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Views, See CARSON1978, Used but the Yeast Is Omitted Copyright 0 1987 by the Genetics Society of America High Fitness of Heterokaryotypic Individuals Segregating Naturally Within a Long-standing Laboratory Population of Drosophila silvestris Hampton L. Carson Department of Genetics, University of Hawaii, Honolulu, Hawaii 96822 Manuscript received September 8, 1986 Revised copy accepted March 23, 1987 ABSTRACT Natural populations of Drosophila szlvestris are polymorphic for inversions in one or more of four of the five major chromosome arms; laboratory stocks tend to retain this heterozygosity. A laboratory stock, U28T2, was started from a single naturally inseminated wild female caught at Kilauea Forest Reserve, Hawaii, in January 1977. Polytene analysis in 1980 showed the presence of three natural inversions in chromosome 4: k2 is distal, t is central and 1’ is proximal. The inversions are short but only short uncovered euchromatic sections exist at the distal and proximal ends. Periodic examinations through 1986 showed all three inversions to be persistent at moderately high frequencies. In 1984, a series of tests of mating performance of caged, mature males, taken at random as they eclosed from the stock, were followed by cytological testcrosses to females from a homokaryotypic stock. Only three of the eight possible haplotypes, k2/t/+ (A), +/+/12 (a)and +/+/+ (a’) were present. Tests of crossing over show none in males; in females, there is about 1% in each of the two regions between the inversions. Only one such apparent crossover haplotype was found among 1084 examined in samples from this stock. Thus, chromosome arrangements A, a and a’ virtually behave as whole- chromosome alleles in both sexes. Of 146 males marked and tested in cages, 61 produced progeny; the others failed to reproduce. Of 58 males and 80 females producing progeny and analyzed cytologically, there were, respectively, 49 and 59 heterokaryotypes. On the basis of frequencies calculated for fertilized eggs, 33.6 males and 46.3 females are expected. The facts suggest that individual males with the Aa karyotype are particularly successful in production of offspring. Adult females show an excess of Aa‘ as well as Aa. Such high fitness of heterokaryotypes in the effective breeding adults could be a major factor in the maintenance of stable chromosomal polymorphisms both in laboratory stocks and in nature. Although some of this heterosis is clearly ascribable to differential survival, the facts suggest that there is a substantial opportunity, indeed a likelihood, for a contribution from differential mating among surviving adults. F the various components of Darwinian fitness, to, the deme under examination. Since fitness char- 0 simple survivability is fairly easy to measure and acters have a polygenic basis, the use of single-gene has tended to dominate thinking about selective proc- markers is insufficient. Polymorphisms consisting of esses. New data on sexual selection, however, indicate inversions, however, may cover some considerable that many individual organisms, especially males, may part of the genome; as markers, these are much more survive well and engage in courtship yet fail to partic- desirable. This set of conditions has almost never been ipate significantly in reproduction (e.g., LANDE198 1 ; realized experimentally. For example, BOSIGER THORNHILLand ALCOCK1983). The sexual activity (1962), and those who followed him using similar of the individual is surely of paramount theoretical techniques, have tended to rely on the use of geno- importance in fitness yet has been little studied (but types marked experimentally by initially making inter- see ANDERSONet al. 1979). The reason for the lack of strain crosses. Individuals carrying the markers are data appears to stem from the double difficulty of then introduced into an experimental population, per- measuring this trait phenotypically and then relating mitting them to be distinguished from the resident the measure directly to a genetic basis. The individual members of the deme. As a result, the differential not only must be marked so that sexual performance reproduction that may be observed does not represent can be monitored but the relative contribution of this that which occurs naturally within the deme. Rather, individual to the next generation must also be esti- any effect is the result of artificial interdeme hybridi- mated. zation. Striking heterozygote advantage has often As fitness of an individual must be determined been demonstrated in this manner, yet the relevance relative to other competing members of the same local of the results is questionable. The goal of such exper- population or deme, proper genetic control requires iments, namely, to understand the genetics of the the use of markers that are intrinsic in, and not foreign mating patterns that have evolved and exist in a Genetics 116 415-422 (July, 1987) 416 H. L. Carson natural, complex balanced gene pool is not well served a series of such samples from a single locality, the frequencies by such a procedure. of the various inversions carried in the source wild popula- tion can be deduced from orcein smears of the salivary When a field of related surviving males compete gland chromosomes of the F, larvae. It may sometimes be for the favors of females in natural populations, a inferred that the female was carrying sperm from more than crucial question is: to what extent does relevant seg- one wild male (CRADDOCKand JOHNSON 1978). regating genetic variation occur among the members Laboratory stocks: In order to produce a vigorous iso- female stock of D. silvestris, F, of such a field? If such genetic variation can indeed an from a single wild female of no less than 30 flies of each sex is desirable. This should be shown to exist, then is it possible to demonstrate assure that about 10 high-fitness males are available for that differential reproductive success is served by any getting the stock started (CARSON1986). If possible, how- of the blocks of polygenic genetic variants that are ever, 72 flies matured in vials are used. These imagoes are segregating naturally within it? placed together in a large (4 liter) glass jar, the bottom of The experiments to be described here employ a which contains a layer of about 8 cm of sterile sand mois- tened with distilled water. As a source of food and as an single laboratory population of Drosophila silvestris, a oviposition site, about six shell vials (95 X 30 mm) containing species endemic to the Hawaiian islands. This species a small amount of food high in plant proteins are placed in has been subjected to a number of genetic and behav- the jar. The formula of WHEELERand CLAYTON(1965) is ioral investigations (for reviews, see CARSON1978, used but the yeast is omitted. These vials are left open at 1982, 1986). Like many Hawaiian Drosophilas, the end and are laid horizontally on the sand. Each vial also D. contains a piece of paper tissue that has been saturated with silvestris displays a number of secondary sexual char- an aqueous extract of the leaves of a host plant. The flies acters of males that are used in the courtship proce- are free to enter and leave the vials for feeding and ovipo- dure (SPIETH 1978). The species has extensive genetic sition. A cloth screen covers the tap. The large open area variability in inversions and allozymes both within and within the jar serves as an arena for courtship, mating and between populations (SENEand CARSON1977; CRAD- reproduction much as in an ordinary population cage. The life cycle is completed in the following manner. Vials DOCK and JOHNSON 1979). More recently, intra- and containing eggs and small larvae are harvested from the jars interpopulation genetic variance in certain secondary and at the same time are replaced with fresh ones. During sexual characters has also been demonstrated (CARSON this procedure, the standing adult population is allowed to and BRYANT1979; CARSONet al. 1982; CARSONand remain undisturbed within the jar. Vials containing larvae LANDE1984; CARSON1985). are given a heavy feeding with cornmeal medium, plugged with stoppers, slanted and stored separately until mature Experiments with marked males in experimental third-instar larvae start leaving the food. At this time, the cage situations strongly suggest that both epigamic vials are placed on sterile sand in a fresh 4-literjar. Pupation and intrasexual sexual selection is operative in popu- occurs in the sand. lations of this species (SPIESSand CARSON198 1 ; CAR- After the larvae have evacuated the food vials, the latter are removed and replaced with open yeastless vials that SON 1986). In cages, approximately one third of ma- serve as a source of nutrition for the emerging imagoes. ture, healthy, actively courting males surviving to four Occasionally, young maturing adults are added to the stand- weeks of age were found to be unsuccessful in achiev- ing population in the oviposition jars in order to gradually ing copulation whereas another third accomplish replace the older flies, create a distribution of ages and to about two-thirds of the observed matings. maintain a census population size of between 40 and 60 flies The present study extends the differential analysis per jar. Two such jars are normally maintained for each stock. These cultures are maintained at 18" and yield 3-4 of marked males to include assaying the reproduc- generations per year; they are maintained without outcross- tively successful ones for genetic inversion markers ing. carried naturally by the experimental population. The Experimental population: The experiments to be de- results indicate (1) that there is ample genetic varia- scribed here were done with a single chromosomally poly- bility carried naturally in males of this population, (2) morphic laboratory population (U28T2). It is descended from a single wild female collected at Kilauea Forest Re- that this variation can be related to the reproductive serve, Island of Hawaii, in January 1977. It is a vigorous success or failure of these males and (3) that success- stock that has been maintained approximately as described fully reproducing individuals of both sexes show a above without bottlenecks.
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