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Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species


Temperature profoundly impacts the rate of development of “cold-blooded” animals, which proceeds far faster when it is warm. There is, however, no universal relationship. Closely related species can develop at markedly different speeds at the same temperature. This creates a major challenge when comparing development among species, as it is unclear whether they should be compared at the same temperature or under different conditions to maintain the same developmental rate. Facing this challenge while working with flies (Drosophila species), we found there was little data to inform this decision. So, using time-lapse imaging, precise temperature-control, and computational and manual video-analysis, we tracked the complex process of embryogenesis in 11 species at seven different temperatures. There was over a three-fold difference in developmental rate between the fastest species at its fastest temperature and the slowest species at its slowest temperature. However, our finding that the timing of events within development all scaled uniformly across species and temperatures astonished us. This is good news for developmental biologists, since we can induce species to develop nearly identically by growing them at different temperatures. But it also means flies must possess some unknown clock-like molecular mechanism driving embryogenesis forward.


Vyšlo v časopise: Embryogenesis Scales Uniformly across Temperature in Developmentally Diverse Species. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004293
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004293

Souhrn

Temperature profoundly impacts the rate of development of “cold-blooded” animals, which proceeds far faster when it is warm. There is, however, no universal relationship. Closely related species can develop at markedly different speeds at the same temperature. This creates a major challenge when comparing development among species, as it is unclear whether they should be compared at the same temperature or under different conditions to maintain the same developmental rate. Facing this challenge while working with flies (Drosophila species), we found there was little data to inform this decision. So, using time-lapse imaging, precise temperature-control, and computational and manual video-analysis, we tracked the complex process of embryogenesis in 11 species at seven different temperatures. There was over a three-fold difference in developmental rate between the fastest species at its fastest temperature and the slowest species at its slowest temperature. However, our finding that the timing of events within development all scaled uniformly across species and temperatures astonished us. This is good news for developmental biologists, since we can induce species to develop nearly identically by growing them at different temperatures. But it also means flies must possess some unknown clock-like molecular mechanism driving embryogenesis forward.


Zdroje

1. PowsnerL (1935) The effects of temperature on the durations of the developmental stages of drosophila melanogaster. Physiological Zoology 8: 474–520.

2. JamesAC, AzevedoRB, PartridgeL (1995) Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140: 659–666.

3. JamesAC, AzevedoRB, PartridgeL (1997) Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. Genetics 146: 881–890.

4. YamamotoA, OhbaS (1982) Strategic differences in thermal adaptation between two drosophila species, d. virilis and d. immigrans. Oecologia 52: 333–339.

5. LillieFR, KnowltonFP (1897) On the effect of temperature on the development of animals. Zoological Bulletin 1: 179–193.

6. LoebJ, NorthropJH (1916) Is there a temperature coefficient for the duration of life? PNAS 2: 456–7.

7. PartridgeL, BarrieB, FowlerK, FrenchV (1994) Evolution and development of body and cell size in drosophila melanogaster in response to temperature. Evolution 48: 1269–1276.

8. KimJ, KerrJQ, MinGS (2000) Molecular heterochrony in the early development of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 97: 212–216.

9. TantawyAO (1963) Effects of temperature and x-ray irradiation on intrinsic growth rate in populations of drosophila pseudoobscura. Genetica 34: 34–45.

10. StratamanR, MarkowTA (1998) Resistance to thermal stress in desert drosophila. Functional Ecology 12: 965–970.

11. MorinJ, MoreteauB, PétavyG, ParkashR, DavidJ (1997) Reaction norms of morphometrical traits in drosophila: adaptive shape changes in a stenotherm circumtropical species. Evolution 51: 1140–1148.

12. Montchamp-MoreauC (1983) Interspecific competition between drosophila melanogaster and drosophila simulans: temperature effect on competitive ability and fitness components. Genet Sel Evol 15: 367–78.

13. HoffmannAA, HallasR, SinclairC, MitrovskiP (2001) Levels of variation in stress resistance in drosophila among strains, local populations, and geographic regions: patterns for desiccation, starvation, cold resistance, and associated traits. Evolution; international journal of organic evolution 55: 1621–1630.

14. HoffmannAA, WeeksAR (2007) Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129: 133–147.

15. RakoL, BlacketMJ, MckechnieSW, HoffmannAA (2007) Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Molecular Ecology 16: 2948–2957.

16. GibertP, De JongG (2001) Temperature dependence of development rate and adult size in drosophila species: biophysical parameters. Journal of Evolutionary Biology 14: 267–276.

17. Markow TA, O'Grady PM (2005) Drosophila: A Guide to Species Identification and Use. Academic Press.

18. MarkowTA, BeallS, MatzkinLM (2009) Egg size, embryonic development time and ovoviviparity in drosophila species. Journal of Evolutionary Biology 22: 430–434.

19. Campos-Ortega J, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Berlin, New York: Springer-Verlag.

20. Foe VE, Odell GM, Edgar BA (1993), chapter 3: Mitosis and Morphogenesis in the Drosophila Embryo. In: The Development of Drosophila melanogaster. Cold Spring Harbor Press. Chapter 3: pp. 149–300.

21. Drosophila 12 Genomes Consortium (2007) ClarkA, EisenM, SmithD, BergmanC, et al. (2007) Evolution of genes and genomes on the drosophila phylogeny. Nature 450: 203–218.

22. FoeVE, AlbertsBM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. Journal of Cell Science 61: 31–70.

23. KamZ, MindenJS, AgardDA, SedatJW, LeptinM (1991) Drosophila gastrulation: analysis of cell shape changes in living embryos by three-dimensional fluorescence microscopy. Development (Cambridge, England) 112: 365–370.

24. Arrhenius S (1915) Quantitative laws in biological chemistry. G. Bell and sons, ltd.

25. MackayTFC, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178.

26. FabianD, KapunM, NolteV, KoflerR, SchmidtP, et al. (2012) Genome-wide patterns of latitudinal differentiation among populations of drosophila melanogaster from north america. Molecular Ecology 21: 4748–4769.

27. KimmelCB, BallardWW, KimmelSR, UllmannB, SchillingTF (1995) Stages of embryonic development of the zebrafish. Developmental Dynamics 203: 253–310.

28. Riddiford LM (1993) Hormones and drosophila development. In: Bate M, Martinez Arias A, editors. The Development of Drosophila melanogaster volume II. Cold Spring Harbor Press. pp. 899–939.

29. ChávezVM, MarquésG, DelbecqueJP, KobayashiK, HollingsworthM, et al. (2000) The drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome p450 enzyme that regulates embryonic ecdysone levels. Development 127: 4115–4126.

30. LucchettaEM, LeeJH, FuLA, PatelNH, IsmagilovRF (2005) Dynamics of Drosophila embryonic patterning network perturbed in space and time using microfluidics. Nature 434: 1134–1138.

31. NiemuthJ, WolfR (1995) Developmental asynchrony caused by steep temperature gradients does not impair pattern formation in the wasp, pimpla turionellae l. Roux's Arch Dev Biol 204: 444–452.

32. GirdlerGC, ArayaC, RenX, ClarkeJDW (2013) Developmental time rather than local environment regulates the schedule of epithelial polarization in the zebrafish neural rod. Neural Development 8: 5.

33. DavidsonJ (1944) On the relationship between temperature and rate of development of insects at constant temperatures. Journal of Animal Ecology 13: 26–38.

34. GilloolyJF, BrownJH, WestGB, SavageVM, CharnovEL (2001) Effects of size and temperature on metabolic rate. Science 293: 2248–2251.

35. GilloolyJF, CharnovEL, WestGB, SavageVM, HBJ (2002) Effects of size and temperature on developmental time. Nature 417: 70–73.

36. ClarkeA (2004) Is there a universal temperature dependence of metabolism? Functional Ecology 18: 252–256.

37. ClarkeA, FraserKPP (2004) Why does metabolism scale with temperature? Functional Ecology 18: 243–251.

38. McNamaraKJ (1982) Heterochrony and phylogenetic trends. Paleobiology 8: 130–142.

39. JonesDS, GouldSJ (1999) Direct measurement of age in fossil gryphaea: the solution to a classic problem in heterochrony. Paleobiology 25: 158–187.

40. FélixMA, HillRJ, SchwarzH, SternbergPW, SudhausW, et al. (1999) Pristionchus pacificus, a nematode with only three juvenile stages, displays major heterochronic changes relative to caenorhabditis elegans. Proceedings Biological sciences/The Royal Society 266: 1617–1621.

41. PatelNH, CondronBG, ZinnK (1994) Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367: 429–434.

42. KellerA (2007) Drosophila melanogaster's history as a human commensal. Current Biology 17: R77–R81.

43. TechnauGM (1986) Lineage analysis of transplanted individual cell in embryos of drosophila melanogaster. i. the method. Roux's Arch Dev Biol 195: 389–398.

44. SantosA, Ortiz de SolórzanoC, VaqueroJJ, PeñaJM, MalpicaN, et al. (1997) Evaluation of autofocus functions in molecular cytogenetic analysis. Journal of microscopy 188: 264–72.

45. VollathD (1988) The influence of the scene parameters and of noise on the behaviour of automatic focusing algorithms. Journal of microscopy 151: 133–146.

46. BownesM (1975) A photographic study of development in the living embryo. J Embryol exp Morph 33: 789–801.

47. LachaiseD, SilvainJF (2004) How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120: 17–39.

48. Patterson JT, Stone WS (1952) Evolution in the genus Drosophila. New York: Macmillan, 1 edition.

49. GranzottoA, LopesF, LeratE, VieiraC, CararetoC (2009) The evolutionary dynamics of helena retrotransposon revealed by sequenced drosophila genomes. BMC Evolutionary Biology 9: 174.

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