D. TRANSVERSA (DROSOPHILIDAE:DIPTERA)
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1 Evolution, 35(1), 1981, pp GEOGRAPHICAL VARIATION IN THE REPRODUCTIVE CYCLE AND PHOTOPERIODIC DIAPAUSE OF DROSOPHILA PHALERATA AND D. TRANSVERSA (DROSOPHILIDAE:DIPTERA) OUTI MUONA AND JAAKKO LUMME Department of Genetics, University of Helsinki, SF Helsinki 10, Finland and Department of Genetics, University of Oulu, SF Oulu 10, Finland Adaptation to seasonal changes is of great importance to insects. The energyconsuming developmental processes are limited in the north by winter and often in the south by summer drought. Many insects spend the adverse seasons in a state of dormancy controlled by photoperiod (Beck, 1968). Geographical variation in photoperiodic reactions is well known in insects (see reviews by Danilevskii, 1965; Beck, 1968; Saunders, 1976; Hoy, 1978). In general, a clear south-north cline is observed, with northern populations entering the hibernation stage earlier than southern. Such geographical variation in Drosophila littoralis has been studied by Lumme and Oikarinen (1977) and Oikarinen and Lumme (1979) (see also Lumme, 1978). However, field studies corresponding to laboratory results have been lacking. We undertook to study the adaptation to seasonal environment by relating field observations on population dynamics to the laboratory determined photoperiodic reactions. We studied populations at different latitudes to find out how different climatic conditions are reflected in the population dynamics in the field, and, on the other hand, in photoperiodic reaction curves. Photoperiodic timing of adult reproductive diapause in the genus Drosophila was first demonstrated in D. phalerata Meigen and D. transversa Fallen (Geyspits and Simonenko, 1970). From photoperiodic reaction curves obtained in laboratory studies, Geyspits et al. (1976) inferred that D. phalerata must have a summer diapause as well as a winter one. Geyspits and Simonenko (1970) studied populations Received September 7, Revised March 18, of D. phalerata from two different latitudes and found diapause differences between them. Both species are quite common and easily collected with fermenting baits. Both are known to be fungivorous (Burlaand Bachli, 1968). Their distributions overlap widely, but D. phalerata reaches its ecological margin in Central Finland. Itis more common in central and southern parts of Europe (Shorrocks, 1977), but its southern limit is not well known. Drosophila transversa is abundant up to the coast of the Arctic Ocean, but rather rare in Central Europe, where it is mostly found at high altitudes (Burla, 1951; Shorrocks, 1977). These species thus obviously have different adaptations to climate. Can this be seen in their phenology or photoperiodic reactions? METHODS Observations on wild populations. Data on natural populations were collected in 1974 and 1975 in Finland. In 1974 the studies were made in Lammi (61 3'N, 25 5'E) and Oulu (four separate localities, about 65 N, E; see Lumme et al., 1978). In 1975 we collected flies in Helsinki (60 01O'N, 24 57'E; see Muona et al., 1978), Hattula (61 8'N, 24 21'E) and Oulu. The methods used in the field work have been described earlier (Lumme et al., 1978), and are similar to those generally used since the work of Dobzhansky and Epling (1944). We classified the wild collected females into three categories: 1) having ovaries that are completely undeveloped, 2) having ovaries that are developing, but not yet mature, and 3) having mature ovaries. The males were not dissected, but were counted. The general ap-
2 Locality, country 2 TABLE 1. The origins of laboratory strains. () t':i Number of founders 0 Mean temperature () transversa phalerata Altitude Daylength range Latitude m above July January ~ " 2 " N Longitude sea level minimum maximum C C >,;j ::q Ivalo, Finland' ' 27 38' E h H () Kuusamo, Finland' ' 29 21' E h r- > Oulu, Finland' r 25 30' E 5 3 h 35' 22 h 4' Vaajasalo, Finland" ' 27 50' E 80 5 h 4' 19 h 53' < > Hattula, Finland' ' 24 21' E 80 5 h 30' 19 h2o' 17-8 ~ > Helsinki, Finland! ' 24 57' E 10 5 h 50' 18 h 55' 18-5 >-3 Leeds, England" ' 1 35' W 50 7 h 22' 17 h 9' 16 3 H Zakopane, Poland' ' 19 54' E 1,000 8 h 14' 16 h 15' 18-3 Z Stare Hory, Czechoslovakia' ' 19 7' E h 22' 16 h 3' 18-3 H Z Rossatz, Austria' ' 15 30' E h 25' 16 h 0' 20-1 t:i Langenwang, Austria' ' 15 37' E h 30' 15 h 53' 20-1 ~ Budapest, Hungary' ' 19 3' E h 31' 15 h 52' 22-1 a VJ Cluj, Roumania" ' 23 37' E h 40' 15 h 48' 20-3 a Zernez, Switzerland" ' 10 6' E 1,500 8 h 42' 15 h 46' 14-7 ~ ::t: Rila, Bulgaria' ' 23 33' E 1,000 9 h 10' 15 h2o' 21-2 I Collected and studied in 1975, :l coll. and studied in 1976,:1 coil. and studied in 1978, 4 data from Charlesworth and Shorrocks, ~... U1. \0
3 160 O. MUONA AND J. LUMME D. transversa Helsinki 20 Lammi HaUula % 100 Oulu o May June July Aug Sap May June July I Aug I Sep FIG. 1. Reproductive status of Drosophila transversa populations in different localities. In each column: black-proportion of females with mature ovaries; shaded-females with developing ovaries; white-females with undeveloped ovaries. The columns represent two-week periods. The number of females studied is indicated above each column. pearance of flies of both sexes also gives information on the developmental status of the population. Overwintered flies can be distinguished by their dark pigementation, damaged wings and broken bristles, which make them look "aged." Newly emerged flies are very lightly pigmented. Outdoor culture experiments.-to obtain basic information on the developmental rates, some small culture experiments were performed in the summer of 1975 in Oulu and in 1976 in Helsinki. The methods were those used by Begon (1976) and Lumme et al. (1978). Males and females caught from the wild were put in malt medium tubes, which were set outside to receive natural light and temperature. The females laid eggs and were then transferred to new tubes. Laboratory experiments.-establishment of the laboratory strains is described in Table 1. To avoid unintentional selec-
4 GEOGRAPHICAL VARIATION IN DROSOPHILA 161 D. phalerata Helsinki 2 35 Hi 4 Lammi Hattula % loa Oulu o May June July Aug Sep May June July Aug Sep FIG. 2. Reproductive status of D. phalerata populations in different localities. See Fig. 1 for explanations. tion, we studied the strains as soon as possible, usually within the first three laboratory generations (Oikarinen and Lumme, 1979). Photoperiodic reactions were determined according to methods described by Lumme and Oikarinen (1977): females eclosed under continuous light (at about 20 C) were kept for three weeks on malt medium at 16 C in different daylengths, and were dissected and classified into two categories: 1) diapausing (ovaries previtellogenic) and 2) non-diapausing (vitellogenesis at least started). The average number of females dissected per strain per light regime was about 80. The following points were based on less than 40 females: pha Lang 9:15 (31), pha Rila 10.5:13.5 (34), pho Lang 13.5:10.5 (21), pha Rila 13.5:10.5 (37), and pha Lang 15:9 (37). RESULTS Description of the seasonal life cycle in Finnish populations.-the results of our study ofthe reproductive status of natural populations are presented in Figure 1 for
5 162 O. MUONA AND J. LUMME TABLE 2. D. transversa in outdoor culture experiments. Number of emerged Parents Egg-laying time Time ofeclosion individuals Ovarial stages! Helsinki 1976 Wintered flies June 8-30 July July July 31-Aug Aug st generation July Aug Aug. 25-Sept Sept Sept. 18-0ct Oulu 1975 Wintered flies June July July st generation Aug. 2-5 Sept no females Sept were dissected Oct Oct Aug Sept Oct Oct Ovarial stages 3 weeks after the last eclosion date: 1) undeveloped, 2) developing, 3) mature. D. transversa and Figure 2 for D. phalerata. The data from localities Lammi (1974) and Hattula (1975) are on the same part of the Figures, because the localities are less than 40 km apart. For both species and all populations, the reproductive cycle is basically similar. In the spring the change from an immature at least apparently diapausing population, to an egg-laying one is gradual. The wintered adults become active and the ovaries of females start developing (shaded in Figs. 1 and 2). Then the flies mate. The correspondence between ovarial stages and insemination proved to be good: only females with developing or mature ovaries are inseminated. Females with undeveloped ovaries had no sperm in their spermathecae. The females begin to lay eggs in May and some may live until July. Throughout May and the beginning of June both mature and immature females of the overwintered generation are present in the populations (Figs. 1 and 2). The first adults assignable to the summer generations begin emerging at about the end of June. We know from outdoor culture experiments that most, if not all, of the females emerging in June or July reproduce that year and die before September (see Table 2). Toward the end of summer few mature females are caught (see September results in Oulu for both species), and in outdoor cultures mature females are killed by frost. Females emerging late in the summer remain immature (i.e., diapause) until the following spring. We were unable to make detailed comparisons between latitudes, because certain samples were not sufficiently large. The lack of D. phalerata in Oulu in 1974 was due to a real rarity of the species in this marginal area of the distribution. D. transversa.-some specifics shown in Figures 1 and 2 may be added to the main features of the reproductive cycle described above. In spring, 1974, the flies seemingly developed faster in Lammi than in Oulu, In both localities the first summer generation did not start emerging until the beginning of July. Many of the first generation flies developed and reproduced, as shown by the high proportion of developing females in August. These females laid their eggs on fungi, and the 1974 fun-
6 GEOGRAPHICAL VARIATION IN DROSOPHILA 163 gal crop was exceptionally abundant in all parts of Finland. In September most females were diapausing. In 1975 the flies were much more numerous than in 1974, probably due to the good fungal crop of Comparisons between Oulu and Helsinki show that reproduction started earlier in the south (differences in female reproductive stages: May, X 2 = 6.0, P <.05; beginning of June, X 2 = 9.7, P <.01). In the last days of June no trapping was done in Helsinki, but in Hattula and Oulu the first flies of the summer generation were caught. In Oulu, the first flies of the summer generation were trapped two weeks earlier than in 1974 probably because in 1974 the May mean temperature was 5.7 C and in 1975 it was 8.9 C. The 1975 samples provide a comparison on the timing of the end of the reproductive season. Reproduction continues longer in Helsinki than in Oulu (X 2 = 49.0, P <.001). D. phalerata.-the reproductive cycle is very similar to that of D. transversa. Comparisons between latitudes are difficult because D. phalerata was so rare in 1974 in Oulu. The first individuals were caught in August. These were newly emerged and probably diapausing. At the same time many females in Lammi were still laying eggs. Outdoor culture experiments.-the results of these experiments-which agree with the field data-are given in Table 2. The developmental time is quite long, about one month during the warmest period and much longer later in the summer. These results and the field observations lead us to the conclusion that both species have about two generations a year in Oulu, and maybe even a partial third generation in Helsinki. However, the generations overlap widely. The long egg-laying time of overwintered flies by itself is enough to prevent completely any synchrony among individuals and thus also non-overlapping generations. The widely varying developmental time also contributes to nonsynchronization. Laboratory experiments: genetic variation in photoperiodic diapause.-the photoperiodic reactions of D. transversa are shown in Figure 3 and those of D. phalerata in Figure 4. The photoperiodic reactions of Finnish strains are about what could be expected. They have a clear-cut short-day diapause reaction: short daylengths towards the end of the summer prevent reproductive maturation of eclosing adults. The critical daylengths (where 50% of the females diapause) varied between 15.9 and 16.6 h for D. transversa and between 15.7 and 17.1 h for D. phalerata in Finland. This agrees with the field observations and culture experiments, too. In middle and late August the daylengths correspond approximately to the above critical daylengths, and at this time most of the females eclosing in the wild remain undeveloped. However, we observed a surprisingly low level of genetic differentiation between strains. Pairwise x2-tests for diapausing vs. nondiapausing females in the important daylengths LD 15:9, 16.5:7.5 and 18:6 proved to be nonsignificant for most strains. This is in contrast to most cases reported in the literature. For instance, the critical daylength of Acronycta rumicis (Lep: Noctuidae) strains changed about 1.5 h with every 5 latitude (Danilevskii, 1965). The critical daylength of the northernmost strain of D. transversa (69 N) corresponds to August 24, that of the southernmost strain within Finland (60 0N) to August 8. Our field data show that these dates do not reflect the behavior of the populations in the field. A similar lack of genetic differentiation was observed for D. phalerata, but to a lesser degree. This surprising result led us to study population samples from more southern parts of Europe. The results are rather similar for both species, but the data are more conclusive for D. phalerata. All the photoperiodic reaction curves of continental European populations were essentially similar to each other. Within the ecological range of daylengths (Table 1), these populations have a high diapause response at Very short and very long daylengths and a low diapause response in the intermediate LD 13.5:10.5 daylength, as
7 164 O. MUONA AND J. LUMME 10 % Diapause 50 o o Light/24h FIG. 3. Photoperiodic reaction curves of D. transversa strains. He: Helsinki, Ku: Kuusamo, Ou: Oulu, Iv: Ivalo, Ha: Hattula, Va: Vaajasalo, Ze: Zernez, Ro: Rossatz, Bu: Budapest. Information on these localities is given in Table 1. seen in Figures 3 and 4. The high responses were observed in light regimes corresponding to daylengths in late fall (and, of course, very early spring, but presumably no adults eclose at that time) and midsummer. Evidently these populations have both a winter and a summer diapause. At the population level, diapausing and reproduction are always partial responses, since we did not observe 0 or 100% diapause. In both species, the high altitude population from Zernez, Switzerland (45 N, 1,500 m above sea level), differed from other central European populations. The shape of the reaction curve was similar to that of Finnish populations, but the critical daylength was 13 h. In the ecologically relevant part of the curve, 9 to 16 h of daylength, there is a gradual decline in diapause percentage, whereas other central European populations have a peak in diapause percentage at LD 10.5:13.5, a low at LD 13.5:10.5, and another peak at LD 15:9. The high alpine populations obviously have a seasonal cycle resembling that in Finland, without any aestivation. Unimodal curves were also observed for English populations by Charlesworth and Shorrocks (1976) (Leeds, 54 N), with critical daylengths 14.8 hand 12.7 h (at 15 C) for D. phalerata and D. transversa, respectively. DISCUSSION Population dynamics and seasonal cycles are in general poorly studied in Drosophila. Many studies have been made on seasonal fluctuations of numbers of flies of different species, but the data are inadequate for understanding population dynamics because nothing is known about the reproductive status of the populations (e.g., seasonal variation in the numbers of D. phalerata has been recorded by Herting, 1955, and Rocha Pite, 1977, in central and southern European populations). Recently, however, a few relevant studies have been made: Begon (1976), Charlesworth and Shorrocks (1976), Watabe (1977, 1979), Watabe and Beppu (1977), Kimura et al. (1978), and Toda and Kimura (1978) recorded the reproductive status of the flies. We have made such a study on several species in northern Finland (Lumme et al., 1978).
8 GEOGRAPHICAL VARIATION IN DROSOPHILA 165 Olapause 100 % He Ha 50 Continental European strains CI o o L1ght/24h FIG. 4. Photoperiodic reaction curves of D. phalerata strains. He: Helsinki, Ha: Hattula, Ou: Oulu; Va: Vaajasalo, Ze: Zernez, La: Langenwang, Ro: Rossatz, SH: Stare Hory, Ri: Rila, Za: Zakopane, CI: Cluj. Even with these kinds of data, there remain certain difficulties in interpretation. The proportion of females in different reproductive stages depends on several inseparable factors: the initial number and longevity of overwintered adults, the eclosion rate of new adults, the proportion of maturing vs. diapausing females among these flies, and the adult maturation rate. Thus additional data, from, e.g., outdoor culture experiments, may be necessary for determining the number of generations or duration of egg-to-adult development. A specific question arising from our observations is: why are the populations not genetically differentiated? In most cases insects have a clear cline in the photoperiodic reaction, so that northern populations stop reproduction and start diapausing at longer daylengths than southern populations (Danilevskii, 1965). The main adaptive significance of the photoperiodic diapause is that changing daylengths allow the organism to obtain very accurate information on the time of season. Temperature and other, less regular environmental factors often have some effect of diapause, but usually photoperiod is the main determinant (Beck, 1968). In the present case it is clear that the timing of diapause has to depend heavily on factors other than daylength. One hypothesis is that the diapausing of these species is very much influenced by the fungal crop, which is a highly variable resource, both temporally and spatially. Our data are in accord with this hypothesis: the population sizes of D. transversa and D. phalerata (as well as that of a third fungivorous species, D. testacea) appear to be more variable between years than those of many other ecological groups of drosophilids. In Oulu the ratio of the number of overwintered flies caught in 1974 to the number caught in 1975 was 1:11 for D. transversa (trapping effort was equal in both years). No overwintered D. phalerata or D. testacea were caught in 1974, but 68 and 496, respectively, were caught in 1975 (Lumme et al., 1978). Similar ratios for five other species ranged from 1:0.6 to 1:5.8 (Oulu is in the center of geographic range for all five species). The fluctuations in the numbers of D. phalerata and D. testacea are presumably partly due to the marginality of the populations, but the D. transversa population is a central one, and we attribute the fluctuation
9 166 O. MUONA AND J. LUMME to variation in the amount of available fungi. Thus the fungivorous species seem to be able to exploit efficiently the occasional abundant fungal crops by continuing reproduction into late summer. The partial diapause response of central European populations in any daylength possibly has a similar explanation. Some individuals in the population can always reproduce, should conditions be favorable. This variation may be maintained by an uncertain and unpredictable environment. The variable resources could promote migration and gene flow, and thus lead to reduced adaptation to the local combination of climate and daylength, but the role of migration in maintaining the genetic similarity of the populations is now known. Good estimates of gene flow in Drosophila in natural conditions are not available, though attempts have been made at measuring migration (see, e.g., Powell et al., 1976). Drosophila phaierata and D. transversa are ecologically similar species, both using the same fungal resources. Our study did not show any real differences in the timing of their annual population cycles. More detailed studies are needed to reveal the causes for their different distributional patterns. SUMMARY Drosophila transversa and D. phalerata are fungivorous species that have a photoperiodically regulated adult reproductive diapause. They both have a wide distribution area in Europe, D. transversa being more common in the north, D. phalerata in the south. We studied population dynamics in the field in Finland and found that these species have two generations a year in northern Finland, and two and a partial third in southern Finland. Laboratory observations on the photoperiodic responses of strains from Finland showed that there was little genetic differentiation with respect to this character. All Finnish populations had a clear-cut short-day diapause. Central European populations were polymorphic with respect to diapausing in all daylengths studied. These results were in contrast with the common pattern among insects, which is a clear north-south cline in photoperiodic responses. Gene flow between populations and adaptation to variable resources are possible explanations for the lack of genetic differentiation. ACKNOWLEDGMENTS We are grateful to Jyrki Muona, Markku Orell, Pekka Lankinen, Pirkko Sammallahti and Marja-Liisa Lokki for help in collecting the material. We wish to thank Prof. Seppo Lakovaara for his support and encouragement throughout this study. Drs. Timothy Prout and Elmarie Hutchinson provided valuable comment on this manuscript. Financial support from The Emil Aaltonen Foundation, The Finnish Academy of Science and the National Research Council for Sciences of Finland is acknowledged. LITERATURE CITED BECK, S. D Insect Photoperiodism. Academic Press, N. Y. BEGON, M Temporal variations in the reproductive condition of Drosophila obscura Fallen and D. subobscura Collin. Oecologia 23: BURLA, H Systematik, Verbreitung und Okologie der Drosophila-Arten der Schweiz. Rev. Suisse Zoo!' 58: BURLA, H., AND G. BXCHLI Beitrag zur Kenntnis der schweizerischen Dipteren, insbesondere Drosophila-Arten, die sich in Fruchtkorpern von Hutpilzen entwickeln. Vierteljahrschr. Naturf. Ges. Zurich 113: CHARLESWORTH, P., AND B. SHORROCKS Overwintering strategies of fungal feeding Drosophila. Abstr. 5th Drosophila Research Confer. Louvain-la-Neuve, Belgium. DANILEVSKU, A. S Photoperiodism and Seasonal Development of Insects. Oliver and Boyd, Edinburgh. DOBZHANSKY, TH., AND C. EPLING Contributions to the genetics, taxonomy, and ecology of Drosophila pseuiioobscura and its relatives. Carnegie Inst. Wash. Pub!. 554: GEYSPITS, K. F., F. D. SAPOZHNIKOVA, AND N. P. SIMONENKO Ecological principles of regulation of the active and diapausing stages seasonal turnover in arthropods, p In O. A. Scarlato, and V. A. Zaslavsky, (eds.), Photoperiodism in Animals and Plants. Zoological Institute Academy of Sciences USSR, Leningrad. (In Russian) GEYPITS, K. F., AND N.P. SIMONENKO An
10 GEOGRAPHICAL VARIATION IN DROSOPHILA 167 experimental analysis of seasonal changes in the photoperiodic reaction of Drosophila phalerata Meig. (Diptera, Drosophilidae). Entomo!. Rev. Wash. 49: HERTING, B Untersuchungen iiber die Okologie der wildlebenden Drosophila-Arten Westphalens. Zeitschr. Morph. Oko!. Tiere 44:1-42. Hoy, M. A Variability in diapause attributes of insects and mites: some evolutionaryand practical implications, p In H. Dingle (ed.), Evolution of Insect Migration and Diapause. Springer Verlag, N.Y. KIMURA, M. T., K. BEPPu, N. ICHIJO, AND M. TODA Bionomics of Drosophilidae (Diptera) in Hokkaido. II. Drosophila testacea. Kontyfi, Tokio 46: LUMME, J Phenology nad photoperiodic diapause in northern populations of Drosophila, p In H. Dingle (ed.), Evolution oflnsect Migration and Diapause. Springer Verlag, N.Y. LUMME, J, O. MUONA, AND M. ORELL Phenology of boreal drosophilids (Diptera). Ann. Entomo!. Fenn. 44: LUMME, J, AND A. OIKARINEN The genetic basis of the geographically variable photoperiodic diapause in Drosophila littoralis. Hereditas 86: MUONA, 0., P. SAMMALLAHTI, AND J MUONA Distribution of species of Drosophila (Diptera, Drosophilidae) on a small island in southern Finland. Notu!.Entomo!. 58: OIKARINEN, A., AND J LUMME Selection against photoperiodic reproductive diapause in Drosophila littoralis. Hereditas 90: POWELL, J. R., TH. DOBZHANSKY, J. E. HOOK, AND H. E. WISTRAND Genetics of natural populations. XLID. Further studies on rates of dispersal of Drosophila pseudoobscura and its relatives. Genetics 82: ROCHA PITE, T Rhythmes d'activite saisonniere des populations naturelles des Drosophilidae dans la region de Sintra-Colares (Portugal). Bull. Mus. Natn. Hist. Nat. Paris. Ecologie Generale 38: SAUNDERS, D. S Insect Clocks. Pergamon Press, Oxford. SHORROCKS, B An ecological classification of European Drosophila species. Oecologia 26: TODA, M. J, AND M. T. KIMURA Bionomics of Drosophilidae (Diptera) in Hokkaido. I. Scaptomyza pallida and Drosophila nipponica. Kontyfl, Tokio 46: WATABE, H Drosophila survey of Hokkaido, XXXIV. Seasonal variations of body color in Drosophila testacea. J Fac. Sci. Hokkaido Univ. Ser, VI, Zoo!' 21: Drosophila survey of Hokkaido, XXXVI. Seasonal changes in the reproductive condition of wild and domestic species of Drosophila. J Fac. Sci. Hokkaido Univ. Ser. VI, Zoo!' In press. WATABE, H., AND K. BEPPu Drosophila survey of Hokkaido, XXXIII. Ovarian development of Drosophila in relation to wild population. J Fac. Sci. Hokkaido Univ. Ser. VI, Zoo!' 20: Corresponding Editor: R. Milkman
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