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In Drosophila Busckii: Tests of the Hierarchy-Threshold Model Heredity 64 (1990) 371-375 The Genetical Society of Great Britain Received 11 October 1989 Host acceptance and life-history traits in Drosophila busckii: tests of the hierarchy-threshold model Steven P. Courtney and Department of Biology, University of Oregon, Jeffrey J. Hard Eugene, Oregon 97403, U.S.A. The hierarchy-threshold model for host-choice in insects predicts positive genetic correlations between use of different hosts, and between host use and the number of eggs carried by females. Life history theory predicts negative covariance between reproductive capacity and lifespan; hence host use and lifespan should be negatively correlated. These predictions were tested in half-sib breeding designs with the cosmopolitan Drosophila busckii. The predictions of the hietarchy-threshold model were met, supporting previous findings with other Drosophila. Predictions from life-history theory were not met for the population studied. INTRODUCTION expected to maintain genetic variability. Courtney et a!. argue that insects rank potential hosts in Anumber of studies have recently documented the order of decreasing acceptability; high ranking presence of genetic variance affecting host choice hosts are always acceptable, while low-ranking behaviour within natural populations of plant- hosts may become acceptable, dependent upon feeding insects (Tavormina, 1982; Jaenike and environmental conditions. An insect accepting a Grimaldi, 1983; Via, 1984; Lofdahl, 1987; Jaenike, low-ranking host must therefore also accept all 1987; Thompson, 1988a; Courtney and Chen, higher-ranked hosts. The model finds some 1988). In reviewing these and other data, Futuyma empirical support in studies by other workers, not- and Petersen (1985) have drawn attention to the ably Wiklund (1981, 1982), Singer (1982, 1986), scarcity of information regarding the factors that Lofdahl (1987) and Thompson (1988a). Factors maintain such variation within populations. In par. influencing the rate at which hosts become accep- ticular, Futuyma and Petersen point out the need ted include current eggload borne by females (Fitt, for studies of genetic covariance of other charac- 1986) and adult experience (Jaenike, 1982, 1983). ters, and of the nature of genetic correlations Specific predictions made by Courtney et a!. (1989) between characters. Genetic correlations due to include: (1) Significant levels of additive genetic pleiotropy may impose constraints on the evol- variance for use of low-ranking hosts will be ution of host choice behaviour. Similarly, corre- maintained in populations, since such variance is lated responses to natural selection may explain rarely subject to direct selection (this holds true both observed patterns of host use, and the main- even if the host is never experienced in the popula- tenance of additive variance for host selection. tion in question, i.e., it is a novel host); (2) less Here we test a model which predicts pleiotropic variance is expected for use of higher-ranked hosts interactions between host use characters, using a (unless they are novel) due to direct selection on population of the cosmopolitan Drosophila busckii. such traits; (3) significant positive genetic correla- Courtney et a!. (1989) have proposed acompre- tions are expected between use of different low- hensive theory for the mechanistic control of host ranking, novel hosts; (4) there will be genetic choice behaviour. The "hierarchy-threshold" correlations between use of low-ranking hosts and model which they advance makes a number of factors influencing acceptance (high eggload predictions concerning genetic variance for host increases acceptance—therefore we expect a posi- use, and covariance with other characters. The tive genetic correlation between these traits); (5) model shows that pleiotropy between traits is no such correlations are expected for characters 372 S. P. COURTNEY AND J. J. HARD measured against use of high-ranking hosts. These tive prediction of life-history theory and the predictions have been met by several studies. hierarchy-threshold model is thus that we expect Lofdahl (1987) reports additive genetic variance negative covariance between lifespan and accept- for use of a novel cactus species by D. mojavensis; ance of low-ranking hosts, due to pleiotropic similar results obtain for D. suboccidentalis, a effects through reproductive allocation. mushroom feeder, when presented with two novel hosts, commercial mushrom (Agaricus campestris) and cucumber (Cucumis sativa) (Courtney and METHODS Chen, 1988; Chen, 1987). Courtney et a!. (1989) Wecarried out a standard half-sib breeding design report a significant positive genetic correlation using tenth generation descendants of D. busckii between use of low-ranked Cucumis and eggload caught at Eugene, Oregon on mushroom baits. in 6-day-old D. suboccidentalis, but no correlation Stocks were maintained at high population num- between use of higher-ranked Agaricus and bers (>1000) over Carolina instant Drosophila eggload. medium at 25°C, and under constant light. In all, D. suboccidentalis might be seen as an atypical 23 males were successfully mated to an average of species. It is an ecologically monophagous species 5•5 females, producing 126 full-sib families. (sensu Smiley, 1978), which uses only fungi of Families were raised on instant medium as before. genus Ramaria in the study population of the Half-sib families were distributed randomly among Cascade mountains in western Oregon (Courtney vials and with respect to position to the rearing el a!., 1989). Here, other fungi are rare and chamber and time of onset. This procedure ensures unpredictable, and Ramaria is the only relatively that common environment (larval rearing media) abundant resource. Monophagous populations effects did not influence the estimates of heritabiliy are, by definition, subject to little direct selection or genetic correlations, derived from half-sib on host choice. Results for D. suboccidentalis might designs (Falconer, 1981). Flies were sexed at emer- therefore reflect the special circumstances of a gence, and the sexes separated. Females were then monophagous species. The present study was car- divided among four treatments. One group was ried out to determine whether similar results may dissected at age 6 days, to determine the eggload be seen in polyphagous species, which live under carried. Eggload is measured as an index of repro- more variable selection regimes. The cosmopolitan ductive allocation, independent of mating history. D. busckii was chosen because of its extreme Eggload was measured in virgins, because mated breadth of diet in the wild (many rotting substrates, females would begin to lay eggs. This seems a including mushrooms, are used), and because it is reasonable way to study host choice, since females distantly related to D. suboccidentalis. D. busckii mate at the oviposition site, and must therefore is in subgenus Drosophila; D. subocciden tails is a sometimes approach hosts as virgins. A second member of the quinaria complex of subgenus Dor- group was maintained (virgin) over medium, and silopha. If the predictions of the hierarchy- the lifespan of each individual recorded. The threshold model are met for such ecologically and remaining flies were mated at day 6 and exposed taxonomically diverse species, the theory may be for 24 hours to approximately 1 g of fresh material robust. of one of two hosts: A. campestris or C. sativa. An additional interest was to incorporate into Oviposition substrates were then examined for the our experimental design consideration of another presence of eggs; if one egg or more was found, life-history character, adult lifespan. Considerable then the host was scored as accepted. The total attention has been given to theories of life-history number of eggs laid on each host was also recor- evolution which rely on antagonistic pleiotrophy ded. Only one host was offered to each fly; This between life-history components. For instance, procedure is necessary because exposure to a host Rose and Charlesworth (1981) show that, in some changes the behaviour of females on other hosts populations of D. meianogaster, early fecundity (Courtney and Gardner unpublished) and may and lifespan are negatively genetically correlated. alter both fecundity and survivorship. Some other studies support this result (e.g., Roach, Heritabilities of the numbers of eggs laid on 1986; Luckinbill et ai., 1987; Schemer et ai., 1989) either host, of female lifespan and of eggload were but others find equivocal (Hughes and Clark, 1988) estimated using standard methods employing or even opposite results (Giesel et aL, 1982). What- nested ANOVA (Falconer, 1981). Heritabilities of ever the generality of the results, antagonistic host acceptance were calculated using methods pleiotropy between fecundity and lifespan could applicable to threshold traits (Robertson and have important ramifications given that fecundity Lerner, 1949); standard errors for unbalanced itself is predicted to covary with host use. A deriva- designs are not calculable, and significance of these HOST ACCEPTANCE IN DROSOPHILA BUSCKII 373 threshold characters were estimated from x2analy- bers of eggs laid on the two hosts were not however sis. Genetic correlations were estimated from correlated, although each did weakly correlate with correlations across family means, following the eggload. We interpret these results as supporting suggestions of Via (1984) for situations where only thehierarchy-thresholdmodel. Acceptance one character
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