Selective maintenance of allozyme differences among sympatric host races of the apple maggot fly

Abstract

Whether phytophagous insects can speciate in sympatry when they shift and adapt to new host plants is a controversial question. One essential requirement for sympatric speciation is that disruptive selection outweighs gene f low between insect populations using different host plants. Empirical support for host-related selection (i.e., fitness trade-offs) is scant, however. Here, we test for host-dependent selection acting on apple (Malus pumila)-and hawthorn (Crataegus spp.)-infesting races of Rhagoletis pomonella (Diptera: Tephritidae). In particular, we examine whether the earlier fruiting phenology of apple trees favors pupae in deeper states of diapause (or with slower metabolisms͞ development rates) in the apple f ly race. By experimentally lengthening the time period preceding winter, we exposed hawthorn race pupae to environmental conditions typically faced by apple f lies. This exposure induced a significant genetic response at six allozyme loci in surviving hawthorn f ly adults toward allele frequencies found in the apple race. The sensitivity of hawthorn f ly pupae to extended periods of warm weather therefore selects against hawthorn f lies that infest apples and helps to maintain the genetic integrity of the apple race by counteracting gene f low from sympatric hawthorn populations. Our findings confirm that postzygotic reproductive isolation can evolve as a pleiotropic consequence of host-associated adaptation, a central tenet of nonallopatric speciation. They also suggest that one reason for the paucity of reported fitness trade-offs is a failure to consider adequately costs associated with coordinating an insect's life cycle with the phenology of its host plant.Host plant-associated fitness trade-offs are critical for sympatric speciation in phytophagous insects (1). Fitness trade-offs refer to trait(s) or gene(s) that confer a selective advantage to an insect on one plant while incurring a cost on alternative plants. Such trade-offs are important because they can act as postzygotic barriers to gene flow between insect populations specialized on different host plants (1).There is currently little empirical evidence for host plantrelated fitness trade-offs in phytophagous insects (ref. 2, although see refs. 3-5 for some exceptions), which has raised questions concerning the likelihood of sympatric speciation (6). But many tests for fitness trade-offs have concentrated on larval feeding performance and the metabolic detoxification of plant secondary compounds while neglecting potential costs associated with coordinating an insect's life cycle with host plant phenology (7). Here, we test for fitness trade-offs in apple (Malus pumila)-and hawthorn (Crataegus spp.)-infesting populations of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae) by examining whether and how differences in the fruiting phenologies (seasonalities) of apple and hawthorn trees affect the genetics of these flies.Previous studies have confirmed the status of apple and hawthorn populations of R. pomonella as g...

THE EFFECTS OF WINTER LENGTH ON THE GENETICS OF APPLE AND HAWTHORN RACES OF RHAGOLETIS POMONELLA (DIPTERA: TEPHRITIDAE)

“…A reanalysis of the prewinter experiment revealed this to be true. Extending the prewintering period resulted in significant linear declines in the frequencies of Aat-2 +75 and Dia-Z 100 in surviving hawthorn-fly males (r 2 Aat-2 +75 = 0.45, P = 0.049, 8 df; r 2 Dia-2 100 = 0.45, P = 0.049, 8 df; note: we included new data for 35-, 42-, and 65-day prewinter treatments in this analysis that were not published in Feder et al 1997). But allele frequencies did not significantly decline in females (r 2 Aat-2 +75 = 0.003, P = 0.896, 8 df; r 2 Dia-2 100 = 0.03, P = 0.660, 8 df).…”

Host-plant-associated genetic differentiation in Northern French populations of the European corn borer

“…In this latter species, there is selective maintenance of sympatric host-plant races differing at six allozyme loci mapping to three different regions of the genome (Feder et al, 1997;Filchak et al, 2000).…”

Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis

“…In particular, the 3-to 4-week earlier phenology of apple selects for a deeper pupal diapause (greater recalcitrance to nondiapause development) in apple flies, allowing them to better withstand longer periods of warm weather before winter. A series of rearing experiments in which conditions were manipulated to simulate the seasonal difference between apple and haw fruiting times supported the ''diapause hypothesis'' by inducing genetic responses in allozyme frequencies in predicted directions (9)(10)(11)(12). Life-history adaptation to apple was therefore due, in part, to inversion frequency changes in apple flies that generated ecologically based pre-and postmating reproductive isolation from haw flies.…”

“…The inversions have been associated with the depth of the facultative overwintering pupal diapause (9)(10)(11)(12). Multiple regression of genotypes for the six allozymes demarcating the inversions explained from 15% to Ͼ40% of the variation in adult eclosion time (13).…”

“…Multiple regression of genotypes for the six allozymes demarcating the inversions explained from 15% to Ͼ40% of the variation in adult eclosion time (13). Diapause variation is important because it differentially adapts apple and haw flies to a seasonal difference in the fruiting times of their hosts (9)(10)(11)(12). In particular, the 3-to 4-week earlier phenology of apple selects for a deeper pupal diapause (greater recalcitrance to nondiapause development) in apple flies, allowing them to better withstand longer periods of warm weather before winter.…”