Genetic complexity of host-selection behavior in Drosophila

Abstract

Genetic variation for settling responses to different types offood and for oviposition behavior exists within natural populations of Drosophila tripunctata. After flies from two isofemale strains and F2 derived from crosses between them were released in the wild and recaptured at either mushroom or tomato baits, the oviposition preferences of females for these foods were determined in the laboratory. Whereas settling behavior and oviposition-site preference were negatively correlated in the parental strains, there was no association of these behaviors in the F2 generation. Furthermore, lines produced by crossing these two strains followed by inbreeding did not manifest such a negative correlation. Together, these results indicate that two important aspects of host selection are under independent genetic control. These findings caution against using a single component of the process of host selection as indicative of the probability that a particular resource will be utilized in the field, and they bear on the question of how speciation based on genetic variation for host selection may be accomplished.Speciation is of central importance in the evolution of biological diversity, and it has, therefore, been a major focus of attention since the time of Darwin (1). However, no consensus of opinion on how new species arise has emerged; thus, recent reviews concerned with the relation between population structure and speciation have promoted radically different hypotheses (2-5). One reason for the wavering direction of speciation theory is the virtual absence of information on the nature ofintraspecific genetic variation for the types of structures, behaviors, and physiologies that would seem to be important in the development of reproductive isolation. A notable and promising exception is the work of Carson and his associates on the mode of inheritance of tibial bristles that characterize males of some populations of Drosophila silvestris and that are thought to be used during courtship (6-8).In many groups of insects, speciation is commonly accompanied by, and may, in fact, be a consequence of, shifts to new larval feeding resources (hosts) (9-13). The traits that bring about such host shifts are believed to be those governing host selection by adults, larval development on alternative resources, and mate preference (13,14). If the host also serves as a rendezvous for mating, as it does for many species (13), then the probability of mating with an individual of a particular genotype will be a pleiotropic consequence of host selection. Furthermore, recent evidence suggests that evolutionary shifts to new hosts may be due more to behavioral than to physiological changes (11). Thus, evolutionary changes in host selection may play a major role in speciation in insects (15). However, essentially nothing is known of the genetics of this process in any insects.All theoretical models of host-related speciation are based on the assumption that, within species of insects, potential hosts are ranked by an individual alo...

Genetics of oviposition-site preference in Drosophila tripunctata

“…Experiment 2 (1983). This experiment on strains S64, S74, and F2 derived from crosses between them investigated the genetic correlation between oviposition behaviour in the laboratory and settling behaviour in the field, and has been reported elsewhere (Jaenike, 1986). Data from it are relevant here to the question of dominance and the existence of modifier loci.…”

“…Maternal effects Strains S64 and S74, which consistently differ in oviposition-site preference (Jaenike, 1985(Jaenike, , 1986, and below), were crossed reciprocally in Experiment 1 to determine if there were cytoplasmic or maternal effects on egg laying behaviour. In these tests, the F1 females derived from the cross S64 x S74 differed somewhat in oviposition behaviour from females produced by the reciprocal cross Experiment 1 involved crosses between S64 and S74 to obtain F1, F2, and various types of backcrossed flies.…”

Laboratory evolution of host plant utilization in the bean weevil (Acanthoscelides obtectus)

“…Due to its special evolutionary importance, several studies have separated genetic and environmental variance in host preference (Tabashnik et al, 1981;Rausher, 1983;Jaenike, 1985Jaenike, , 1986Jaenike, , 1989Lofdahl, 1987;Singer et al, 1988;Fox, 1993) or performance (Rausher, 1984;Via, 1984;Hare and Kennedy, 1986;Futuyma and Philippi, 1987;James et al, 1988). Some of these short-term experiments have demonstrated a genetic correlation between preference and performance (Tavormina, 1982;Via, 1986;Singer et al, 1988;Jaenike, 1989).…”

Genotype-specific habitat selection for oviposition sites in the cactophilic species Drosophila buzzatii

“…There is a spatial hierarchy in habitat choice, where flies may move to habitats or host plants that are generally suitable and then choose microhabitats for oviposition. This distinction has been emphasized by Jaenike (1986) in defining settling behaviour as movement to and settling on a potential host, followed by oviposition site preference. Genetic variation for both these behaviours was found for D. tripunctata by Jaenike (1986) but his results indicated them to be independent genetically.…”