
pumila L.) and hawthorn (Crataegus mollis L. spp.)-infesting races of Rhago
letis pomonella (Walsh). Samples of larvae were reared in the field and und
er protective conditions in a garage. Our rationale was that the garage sho
uld slow rates of fruit rot relative to the field, relaxing selection press
ures associated with declining fruit quality. Four findings emerged from th
e study. (1) Larvae suffered higher mortality in fruits in the field than t
he garage. (2) The increase in mortality was greater for larvae in haws. (3
) Larvae possessing the alleles Me 100, Acon-2 95, and Mpi 37, three allozy
mes displaying host-related differentiation in R. pomonella that map to lin
kage group II in the fly, left fruits earlier than other genotypes. (4) All
ele frequencies for Me 100, Acon-2 95, and Mpi 37 were significantly higher
in both apple and haw larvae surviving the field versus the garage treatme
nt.
Our results suggested that field conditions favored larvae that rapidly dev
eloped and left rotting fruits. Since these individuals tended to possess t
he alleles Me 100, Acon-2 95, and Mpi 37, frequencies of these allozymes we
re higher in the field. Selection on larvae was directional for Me 100, Aco
n-2 95, and Mpi 37 (or linked genes) in both host races. We previously show
ed that these same alleles can be disfavored in the pupal stage, especially
in the apple race, where they correlate with premature diapause terminatio
n. Fitness trade-offs in Rhagoletis may therefore be due as much to differe
nces in the relative strengths of directional selection pressures acting on
different life stages as to disruptive selection affecting any one particu
lar stage. The necessity to consider details of the entire life-cycle highl
ights one of the many challenges posed to documenting fitness trade-offs fo
r phytophagous insects.