Great Basin Naturalist

Volume 47 Number 1 Article 5

1-31-1987

Drosophila pseudoobscura (Diptera: ) of the Great Basin IV: a release experiment at Bryce Canyon

Monte E. Turner University of Akron, Akron, Ohio

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Recommended Citation Turner, Monte E. (1987) " pseudoobscura (Diptera: Drosophilidae) of the Great Basin IV: a release experiment at Bryce Canyon," Great Basin Naturalist: Vol. 47 : No. 1 , Article 5. Available at: https://scholarsarchive.byu.edu/gbn/vol47/iss1/5

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DROSOPHILA PSEUDOOBSCURA (DIPTERA: DROSOPHILIDAE) OF THE GREAT BASIN IV: A RELEASE EXPERIMENT AT BRYCE CANYON

Monte E. Turner'

Abstract —Some populations of Drosophila pseudoohscura in the Great Basin have verv httle genetic variation for third chromosome mversion gene arrangements. These populations are essentially monomorphic for the Arrowhead gene arrangement. At Bryce Canyon, Utah, individuals with other gene arrangements (Standard, Pikes Peak and Treelme) were released and their frequencies monitored. One generation after release, the released arrangements had mcreased in frequency from 0.7% to almost 10%. After overwintering, the arrangement frequencies were not statistically different from the prerelease samples. The samples did demonstrate a low-level retention of the released Pikes Peak arrangement. The decline in the released arrangements was probably the result of large population size at Bryce Canyon and the bottleneck effects of overwintering. The results do not seem consistent with a model of the released arrangements having a lowered fitness.

Natural populations of Drosophila pseti- characterized as nearly monomorphic for the doobscura have been studied for over 40 Arrowhead (AR) gene arrangement, while the years. Populations were originally cytologi- other races are highly polymorphic. cally characterized for the gene arrangements Populations of the Intermountain Plateau of the third chromosome (Dobzhansky and were originally sampled and characterized in Sturtevant 1938), and these arrangement fre- the early 1940s. Those areas which have been quencies were monitored. The different gene sampled regularly (Bryce Canyon, Utah; Leh- arrangements are the result of a phylogeny of man Caves, Nevada; and three localities in mostly overlapping inversions of segments of Arizona) have remained essentially the same the third chromosome (Dobzhansky 1944). as the original samples (Anderson et al. 1975). Because of greatly reduced recombination During 1976 and 1977 six areas in the north- within the inverted segments in heterokary- ern Intermountain Plateau area were sam- otypes, these inversions act to tie together pled; some of these sites had not been sam- portions of the chromosome into large super- pled since they were originally characterized genes. These supergenes (gene arrange- in the 1940s and 1950s. This area, which had ments) are inherited and behave in popula- previously been characterized as nearly tions as alleles at a single locus. Some natural monomorphic AR, had undergone populations of D. pseudoohscura have been great changes both in the particular gene arrange- sampled repeatedly since the 1930s (Ander- ments present and their frequencies (Turner son et al. 1975) and provide an excellent his- and Jeffery 1980). These populations now torical basis for current research. These con- have an arrangement array very similar to that tinuing geographic surveys over the range of found in the Rocky Mountain populations D. pseudoohscura have led to the division of (Race 3) including the endemic Fort Collins the into five geographic races, each arrangement, previously found only characterized by the gene arrangements in a few areas of the Rocky Mountains. It was present and their frequencies (Dobzhansky hypothe- sized that these changes came about because and Powell 1975). These races are: of gene flow into these northern Intermoun- Pacific Coast tain Plateaus (Race 2) from the Rocky Moun- Intermountain Plateau tains (Race 3) (Turner and Jeffery 1980). Rocky Mountains and Texas The release of Northern Mexico genes into natural popula- Southern Mexico and Guatemala tions has been attempted previously with pos- itive results. Bryant (1976) released D. pseu- Race 2, the Intermountain Plateau, has been doohscura with a rare esterase allozyme into a

Department of Biology, University of Akron, Akron. Ohio 44.325.

32 January 1987 Turner: Drosophila Release Experiment 33

small oasis population in Death Valley, Cali- (PP) gene arrangements were released in the fornia, in an attempt to swamp the population southern sampling area. The to be re- and then determine the amount of immigra- leased were grown in large population cages tion in the population. Thirty-eight days after which support approximately 12,000 adult the release, the frequency of the genetic flies. The releases were accomplished by marker had increased from 2% before the re- opening these cages and allowing the adults to lease to approximately 80%. Dubinin and escape. Thus the released flies were a mixed Tiniakov (1946) released D. funebris with an sample of age and sex, and no attempt was inversion from another locality into a popula- made to release only virgin flies. This was tion where that inversion was rare. The fre- done in five separate release events over the quency of the released inversion was origi- span of three days, one release daily during nally 0.35% and increased to a high of 49.5% the evening activity period and on two days approximately one generation after the re- releases during the morning activity periods. lease. These two results show that it is possi- Approximately equal numbers (approx. ble to introduce outside genes or gene ar- 12,000) of each homozygous type were re- rangements (even those that have been in the leased during each event, and the total num- laboratory for some time) into a natural popu- ber of individuals released was approximately lation and that they can become integrated 200,000. No flies were released in the other into that population at fairly high frequencies. two sampling sites. Afl three sites were subse- This research investigates, through the use quently sampled and characterized geneti- of a release experiment, the inversion gene cafly during August 1978 and June, August, arrangement polymorphism in an Intermoun- and September 1979. tain Plateau population of Drosophila pseu- Origin of Released Chromosomes.—The doobscura. released PP stock was derived from a collec- tion made in June 1977 at American Fork, Utah. In this collection PP had a frequency of Materials and Methods 18.9%. The TL stock came from a collection in Sampling Sites and Methods.—Three lo- Big Cottonwood Canyon, Utah (near Salt of cations in Biyce Canyon National Park, Utah, Lake City), in June 1977. The frequency TL were selected as sampling sites. These three in this population was 25.0% (Turner and Jeff"- Mather, sites are separated by distances such that mi- ery 1980). The ST stocks were from the gration by individuals between the sites was California, and have been maintained in thought to be negligible. The southern and laboratory since 1959. northern sampling sites are 14 km apart. The middle site is 5 km from the southern site and Results and Discussion 9 km from the northern site. These three areas chromosome are quite diverse and probably encompass the The frequencies of the third initial sample entire range of possible D. pseudoobscura gene arrangements from the along with the habitats in Bryce Canyon. The southern sam- (June 1978) are given in Table 1 previous samples of Bryce pling site is the least arid and the most similar totals from are significantly of the three sites to the northern Intermoun- Canyon. The June 1978 totals samples total (X tain Plateau. Because of this similarity, this different from the previous

= df ) but not significantly site was chosen for the release. During 21-28 13.45, p < .01, 3 sample of June 1978, samples were obtained from each different from the latest (1973) = .25, 1 df). The three of these three sites. Individual females ob- Bryce (X' 1.51, p < differences in tained from nature were used to establish sample sites have no significant frequencies (Table (X" = isofemale lines, and Fl larvae were character- gene arrangement 1)

). 1978 samples had ized cytologically for the gene arrangement of 1.4, p< .79, 2 df The June (TL) and Bryce the third chromosome using standard two arrangements, Treeline Bryce Canyon Drosophila salivary techniques. (BR), not previously found in is a new ar- The Release —On the three days immedi- samples. The BR arrangement inversion of Arrowhead (AR) ately following the completion of the initial rangement, an 80C. samples, D. pseudoobscura homozygous for with breakpoints 71B and place after the June 1978 Standard (ST), Treehne (TL), or Pikes Peak The release took 34 Great Basin Naturalist Vol. 47, No. 1

Table 1. Percentage of third chromosome gene arrangements of D. p.->eiidoobscura from Brvce Canyon before the release (n = number of chromosomes).

Site January 1987 Turner: Drosophila Release Experiment 35

Table 3. Percentage of third chromosome gene arrangements from sites in Bryce Canyon for snnnner following August 1978 release (n - nnmher of chromosomes).

Date 36 Great Basin Naturalist Vol. 47, No. 1

fery 1980), nearly 5,000 chromosomes have enter a small isolate and increase in frequency been characterized and SC has never been (as the result of either stochastic or selective identified in this region. Whether SC has al- mechanisms). This type of population struc- ways at been Bryce but in extremely low fre- ture would minimize the effects of migration quency or whether this SC came with an indi- in changing gene frequencies. vidual immigrant (active or passive) from a Additionally, to persist in this population, population where the SC arrangement is an arrangement (or gene) must survive the found cannot be determined at this time, al- winter. When high-elevation populations though the latter seems the more probable overwinter, they undergo a severe bottleneck alternative. in population size because of the low tempera- TL, which had reached levels close to 5% in tures. How D. pseudoob.scura overwinter is the southern sampling area 42 days following not known, but overwintering is unquestion- the release (Table 2), was not observed in over ably a severe process. In laboratory experi- 1,000 chromosomes examined in 1979, of ments on overwintering ability only a small which almost 500 came from the southern frequency of the flies survive cold shocks of (release) area (Table 3). A second gene ar- just a few days (Jefferson et al. 1974), and over rangement in the release. Standard (ST), did a winter of six to eight months only a very not show a significant increase in postrelease small number of individuals may survive. In samples (Table 2) and had approximately the this way, the released arrangements may not same frequency in 1979 (Table 3) as that seen survive the winter and the sampling effect of in the 1978 prerelease samples (Table 1). In the resultant population bottleneck. This bot- the June 1979 sample from the northern site, tleneck would eventually cause the popula- Standard has a frequency of 4.4% (Table 3), tion to lose variability through genetic drift. but it decreased and was not found in the These results also bear on the question of August 1979 sample from this site. Standard overwintering; that is, whether these higher- did not show a frequency increase in the re- altitude populations overwinter in place (at lease area (Tables 1,2). The observation from altitude) rather than be repopulated each the northern site could be the result of migra- spring from lower-altitude overwintering tion of the released flies (or their offspring) to refugia. The latter hypothesis is similar to that the northern site or the result of sampling observed in the desert populations of D. pseu- error due to small sample sizes. The results of doobscura where populations are refounded these two arrangements (TL and ST) are simi- each year from neighboring mountains after lar and consistent with no long-term effect of the hot summers have eliminated the popula- the release. tions (Jones et al. 1981). The persistence of the The PP gene arrangement had not been Pikes Peak (PP) arrangement would be consis- found in Bryce since 1964, but it did reach a tent with an overwintering-in-place hypothe- level of 3.6% following the release (Table 2) sis and not a repopulation each spring from and was found in low frequency (0.3%) in lower-altitude populations. 1979. During the 1979 samples PP was found A decrease in frequency due to small fitness in all three sample sites and is most probably a differences would take many generations. The low-level retention following the incorpora- PP and TL arrangements were isolated from tion of the released PP arrangement into the areas with an environment and elevation Bryce Canyon gene pool. This result would roughly similar to Bryce Canyon. Both ar- indicate that the earlier assumption that the rangements were in relatively high frequency sites were far enough apart to ignore migra- where found originally, PP being almost 20% tion was incorrect. In the two to three genera- and TL 25%. Thus, if fitness differences do tions since the release all three sites have two exist between the released chromosomes and (PP and ST) of the three released arrange- the native AR, they most likely would be ments, a linear distance of 14 km. With this small. Since D. pseudoobscura do not repro- level of migration we can consider this area as duce during the winter, from August 1978 supporting one large breeding population. In until June 1979 there is only one generation this large population an introduced gene (re- and at most two. The rapidity of the decrease leased or migrant) may be swamped by the would suggest that if the decrease were due to local (AR) gene pool, without being able to an inherent selective disadvantage, this fit- January 1987 Turner: Drosophila Release Experiment 37

Drosophila pseudoohscura and its relatives. ness diflference must be extremely large. The Carnegie Institution of Washington Publication rapid decrease would seem more consistent 554. 133 pp. effect of a large population 1975. Drosophila with the swamping Dobzhansky, T., and J K Powell. size and random drift in ovei-wintering popu- pseudoohscura and its American relatives and Drosophila miranda. In lations. R. C. King, ed.. Handbook of genetics: inverte- brates of genetic interest. Vol. 3. Acknowledgments Dobzhansky. T.. and A. H Sturtevant. 19.38. Inversion in the chromosomes of Drosophila pseudooh- 28-64. scura . Genetics 23: I am grateful for the assistance of the Na- Dobzhansky, T., and S. Wright. 1943. Dispersion rates tional Park Service staff at Bryce Canyon Na- in Drosophila pseudoohscura. Genetics 28: of this project tional Park and for discussions 304-340. and Duane E. Jeffery. 1946. Inversion gra- with Wyatt Anderson Dubinin, N P , and G. G. Tiniakov. This research was supported by an NSF doc- dients and natural selection in ecological races of Drosophila funehris. Genetics 31: 537-.545. toral dissertation improvement grant. Jefferson, M. C, D. W Crumpacker, and J S. Williams. 1974. Cold temperature resistance, Literature Cited chromosomal polymorphism and interpopula- tional heterosis in Drosophila pseudoohscura. Powell. Genetics 76: 807-822. Anderson, W. T. Dobzhansky, O. Pavlovsky, J. Lewontin, A Moore, S , S H. Bryant. R C andD.Yardley. 1975. Genetics of natural popula- Jones, J. J. Prout. 1981. Gene flow and the geographi- tions. XLII. Three decades of genetic change in andT polymorphism in Drosophila pseudoohscura. Evolution 29: 24-36. cal distribution of a molecular lethal Drosophila pseudoohscura. Genetics 98: 157-178. Bryant, S. H 1976. The frequency and allelism of 1980. Drosophila . E. Jeffery. chromosomes in isolated desert populations of Turner. M E and D Basin. II. Third chro- Drosophila pseudoohscura. Unpublished disser- pseudoohscura of the Great arrangements of selected northern Utah tation, University of California, Riverside. mosome populations. American Naturalist 115: 771-779. Dobzhansky, T. 1944. Chromosomal races in Dro.wp/H/« 1983. Multiple pseudoohscura and Drosophila pcrsimilis. Pages Turner. M E , and W W Anderson. female fitness in Drosophila pseu- 47_144 in T. Dobzhansky and C. Epling, Contri- mating and Evolution 37: 714-723. butions to the genetics, and ecology of doohscura.