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Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions

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Abstract

The relation between thermal tolerance and latitudinal distribution was studied with 30 drosophilid species collected from the cool-temperate region (Sapporo), the warm-temperate region (Tokyo and Kyoto) and the subtropical region (Iriomote island) in Japan. In addition, intraspecific variation was examined for five species collected from two localities. The subtropical strains of Scaptodrosophila coracina, Drosophila bizonata and D. daruma were less tolerant to cold than their temperate strains. However, the difference of cold tolerance between these two geographic strains was much smaller than the difference between the species restricted to the subtropical region and those occurring in the temperate region. In D. auraria and D. suzukii, no difference was observed in thermal tolerance between their cool- and warm-temperate strains. Thus, geographic variation in thermal tolerance within species was low or negligible. Interspecific comparisons by phylogenetic independent contrasts revealed that species which had the northern boundaries of their distributions at higher latitudes were generally more tolerant to cold than those which had their boundaries at lower latitudes. However, the data for some species did not agree with this trend. The use of man-protected warm places for overwintering, competition or predation would also affect their distributions. It also appeared that species which had their southern boundaries at higher latitudes were generally more cold-tolerant. The acquisition of cold tolerance may lower a fly’s capacity to compete, survive or reproduce in warmer climates. On the other hand, no relation was observed between heat tolerance and latitudinal distribution. Heat tolerance was higher in species inhabiting openlands or the forest canopy than in those inhabiting the forest understorey.

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References

  • Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc Roy Soc Lond B 267:739–745

    Article  CAS  Google Scholar 

  • Beppu K (1976) Drosophila survey of Hokkaido. XXXI. Microdistribution of drosophilid flies in the vicinity of the stream. J Fac Sci Hokkaido Univ VI (Zool) 20:203–210

    Google Scholar 

  • Beppu K (1979) Habitat segregation of the drosophilid flies in the vicinity of streams. Kontyû 47:443–445

  • Beppu K (1980) Drosophilid fauna at the lower reaches of a river (in Japanese with English summary). Kontyû 48:435–443

  • Beppu K (2000) Faunal and ecological surveys on drosophilid flies in the Imperial Palace, Tokyo. Mem Nat Sci Mus 36:409–435

    Google Scholar 

  • Berrigan D, Hoffmann AA (1998) Correlations between measures of heat resistance and acclimation in two species of Drosophila and their hybrids. Biol J Linn Soc 64:449–462

    Article  Google Scholar 

  • Brattstrom BH (1968) Thermal acclimation in anuran amphibians as a function of latitude and altitude. Comp Biochem Physiol 24:93–111

    Article  CAS  PubMed  Google Scholar 

  • Case TJ, Tarper ML (2000) Interspecific competition, environmental gradients, gene flow, and the coevolution of species’ borders. Am Nat 155:583–605

    Article  PubMed  Google Scholar 

  • Coyne JA, Bundgaard J, Prout T (1983) Geographic variation of tolerance to environmental stress in Drosophila pseudoobscura. Am Nat 122:474–488

    Article  Google Scholar 

  • Danilevskii AS (1965) Photoperiodism and seasonal development of insects. Oliver and Boyd, London

  • David JR, Gilbert P, Moreteau B, Cilchrist GW, Huey RB (2003) The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Funct Ecol 17:425–430

    Article  Google Scholar 

  • Eger JE Jr, Wits JA, Hartstack AW Jr, Stering WL (1982) Survival of pupae of Heliothis virescens and H. zea (Lepidoptera: Noctuidae) at low temperatures. Can Entomol 114:289–301

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Gaston KJ (2003) The structure and dynamics of geographic ranges. Oxford University Press, New York

  • Goto SG, Kimura MT (2001) Phylogenetic utility of mitochondrial COI and nuclear Gpdh genes in Drosophila. Mol Phylogenet Evol 18:404–422

    Article  CAS  PubMed  Google Scholar 

  • Goto SG, Yoshida KM, Kimura MT (1998) Accumulation of Hsp70 mRNA under environmental stresses in diapausing and nondiapausing adults of Drosophila triauraria. J Insect Physiol 44:1009–1015

    Article  CAS  PubMed  Google Scholar 

  • Goto SG, Yoshida T, Beppu K, Kimura MT (1999) Evolution of overwintering strategies in Eurasian species of the Drosophila obscura species group. Biol J Linn Soc 68:429–441

    Article  Google Scholar 

  • Harvey PH, Pagel M (1991) The comparative method in evolutional biology. Oxford University Press, Oxford

  • Hirai Y, Goto SG, Yoshida T, Kimura MT (2000) Faunal and ecological surveys on drosophilid flies in Iriomote-jima, a subtropical island of Japan. Entomol Sci 3:273–284

    Google Scholar 

  • Hoffmann AA, Blows MW (1994) Species borders: ecological and evolutionary perspectives. Trends Ecol Evol 9:223–227

    Article  Google Scholar 

  • Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford University Press, New York

  • Hoffmann AA, Parsons PA (1997) Extreme environmental change and evolution. Cambridge University Press, Cambridge

  • Hoffmann AA, Sorensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approach. J Theor Biol 28:175–216

    Article  Google Scholar 

  • Hori Y, Kimura MT (1998) Relationship between cold stupor and cold tolerance in Drosophila (Diptera: Drosophilidae). Environ Entomol 27:1297–1302

    Google Scholar 

  • Kaneko A, Tokumitsu T (1963) Seasonal fluctuations of Drosophila populations in two adjacent localities of Japan (in Japanese with English summary). Zool Mag 72: 123–127

    Google Scholar 

  • Kastanis P, Eliopoulos E, Goulielmos GN, Tsakas S, Loukas M (2003) Macroevolutionary relationships of species of Drosophila melanogaster group based on mt DNA sequences. Mol Phylogenet Evol 28:518–528

    Article  CAS  PubMed  Google Scholar 

  • Katoh T, Tamura K, Aotsuka T (2000) Phylogenetic position of the subgenus Lordiphosa of the genus Drosophila (Diptera: Drosophilidae) inferred from alcohol dehydrogenase (Adh) gene sequences. J Mol Evol 51:122–130

    CAS  PubMed  Google Scholar 

  • Kimura MT (1976a) Drosophila survey of Hokkaido, XXX. Microdistribution and seasonal fluctuation of drosophilid flies dwelling among the undergrowth plants. J Fac Sci Hokkaido Univ VI (Zool) 20:192–202

    Google Scholar 

  • Kimura MT (1976b) Drosophila survey of Hokkaido, XXXII. A field survey of fungus preferences of drosophilid flies in Sapporo. J Fac Sci Hokkaido Univ VI (Zool) 20:288–298

    Google Scholar 

  • Kimura MT (1982) Cold-hardiness and preimaginal period in two closely related species, Drosophila takahashii and D. lutescens. Kontyû 50:638–648

  • Kimura MT (1984) Geographic variation of reproductive diapause in the Drosophila auraria complex (Diptera: Drosophilidae). Physiol Entomol 9:425–431

    Google Scholar 

  • Kimura MT (1987) Habitat differentiation and speciation in the Drosophila auraria species-complex (Diptera; Drosophilidae). Kontyû 55:429–436

  • Kimura MT (1988) Adaptations to temperate climates and evolution of over-wintering strategies in the Drosophila melanogaster species group. Evolution 42:1288–1297

    Google Scholar 

  • Kimura MT (2001) Evolutionary aspects of photoperiodism in Drosophila. In: Denlinger DL, Giebltowicz JM, Saunders DS (eds) Insect timing: circadian rhythmicity to seasonality. Elsevier, Amsterdam, pp 123–132

  • Kimura MT, Beppu K (1993) Climatic adaptations in the Drosophila immigrans species group: seasonal migration and thermal tolerance. Ecol Entomol 18:141–149

    Google Scholar 

  • Kimura MT, Toda MJ (1989) Food preferences and nematode parasitism in mycophagous Drosophila. Ecol Res 4:209–218

    Google Scholar 

  • Kimura MT, Ohtsu T, Yoshida T, Awasaki T, Lin FJ (1994) Climatic adaptations and distributions in the Drosophila takahashii species-subgroup (Diptera: Drosophilidae). J Nat Hist 28:401–409

    Google Scholar 

  • Kopp A, True JR (2002) Phylogeny of the oriental Drosophila melanogaster species group: a multilocus reconstruction. Syst Biol 51:786–805

    Article  PubMed  Google Scholar 

  • Loik ME, Nobel PS (1993) Freezing tolerance and water relations of Opuntia fragilis from Canada and the United States. Ecology 74:1722–1732

    Google Scholar 

  • MacArthur RH (1972) Geographical ecology: patterns in the distribution of species. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Mitsui H, Kimura MT (2000a) Food preference of drosophilid flies in domestic and forest areas of central Japan. Entomol Sci 3:285–289

    Google Scholar 

  • Mitsui H, Kimura MT (2000b) Coexistence of drosophilid flies: aggregation, patch size diversity and parasitism. Ecol Res 15:95–100

    Article  Google Scholar 

  • Momma E (1954) Drosophila survey of Hokkaido, V. Distribution and habitats of drosophilid flies. J Fac Sci Hokkaido Univ VI (Zool) 13:93–98

    Google Scholar 

  • Momma E (1965) The dynamic aspects of Drosophila populations in semi-natural areas. 1. Associations and relative numbers of species. Part 1. Results of trapping. Jpn J Genet 40:275–295

    Google Scholar 

  • Nishiharu S (1980) A study of ecology and evolution of drosophilid flies with special regard to imaginal and larval feeding habits and seasonal population fluctuations. DSci thesis. Tokyo Metropolitan University, Tokyo

  • Ohtsu T, Kimura MT, Hori SH (1992) Energy storage during reproductive diapause in the Drosophila melanogaster species group. J Comp Physiol B 162:203–208

    CAS  PubMed  Google Scholar 

  • Ohtsu T, Katagiri C, Kimura MT, Hori SH (1993) Cold adaptations in Drosophila: qualitative changes of triacylglycerols with relation to overwintering. J Biol Chem 268:1830–1834

    CAS  PubMed  Google Scholar 

  • Ohtsu T, Kimura MT, Hori SH (1995) The influence of eclosion timing on winter survival and triacylglycerol accumulation in four temperate species of Drosophila. Physiol Entomol 20:248–252

    CAS  Google Scholar 

  • Ohtsu T, Kimura MT, Katagiri C (1998) How Drosophila species acquire cold tolerance qualitative changes of phospholipids. Eur J Biochem 252:608–611

    Article  CAS  PubMed  Google Scholar 

  • Ohtsu T, Katagiri C, Kimura MT (1999) Biochemical aspects of climatic adaptations in Drosophila curviceps, D. immigrans, and D. albomicans (Diptera: Drosophilidae). Environ Entomol 28:968–972

    CAS  Google Scholar 

  • Okada T (1956) Systematic study of Drosophilidae and allied families of Japan. Gihodo, Tokyo

  • Pélandakis M, Solignac M (1993) Molecular phylogeny of Drosophila based on ribosomal RNA sequences. J Mol Ecol 37:525–543

    Google Scholar 

  • Perlman SJ, Spicer GS, Shoemaker D, Jaenike J (2003) Associations between mycophagous Drosophila and their Hawardula nematode parasites: a worldwide phylogenetic shuffle. Mol Ecol 12:237–249

    Article  CAS  PubMed  Google Scholar 

  • Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analyzing comparative data. Comput Appl Biosci 11:247–251 (available at http://www.bio.ic.ac.uk/evolve/software/caic/)

  • Sakai A (1975) Freezing resistance of evergreen and deciduous broad-leaf trees in Japan with special reference to their distributions (in Japanese with English summary). Jpn J Ecol 25: 101–111

    Google Scholar 

  • Sakai A, Weiser CJ (1973) Freezing resistance of trees in northern America with reference to tree regions. Ecology 54:118–126

    Google Scholar 

  • Schawaroch V (2002) Phylogeny of a paradigm lineage: the Drosophila melanogaster species group (Diptera: Drosophilidae) Biol J Linn Soc 76:21–37

  • Toda MJ (1973) Seasonal activity and microdistribution of drosophilid flies in Misumai in Sapporo. J Fac Sci Hokkaido Univ VI (Zool) 18:532–550

    Google Scholar 

  • Toda MJ, Kimura MT, Enomoto O (1984) Bionomics of Drosophilidae (Diptera) in Hokkaido, VI. decayed herbage feeders, with special reference to their reproductive strategies. Jpn J Ecol 34:253–270

    Google Scholar 

  • Tucic N (1979) Genetic capacity for adaptation to cold resistance at different developmental stages of Drosophila melanogaster. Evolution 33:350-358

    Google Scholar 

  • Wakahama K (1957) Further notes on the seasonal activity of Drosophila observed in the University Botanical Garden, Sapporo. Annot Zool Jpn 30:217–224

    Google Scholar 

  • Watabe H, Momma E, Kimura MT (1980) Changes in drosophilid fauna at the University Botanical Garden in Sapporo, Japan. Drosophila Inform Ser 55:141–142

    Google Scholar 

  • Yamamoto AH (1992) Niche differentiation of drosophilids in Oiso, Japan. Memor Konan Univ Sci Ser 39:287–299

    Google Scholar 

  • Yang Y, Zhang Y, Qian Y, Zeng Q (2004) Phylogenetic relationships of Drosophila melanogaster species group deduced from spacer regions of histone gene H2A-H2B. Mol Phylogenet Evol 30:336–343

    Article  CAS  PubMed  Google Scholar 

  • Young I, Coleman AW (2004) The advantages of the ITS2 region of the nuclear rDNA cistron for analysis of phylogenetic relationships of insects: a Drosophila example. Mol Phylogenet Evol 30:236–242

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I thank Dr T. Aotsuka for providing unpublished data, and H. Chen, H. Mitsui, H. Abe, K. Ishii, S. Daibo, K. Takahashi, A. Shiota and T. Nakamura for their help in collections of flies. This work was supported by a Grant-in-Aid from Ministry of Education, Science, Sports and Culture of Japan (nos. 14540571 and 15255006).

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Correspondence to Masahito T. Kimura.

Appendix

Appendix

Lethal temperatures (LT25, LT50, LT75) at cold and heat in the experimental species (Scaptodrosophila, Drosophila,Hirtodrosophila ). F Female, M male

 

 

Cold

Heat

LT25

LT50

LT75

LT25

LT50

LT75

Species originated from Sapporo

 S. coracina

F

−4.1

−5.2

−5.6

34.1

34.4

34.7

M

−5.1

−5.4

−5.7

34.1

34.4

34.7

 S. pallida

F

−5.7

−6.3

−6.6

33.4

33.9

34.5

M

−5.1

−5.6

−6.2

33.1

33.7

34.3

 H. histrioides

F

−3.3

−3.5

−3.8

32.0

32.3

32.7

M

−3.3

−3.5

−3.8

32.1

32.4

32.7

 D. auraria

F

−1.9

−3.3

−3.6

33.3

33.9

34.4

M

−2.6

−3.3

−3.6

33.3

33.6

34.0

 D. biauraria

F

−1.5

−2.7

−3.4

32.3

32.5

32.8

M

−1.3

−2.1

−2.5

32.3

32.5

32.8

 D. suzukii

F

−1.1

−1.6

−1.8

32.3

32.6

32.9

M

0.5

−0.1

−0.7

31.6

32.2

32.6

 D. nigromaculata

F

−4.2

−4.5

−4.7

33.8

34.3

34.6

M

−3.3

−4.3

−4.6

33.4

33.8

34.3

 D. brachynephros

F

−3.3

−3.7

−4.2

33.3

33.6

33.9

M

−3.3

−3.7

−4.2

33.3

33.5

33.8

 D. curvispina

F

−4.3

−4.5

−4.8

32.3

32.6

32.9

M

−4.1

−4.4

−4.7

32.3

32.5

32.8

 D. unispina

F

−3.3

−3.5

−3.8

31.9

32.3

32.7

M

−3.3

−3.5

−3.8

31.5

31.9

32.5

 D. orientacea

F

−4.0

−4.5

−4.9

31.4

31.9

32.4

M

−4.1

−4.4

−4.8

31.3

31.6

31.9

 D. lacertosa

F

1.6

0.7

−2.0

30.4

31.0

31.5

M

0.3

−1.2

−1.9

30.4

31.0

31.5

 D. kanekoi

F

−5.3

−5.5

−5.8

35.1

35.4

35.7

M

−5.3

−5.5

−5.8

35.0

35.4

35.7

Species originated from Tokyo (D. daruma from Kyoto)

 D. auraria

F

−1.7

−3.2

−3.6

33.1

33.4

33.8

M

−3.1

−3.4

−3.7

33.3

33.6

33.9

 D. suzukii

F

−0.5

−1.2

−1.6

32.4

32.7

33.3

M

0.3

−0.3

−0.7

31.8

32.3

32.6

 D. lutescens

F

1.7

0.5

−1.4

30.5

31.1

31.6

M

1.6

1.1

−1.3

30.4

31.2

31.6

 D. rufa

F

2.0

0.6

0.1

32.3

32.9

33.3

M

2.3

−0.8

−1.3

32.0

32.6

33.3

 D. bizonata

F

−1.6

−2.7

−3.5

32.4

32.9

33.4

M

−1.4

−2.3

−2.8

32.3

32.8

33.3

 D. angularis

F

−1.4

−2.1

−2.6

34.1

34.4

34.7

M

−1.4

−1.9

−2.5

34.1

34.4

34.7

 D. sternopleuralis

F

2.3

1.7

−0.3

31.1

31.4

31.7

M

3.7

3.2

2.5

31.2

31.5

31.8

 D. daruma

F

0.4

−0.2

−0.6

33.0

33.4

33.7

M

1.5

0.8

0.2

31.4

32.5

33.4

Species orginated from Iriomote island

 S. coracina

F

−1.3

−2.4

−3.3

34.3

34.5

34.8

M

−3.2

−3.5

−3.7

34.3

34.5

34.8

 S. dorsocentralis

F

8.6

8.3

7.8

33.6

34.2

34.6

M

8.6

8.2

6.7

33.4

33.7

34.1

 S. bryani

F

5.9

4.2

3.5

35.3

35.5

35.8

M

6.5

4.0

3.2

35.3

35.5

35.8

 D. lacteicornis

F

2.9

1.7

0.7

32.2

32.5

32.7

M

3.5

1.8

0.5

31.7

32.2

32.6

 D. bocki

F

7.5

6.8

5.0

32.7

33.2

33.6

M

6.8

6.2

5.5

32.7

33.2

33.6

 D. ficusphila

F

2.4

1.7

1.3

33.2

33.5

33.8

M

3.8

3.0

2.0

33.2

33.4

33.7

 D. takahashii

F

5.2

4.5

3.9

32.3

32.5

32.8

M

5.3

4.6

3.7

32.3

32.5

32.8

 D. elegans

F

3.9

3.6

3.3

33.3

33.6

33.9

M

4.7

4.2

3.6

33.4

33.8

34.3

 D. bipectinata

F

8.5

7.1

5.7

33.2

33.5

33.7

M

8.7

8.3

7.4

32.5

33.1

33.5

 D. albomicans

F

5.8

5.3

4.2

32.1

32.5

32.8

M

6.5

5.4

3.7

32.1

32.4

32.7

 D. ruberrima

F

3.1

2.5

2.0

31.5

32.1

32.5

M

4.3

2.6

2.1

31.4

31.8

32.3

 D. quadrilineata

F

7.6

6.8

6.3

33.4

33.9

34.4

M

8.7

7.9

7.2

33.3

33.6

34.0

 D. daruma

F

1.8

1.5

1.2

32.3

32.8

33.4

M

4.6

2.4

1.6

32.2

32.6

33.0

 D. bizonata

F

−0.9

−1.5

−2.1

31.2

31.5

31.8

M

−0.3

−0.9

−1.5

31.1

31.5

31.9

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Kimura, M.T. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140, 442–449 (2004). https://doi.org/10.1007/s00442-004-1605-4

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