Seasonal variation in wing size and shape of Drosophila melanogaster reveals rapid adaptation to environmental changes

Roff, D. Optimizing development time in a seasonal environment: the ‘ups and downs’ of clinal variation. Oecologia 45(2), 202–208 (1980).
Google Scholar
Mittelbach, G. G. et al. Evolution and the latitudinal diversity gradient: Speciation, extinction and biogeography. Ecol. Lett. 10(4), 315–331 (2007).
Google Scholar
Kapun, M., Fabian, D. K., Goudet, J. & Flatt, T. Genomic evidence for adaptive inversion clines in Drosophila melanogaster. Mol. Biol. Evol. 33(5), 1317–1336 (2016).
Google Scholar
Rajpurohit, S., Zhao, X. & Schmidt, P. S. A resource on latitudinal and altitudinal clines of ecologically relevant phenotypes of the Indian Drosophila. Sci. Data 4(1), 1–6 (2017).
Google Scholar
Hawkins, B. & DeVries, P. J. Altitudinal gradients in the body sizes of Costa Rican butterflies. Acta Oecol. 17, 185–194 (1996).
Sørensen, J. G., Norry, F. M., Scannapieco, A. C. & Loeschcke, V. Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatii from the New World. J. Evol. Biol. 18(4), 829–837 (2005).
Google Scholar
Pitchers, W., Pool, J. E. & Dworkin, I. Altitudinal clinal variation in wing size and shape in African Drosophila melanogaster: one cline or many?. Evolution 67(2), 438–452 (2013).
Google Scholar
Klepsatel, P., Gáliková, M., Huber, C. D. & Flatt, T. Similarities and differences in altitudinal versus latitudinal variation for morphological traits in Drosophila melanogaster. Evolution 68(5), 1385–1398 (2014).
Google Scholar
Ayhan, N., Güler, P. & Onder, B. S. Altitudinal variation in lifespan of Drosophila melanogaster populations from the Firtina Valley, northeastern Turkey. J. Therm. Biol. 61, 91–97 (2016).
Google Scholar
Dobzhansky, T. & Ayala, F. J. Temporal frequency changes of enzyme and chromosomal polymorphisms in natural populations of Drosophila. Proc. Natl. Acad. Sci. USA 70(3), 680–683 (1973).
Google Scholar
Williams, C. M. et al. Understanding evolutionary impacts of seasonality: An introduction to the symposium. Integr. Comp. Biol. 57(5), 921–933 (2017).
Google Scholar
Bergland, A. O., Behrman, E. L., O’Brien, K. R., Schmidt, P. S. & Petrov, D. A. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLoS Genet. 10(11), e1004775 (2014).
Google Scholar
Machado, H. E. et al. Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in Drosophila. Elife 10, e67577 (2021).
Google Scholar
Rodrigues, M. F., Vibranovski, M. D. & Cogni, R. Clinal and seasonal changes are correlated in Drosophila melanogaster natural populations. Evolution 75(8), 2042–2054 (2021).
Google Scholar
Hairston, N. G. & Dillon, T. A. Fluctuating selection and response in a population of freshwater copepods. Evolution 44(7), 1796–1805 (1990).
Google Scholar
Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296(5568), 707–711 (2002).
Google Scholar
Brown, C. R., Brown, M. B. & Roche, E. A. Fluctuating viability selection on morphology of cliff swallows is driven by climate. J. Evol. Biol. 26(5), 1129–1142 (2013).
Google Scholar
Bergland, A. O., Tobler, R., González, J., Schmidt, P. & Petrov, D. Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster. Mol. Ecol. 25(5), 1157–1174 (2016).
Google Scholar
Haldane, J. B. S. & Jayakar, S. D. Polymorphism due to selection of varying direction. J. Genet. 58(2), 237–242 (1963).
Google Scholar
Rhomberg, L. R. & Singh, R. S. Evidence for a link between local and seasonal cycles in gene frequencies and latitudinal gene clines in a cyclic parthenogen. Genetica 78(1), 73–79 (1986).
Google Scholar
Cogni, R. et al. The intensity of selection acting on the couch potato gene—spatial–temporal variation in a diapause cline. Evolution 68, 538–548 (2014).
Google Scholar
Behrman, E. L., Watson, S. S., O’brien, K. R., Heschel, M. S., & Schmidt, P. S. Seasonal variation in life history traits in two Drosophila species. J. Evol. Biol. 28(9), 1691–1704 (2015).
Cogni, R. et al. Variation in Drosophila melanogaster central metabolic genes appears driven by natural selection both within and between populations. Proc. Biol. Sci. 282, 20142688 (2015).
Google Scholar
Wittmann, M. J., Bergland, A. O., Feldman, M. W., Schmidt, P. S. & Petrov, D. A. Seasonally fluctuating selection can maintain polymorphism at many loci via segregation lift. Proc. Natl. Acad. Sci. USA 114(46), E9932–E9941 (2017).
Google Scholar
Behrman, E. L., et al. Rapid seasonal evolution in innate immunity of wild Drosophila melanogaster. P. Roy. Soc. B Biol. Sci. 285(1870), 20172599 (2018).
Rudman, S. M. et al. Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 116(40), 20025–20032 (2019).
Google Scholar
Dowle, E. J. et al. Genome-wide variation and transcriptional changes in diverse developmental processes underlie the rapid evolution of seasonal adaptation. Proc. Natl. Acad. Sci. USA 117(38), 23960–23969 (2020).
Google Scholar
Garcia‐Elfring, et al. Using seasonal genomic changes to understand historical adaptation to new environments: Parallel selection on stickleback in highly‐variable estuaries. Mol. Ecol. 30(9), 2054–2064 (2021).
Dobzhansky, T. Genetics of natural populations IX. Temporal changes in the composition of populations of Drosophila pseudoobscura. Genetics 28(2), 162 (1943).
Dubinin, N. P. & Tiniakov, G. G. Seasonal cycles and the concentration of inversions in populations of Drosophila funebris. Am. Nat. 79(785), 570–572 (1945).
Google Scholar
Stalker, H. D. & Carson, H. L. Seasonal variation in the morphology of Drosophila robusta Sturtevant. Evolution 3(4), 330–343 (1949).
Google Scholar
Stalker, H. D. Chromosome studies in wild populations of Drosophila melanogaster. II. Relationship of inversion frequencies to latitude, season, wing-loading and flight activity. Genetics 95(1), 211–223 (1980).
Rodriguez-Trelles, F., Alvarez, G. & Zapata, C. Time-series analysis of seasonal changes of the O inversion polymorphism of Drosophila subobscura. Genetics 142(1), 179–187 (1996).
Google Scholar
Ananina, G. et al. Chromosomal inversion polymorphism in Drosophila mediopunctata: seasonal, altitudinal, and latitudinal variation. Genet. Mol. Biol. 27, 61–69 (2004).
Google Scholar
Bergmann, K. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Größe. Gottinger Studien 3, 595–708 (1847).
Graves, G. R. Bergmann’s rule near the equator: latitudinal clines in body size of an Andean passerine bird. Proc. Natl. Acad. Sci. USA 88(6), 2322–2325 (1991).
Google Scholar
Partridge, L. & Coyne, J. A. Bergmann’s rule in ectotherms: Is it adaptive?. Evolution 51(2), 632–635 (1997).
Google Scholar
Ashton, K. G. Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Global Ecol. Biogeogr. 11(6), 505–523 (2002).
Google Scholar
Hallas, R., Schiffer, M. & Hoffmann, A. A. Clinal variation in Drosophila serrata for stress resistance and body size. Genet. Res. 79(2), 141–148 (2002).
Google Scholar
Stillwell, R. C., Morse, G. E. & Fox, C. W. Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle. Am. Nat. 170(3), 358–369 (2007).
Google Scholar
Clauss, M., Dittmann, M. T., Müller, D. W., Meloro, C. & Codron, D. Bergmann′ s rule in mammals: A cross-species interspecific pattern. Oikos 122(10), 1465–1472 (2013).
Stearns, S. C. The evolution of life histories (Oxford Univ. Press, 1992).
Blackburn, T. M. & Gaston, K. J. Linking patterns in macroecology. J. Anim. Ecol. 70(2), 338–352 (2001).
Robertson, F. W. The ecological genetics of growth in Drosophila 6. The genetic correlation between the duration of the larval period and body size in relation to larval diet. Genet. Res. 4(1), 74–92 (1963).
Partridge, L., Langelan, R., Fowler, K., Zwaan, B. & French, V. Correlated responses to selection on body size in Drosophila melanogaster. Genet. Res. 74(1), 43–54 (1999).
Google Scholar
Partridge, L. & Farquhar, M. Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Anim. Behav. 31(3), 871–877 (1983).
Google Scholar
Lefranc, A. & Bundgaard, J. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132(3), 243–247 (2000).
Google Scholar
Long, T. A., Pischedda, A., Stewart, A. D. & Rice, W. R. A cost of sexual attractiveness to high-fitness females. PLoS Biol. 7(12), e1000254 (2009).
Google Scholar
Partridge, L. & Fowler, K. Direct and correlated responses to selection on age at reproduction in Drosophila melanogaster. Evolution 46(1), 76–91 (1992).
Google Scholar
Rodriguez, C., Fanara, J. J. & Hasson, E. Inversion polymorphism, longevity, and body size in a natural population of Drosophila buzzatii. Evolution 53(2), 612–620 (1999).
Google Scholar
Norry, F. M. & Loeschcke, V. Temperature-induced shifts in associations of longevity with body size in Drosophila melanogaster. Evolution 56(2), 299–306 (2002).
Google Scholar
Karan, D., Dubey, S., Moreteau, B., Parkash, R. & David, J. R. Geographical clines for quantitative traits in natural populations of a tropical Drosophilid: Zaprionus indianus. Genetica 108(1), 91–100 (2000).
Google Scholar
Shelomi, M. Where are we now? Bergmann’s rule sensu lato in insects. Am. Nat. 180(4), 511–519 (2012).
Google Scholar
Blackburn, T. M., Gaston, K. J. & Loder, N. Geographic gradients in body size: a clarification of Bergmann’s rule. Divers. Distrib. 5(4), 165–174 (1999).
Google Scholar
Cavicchi, S., Guerra, D., Natali, V., Pezzoli, C., & Giorgi, G. Temperature‐related divergence in experimental populations of Drosophila melanogaster. II. Correlation between fitness and body dimensions. J. Evol. Biol. 2(4), 235–251 (1989).
Partridge, L., Barrie, B., Fowler, K. & French, V. Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48(4), 1269–1276 (1994).
Google Scholar
Jones, J. et al. Multiple selection pressures generate adherence to Bergmann’s rule in a Neotropical migratory songbird. J. Biogeogr. 32(10), 1827–1833 (2005).
Google Scholar
Stillwell, R. C., Moya-Laraño, J. & Fox, C. W. Selection does not favor larger body size at lower temperature in a seed-feeding beetle. Evolution 62(10), 2534–2544 (2008).
Google Scholar
Imasheva, A. G., Bubli, O. A. & Lazebny, O. E. Variation in wing length in Eurasian natural populations of Drosophila melanogaster. Heredity 72(5), 508–514 (1994).
Google Scholar
van’t Land, J., P. van Putten, H. Villarroel, A. Kamping & W. van Delden Latitudinal variation in wing length and allele frequencies for Adh and α-Gpdh in populations of Drosophila melanogaster from Ecuador and Chile. Dros. Info. Serv. 76, 156 (1995).
Loeschcke, V., Bundgaard, J., & Barker, J. S. F. Variation in body size and life history traits in Drosophila aldrichi and D. buzzatii from a latitudinal cline in eastern Australia. Heredity 85(5), 423–433 (2000).
Gilchrist, A. S. & Partridge, L. A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 153(4), 1775–1787 (1999).
Google Scholar
Turner, T. L., Stewart, A. D., Fields, A. T., Rice, W. R. & Tarone, A. M. Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genet. 7(3), e1001336 (2011).
Google Scholar
Pitchers, W. et al. A multivariate genome-wide association study of wing shape in Drosophila melanogaster. Genetics 211(4), 1429–1447 (2019).
Google Scholar
Reeve, E. C. R. Genetical aspects of size allometry. P. Roy. Soc. B-Biol. Sci. 137(889), 515–518 (1950).
Google Scholar
Cowley, D. E. & Atchley, W. R. Development and quantitative genetics of correlation structure among body parts of Drosophila melanogaster. Am. Nat. 135(2), 242–268 (1990).
Google Scholar
Reeve, E. C. R. & Robertson, F. W. Studies in quantitative inheritance. J. Genet. 51(2), 276–316 (1953).
Google Scholar
Menezes, B. F., Vigoder, F. M., Peixoto, A. A., Varaldi, J. & Bitner-Mathé, B. C. The influence of male wing shape on mating success in Drosophila melanogaster. Anim. Behav. 85(6), 1217–1223 (2013).
Google Scholar
Ray, R. P., Nakata, T., Henningsson, P. & Bomphrey, R. J. Enhanced flight performance by genetic manipulation of wing shape in Drosophila. Nat. Commun. 7(1), 1–8 (2016).
Falconer D.S., & Mackay T.F.C. Introduction to Quantitative Genetics. (4th ed Benjamin Cummings, Longmans Green: Harlow, UK. 1996).
Rohlf, F. J. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55(11), 2143–2160 (2001).
Google Scholar
Rohlf, F. J. The tps series of software. Hystrix 26(1), (2015).
Klingenberg, C. P. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11(2), 353–357 (2011).
Google Scholar
Patil, I. Visualizations with statistical details: The “ggstatsplot” approach. J. Open Source Softw. 6(61), 3167 (2021).
Google Scholar
R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria 2021).
Wood, S. N., Pya, N. & Säfken, B. Smoothing parameter and model selection for general smooth models. J. Am. Stat. Assoc. 111(516), 1548–1563 (2016).
Google Scholar
Pedersen, E. J., Miller, D. L., Simpson, G. L. & Ross, N. Hierarchical generalized additive models in ecology: An introduction with mgcv. PeerJ 7, e6876 (2019).
Google Scholar
Wood, S. N. Generalized additive models: an introduction with R 2nd edn. (Chapman and Hall/CRC, 2017).
Google Scholar
Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc. B 73(1), 3–36 (2011).
Google Scholar
Kapun, M. et al. Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses. Mol. Biol. Evol. 37(9), 2661–2678 (2020).
Google Scholar
David, J., Bocquet, C. & De Scheemaeker-Louis, M. Genetic latitudinal adaptation of Drosophila melanogaster: new discriminative biometrical traits between European and equatorial African populations. Genet. Res. 30(3), 247–255 (1977).
Google Scholar
Coyne, J. A. & Beecham, E. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117(4), 727–737 (1987).
Google Scholar
Capy, P., Pla, E., & David, J. R. Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans. I. Geographic variations. Genet. Sel. Evol. 25(6), 517–536 (1993).
James, A. C., Azevedo, R. B. & Partridge, L. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140(2), 659–666 (1995).
Google Scholar
Flatt, T. Life-history evolution and the genetics of fitness components in Drosophila melanogaster. Genetics 214(1), 3–48 (2020).
Google Scholar
Zhou, Y., Rodriguez, J., Fisher, N. & Catullo, R. A. Ecological drivers and sex-based variation in body size and shape in the Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae). Insects 11(6), 390 (2020).
Google Scholar
Gibb, H. et al. Habitat disturbance selects against both small and large species across varying climates. Ecography 41(7), 1184–1193 (2018).
Google Scholar
Kennington, W. J., Killeen, J. R., Goldstein, D. B. & Partridge, L. Rapid laboratory evolution of adult wing area in Drosophila melanogaster in response to humidity. Evolution 57(4), 932–936 (2003).
Google Scholar
Przybylska, M. S., Roque, F. & Tidon, R. Drosophilid species (Diptera) in the Brazilian Savanna are larger in the dry season. Ann. Entomol. Soc. Am. 107(5), 994–999 (2014).
Google Scholar
Chown, S. L. & Gaston, K. J. Exploring links between physiology and ecology at macro-scales: The role of respiratory metabolism in insects. Biol. Rev. 74(1), 87–120 (1999).
Google Scholar
Telonis-Scott, M., Guthridge, K. M. & Hoffmann, A. A. A new set of laboratory-selected Drosophila melanogaster lines for the analysis of desiccation resistance: response to selection, physiology and correlated responses. J. Exp. Biol. 209(10), 1837–1847 (2006).
Google Scholar
Gómez, G. F., Márquez, E. J., Gutiérrez, L. A., Conn, J. E. & Correa, M. M. Geometric morphometric analysis of Colombian Anopheles albimanus (Diptera: Culicidae) reveals significant effect of environmental factors on wing traits and presence of a metapopulation. Acta Trop. 135, 75–85 (2014).
Google Scholar
Service & P. M., Hutchinson, E. W., MacKinley, M. D., & Rose, M. R,. Resistance to environmental stress in Drosophila melanogaster selected for postponed senescence. Physiol. Zool. 58(4), 380–389 (1985).
Google Scholar
Al-Saffar, Z. Y., Grainger, J. N. R. & Aldrich, J. Temperature and humidity affecting development, survival and weight loss of the pupal stage of Drosophila melanogaster, and the influence of alternating temperature on the larvae. J. Therm. Biol. 21(5–6), 389–396 (1996).
Google Scholar
Aggarwal, D. D. et al. Rapid effects of humidity acclimation on stress resistance in Drosophila melanogaster. Comp. Biochem. Phys. A 166(1), 81–90 (2013).
Google Scholar
Bogaerts-Márquez, M., Guirao-Rico, S., Gautier, M. & González, J. Temperature, rainfall and wind variables underlie environmental adaptation in natural populations of Drosophila melanogaster. Mol. Ecol. 30(4), 938–954 (2021).
Google Scholar
Carreira, V. P., Mensch, J. & Fanara, J. J. Body size in Drosophila: genetic architecture, allometries and sexual dimorphism. Heredity 102(3), 246–256 (2009).
Google Scholar
Carreira, V. P., Soto, I. M., Mensch, J. & Fanara, J. J. Genetic basis of wing morphogenesis in Drosophila: Sexual dimorphism and non-allometric effects of shape variation. BMC Dev. Biol. 11(1), 1–16 (2011).
Google Scholar
Parker, G. A. et al. Genetic basis of increased lifespan and postponed senescence in Drosophila melanogaster. G3 – Genes Genom. Genet. 10(3), 1087–1098 (2020).
Archer, C. R. et al. Sex-specific effects of natural and sexual selection on the evolution of life span and ageing in Drosophila simulans. Funct. Ecol. 29(4), 562–569 (2015).
Google Scholar