Evolution of drosophila on the newer hawaiian volcanoes

Summary

The 20-year Odyssey taken by the Hawaiian Drosophila project has recently become focussed on a selected microcosm: this consists of the Island of Hawaii (“the Big Island”) and one of its endemic species, Drosophila silvestris. Both the island and the species are considerably less than one million years old. Along with a morphologically distinct, but partially sympatric, close relative, D. heteroneura, silvestris inhabits moderate-altitude rainforests. They are the only members of the planitibia subgroup that occur on this island. The distribution of these species is discontinuous due to the dissection of the forests by recent lava flows and to the irregular distribution of their main host plants. Although allozyme heterozygosity within both species is considerable, local populations of both species show high similarity coefficients. The two species are, furthermore, virtually indistinguishable electrophoretically; nevertheless, significant differences in single-copy DNA have been demonstrated. Within silvestris, five inversion polymorphisms are widespread; six others have more restricted distributions. Populations in some of the geologically newer areas are the most polymorphic, both chromosomally and morphologically. Altitudinal clines of gene arrangement frequency are clear in areas on both sides of the island. The same inversions are involved in these clines on the two sides of the island. Males of silvestris from populations from the north and east side of the island (“Hilo-side”) display a novel morphological secondary sexual character. This is absent not only from south and west (“Kona-side”) silvestris but also from heteroneura and from the three closely related species endemic to older adjacent islands. In view of the phylogenetic novelty of this evolutionary development, Hilo-side silvestris is judged to be derived from Kona-side rather than vice versa. The character in question involves the addition of about 25 large cilia to the dorsal surface of the tibia of the male. This portion of the leg is used in a very specific fashion to stimulate the female’s abdomen during the courtship ritual. Studies of sexual behaviour of individuals drawn from various natural and laboratory populations of silvestris and its relatives have been carried out. Hybrid sterility and/or inviability is lacking in crosses both within and between populations of heteroneura and silvestris. An interesting regularity has been widely observed: there is a positive correlation between the phylogenetic age of a population and the degree of discrimination by the female sex in mating. When this principle is applied to silvestris populations, the Kona-side populations of Hualalai volcano are judged to be the oldest in the species. As expected, Hilo-side populations with the novel bristle character appear to be newly-derived. The behavioural data further suggest that the novel bristle character arose in Kohala mountain populations from Hualalai ancestors and spread south and east from there toward the currently active volcanic areas where further behavioural, morphological and chromosomal changes are continuing. Preliminary evidence indicates that the behavioural attributes, as well as the bristle character, have a polygenic basis, held in balance by stabilizing sexual selection. This secondary sexual differentiation appears to serve as a model, at the microevolutionary level, of the kind of genetic change which has characterized the evolution of much of the Hawaiian Drosophilidae. Specifically, new behavioural patterns appear to have become established through novel but delicate genetic coadaptation of male and female behaviour. The process appears to be driven by sexual selection, with shifts of balance being abetted by the founder effect. Adaptations to the ambient environment are pronounced as these flies evolve, yet they appear to follow speciation rather than initiate it.