Abstract
Great efforts have been sustained to explain the relationships between genotype and phenotype for developmental fitness traits through the study of their genetic architecture. However, crucial aspects of functional architecture influencing the maintenance of genetic variability, and thus the capacity for evolutionary change, are still unexplored. Here we performed Genome-wide Association Studies for phenotypic variability, plasticity and within-line canalization at two temperatures for Larval Developmental Time (LDT), Pupal Developmental Time (PDT), Larval Viability (LV), Pupal Viability (PV), and Pupal Height (PH) in lines derived from a natural population of Drosophila melanogaster. Results suggest changes in genetic networks linked to resource acquisition and allocation underlying variability for all traits. However, we found low genetic pleiotropy between traits and for different aspects of phenotype (means, plasticity, within-line canalization) within each trait. Their genetic bases were also temperature-specific: we found no variants showing an effect for the same trait at both temperatures. Moreover, a genetic decoupling between larval and pupal traits was confirmed, as there were no candidate variants significantly associated to phenotypic variability for the same trait across stages. We found evidence of genetic antagonistic pleiotropy for several loci affecting larval and pupal traits. The high degree of modularity at various levels would allow for the independent evolution of distinct aspects of the phenotype in different environments and ontogenetic stages. This may explain why genetic variation for these adaptive traits is not extinguished in natural populations and may entail important implications regarding evolvability.
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References
Angilletta, M. J., Jr., Steury, T. D., & Sears, M. W. (2004). Temperature, growth rate, and body size in ectotherms: Fitting pieces of a life-history puzzle. Integrative and Comparative Biology, 44(6), 498–509. https://doi.org/10.1093/icb/44.6.498
Arbeitman, M. N., Furlong, E. E., Imam, F., Johnson, E., Null, B. H., Baker, B. S., & White, K. P. (2002). Gene expression during the life cycle of Drosophila melanogaster. Science, 297(5590), 2270–2275. https://doi.org/10.1126/science.1072152
Ayrinhac, A., Debat, V., Gibert, P., Kister, A. G., Legout, H., Moreteau, B., & David, J. R. (2004). Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Functional Ecology, 18, 700–706.
Barker, J. S. F., & Podger, R. N. (1970). Interspecific competition between Drosophila melanogaster and Drosophila simulans: Effects of larval density on viability, developmental period and adult body weight. Ecology, 51(2), 170–189. https://doi.org/10.2307/1933654
Barrett, R. D., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23(1), 38–44. https://doi.org/10.1016/j.tree.2007.09.008
Bull, J. J. (1987). Evolution of phenotypic variance. Evolution, 41(2), 303–315. https://doi.org/10.1111/j.1558-5646.1987.tb05799.x
Callahan, H. S. (2005). (2005) Using artificial selection to understand plastic plant phenotypes. Integrative and Comparative Biology., 45, 475–485.
Casares, P., & Carracedo, M. C. (1987). Pupation height in Drosophila: Sex differences and influence of larval developmental time. Behavior Genetics, 17(5), 523–535.
Chandler, C. H., Chari, S., Kowalski, A., Choi, L., Tack, D., DeNieu, M., & Dworkin, I. (2017). How well do you know your mutation? Complex effects of genetic background on expressivity, complementation, and ordering of allelic effects. PLoS Genetics, 13(11), e1007075. https://doi.org/10.1371/journal.pgen.1007075
Chippindale, A. K., Alipaz, J. A., Chen, H.-W., & Rose, M. R. (1997). Experimental evolution of accelerated development in Drosophila. 1. Developmental speed and larval survival. Evolution, 51(5), 1536–1551. https://doi.org/10.1111/j.1558-5646.1997.tb01477.x
Chippindale, A. K., Alipaz, J. A., & Rose, M. R. (2004). Experimental evolution of accelerated development in Drosophila. 2. Adult fitness and the fast development syndrome. Methuselah flies, a case study in the evolution of aging. 413–35. https://doi.org/10.1142/9789812567222_0034
Chippindale, A. K., Ngo, A. L., & Rose, M. R. (2003). The devil in the details of life-history evolution: Instability and reversal of genetic correlations during selection on Drosophila development. Journal of Genetics, 82(3), 133–145.
Davidowitz, G., D’Amico, L. J., & Nijhout, H. F. (2004). The effects of environmental variation on a mechanism that controls insect body size. Evolutionary Ecology Research, 6(1), 49–62.
Davidson, A. M., Jennions, M., & Nicotra, A. B. (2011). Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecology Letters, 14(4), 419–431. https://doi.org/10.1111/j.1461-0248.2011.01596.x
Del Pino, F., Salgado, E., & Godoy-Herrera, R. (2012). Plasticity and genotype× environment interactions for locomotion in Drosophila melanogaster larvae. Behavior Genetics, 42(1), 162–169. https://doi.org/10.1007/s10519-011-9490-1
DeWitt, T. J. (2016). Expanding the phenotypic plasticity paradigm to broader views of trait space and ecological function. Current Zoology, 62(5), 463–473. https://doi.org/10.1093/cz/zow085
DeWitt, T. J., & Scheiner, S. M. (2004). Phenotypic plasticity: Functional and conceptual approaches. Oxford University Press.
Di Cara, F., & King-Jones, K. (2013). How clocks and hormones act in concert to control the timing of insect development. Current Topics in Developmental Biology, 105, 1–36. https://doi.org/10.1016/B978-0-12-396968-2.00001-4
Flatt, T. (2005). The evolutionary genetics of canalization. The Quarterly Review of Biology, 80(3), 287–316. https://doi.org/10.1086/432265
Flatt, T., & Heyland, A. (2011). Mechanisms of life history evolution: The genetics and physiology of life history traits and trade-offs. Oxford University Press.
Folguera, G., Ceballos, S., Spezzi, L., Fanara, J. J., & Hasson, E. (2008). Clinal variation in developmental time and viability, and the response to thermal treatments in two species of Drosophila. Biological Journal of the Linnean Society, 95(2), 233–245. https://doi.org/10.1111/j.1095-8312.2008.01053.x
Forsman, A., & Wennersten, L. (2016). Inter-individual variation promotes ecological success of populations and species: Evidence from experimental and comparative studies. Ecography, 39(7), 630–648. https://doi.org/10.1111/ecog.01357
Fowler, M. A., & Montell, C. (2013). Drosophila TRP channels and animal behavior. Life Sciences, 92(8–9), 394–403. https://doi.org/10.1016/j.lfs.2012.07.029
Gasch, A. P., Payseur, B. A., & Pool, J. E. (2016). The power of natural variation for model organism biology. Trends in Genetics, 32(3), 147–154. https://doi.org/10.1016/j.tig.2015.12.003
Gibson, G. (2009). Decanalization and the origin of complex disease. Nature Reviews Genetics, 10(2), 134–140. https://doi.org/10.1038/nrg2502
Gibson, G., & Wagner, G. (2000). Canalization in evolutionary genetics: A stabilizing theory? BioEssays, 22, 372–380. https://doi.org/10.1002/(sici)1521-1878(200004)22:4%3C372::aid-bies7%3E3.0.co;2-j
Goddard, M. E., Kemper, K. E., MacLeod, I. M., Chamberlain, A. J., & Hayes, B. J. (2016). Genetics of complex traits: Prediction of phenotype, identification of causal polymorphisms and genetic architecture. Proceedings of the Royal Society b: Biological Sciences, 283(1835), 20160569. https://doi.org/10.1098/rspb.2016.0569
Goldberg, A. D., Allis, C. D., & Bernstein, E. (2007). Epigenetics: A landscape takes shape. Cell, 128, 635–638. https://doi.org/10.1016/j.cell.2007.02.006
Goswami, A., Smaers, J. B., Soligo, C., & Polly, P. D. (2014). The macroevolutionary consequences of phenotypic integration: From development to deep time. Philosophical Transactions of the Royal Society b: Biological Sciences, 369(1649), 20130254. https://doi.org/10.1098/rstb.2013.0254
Hall, B. K. (2003). Evo-Devo: Evolutionary developmental mechanisms. International Journal of Developmental Biology, 47(7–8), 491–495.
Hansen, T. F. (2006). The evolution of genetic architecture. Annual Review of Ecology, Evolution, and Systematics, 37, 123–157.
Harbison, S. T., McCoy, L. J., & Mackay, T. F. C. (2013). Genome-wide association study of sleep in Drosophila melanogaster. BMC Genomics, 14(1), 281. https://doi.org/10.1186/1471-2164-14-281
Herman, J. J., Spencer, H. G., Donohue, K., & Sultan, S. E. (2014). How stable ‘should’ epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution, 68(3), 632–643. https://doi.org/10.1111/evo.12324
Hoffmann, A. A., & Weeks, A. R. (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(2), 133–147. https://doi.org/10.1007/s10709-006-9010-z
Houle, D., Govindaraju, D. R., & Omholt, S. (2010). Phenomics: The next challenge. Nature Reviews Genetics, 11(12), 855–866. https://doi.org/10.1038/nrg2897
Huang, W., Campbell, T., Carbone, M. A., Jones, W. E., Unselt, D., Anholt, R. R., & Mackay, T. F. (2020). Context-dependent genetic architecture of Drosophila life span. PLoS Biology, 18(3), e3000645. https://doi.org/10.1371/journal.pbio.3000645
Huang, W., Massouras, A., Inoue, Y., Peiffer, J., Ràmia, M., Tarone, A. M., & Mackay, T. F. (2014). Natural variation in genome architecture among 205 Drosophila melanogaster genetic reference panel lines. Genome Research, 24(7), 1193–1208. https://doi.org/10.1101/gr.171546.113
Kolss, M., Vijendravarma, R. K., Schwaller, G., & Kawecki, T. J. (2009). Life-history consequences of adaptation to larval nutritional stress in Drosophila. Evolution, 63(9), 2389–2401. https://doi.org/10.1111/j.1558-5646.2009.00718.x
Krimsky, S., & Gruber, J. (2013). Genetic explanations: Sense and nonsense. Harvard University Press.
Lavagnino, N. J., Anholt, R. R. H., & Fanara, J. J. (2008). Variation in genetic architecture of olfactory behaviour among wild-derived populations of Drosophila melanogaster. Journal of Evolutionary Biology, 21(4), 988–996.
Lavagnino, N. J., & Fanara, J. J. (2016). Changes across development influence visible and cryptic natural variation of Drosophila melanogaster olfactory response. Evolutionary Biology, 43(1), 96–108. https://doi.org/10.1111/j.1420-9101.2008.01546.x
Lukacsovich, T., Asztalos, Z., Awano, W., Baba, K., Kondo, S., Niwa, S., et al. (2001). Dual-tagging gene trap of novel genes in Drosophila melanogaster. Genetics, 157, 727–742. https://doi.org/10.1093/genetics/157.2.727
Lyne, R., Smith, R., Rutherford, K., Wakeling, M., Varley, A., Guillier, F., et al. (2007). FlyMine: An integrated database for Drosophila and Anopheles genomics. Genome Biology, 8(7), R129. https://doi.org/10.1186/gb-2007-8-7-r129
Mackay, T. F. C. (2001). The genetic architecture of quantitative traits. In G. Wagner (Ed.), The Character Concept in Evolutionary Biology. Academic Press.
Mackay, T. F. C., & Huang, W. (2018). Charting the genotype-phenotype map: Lessons from the Drosophila melanogaster genetic reference panel. Wiley Interdisciplinary Reviews: Developmental Biology, 7(1), e289. https://doi.org/10.1002/wdev.289
Mackay, T. F. C., & Lyman, R. F. (2005). Drosophila bristles and the nature of quantitative genetic variation. Philosophical Transactions of the Royal Society B, 360(1459), 1513–1527. https://doi.org/10.1098/rstb.2005.1672
Mackay, T. F. C., Richards, S., Stone, E. A., Barbadilla, A., Ayroles, J. F., Zhu, D., et al. (2012). The Drosophila melanogaster genetic reference panel. Nature, 482(7384), 173–178. https://doi.org/10.1038/nature10811
Mäkinen, H., Sävilammi, T., Papakostas, S., Leder, E., Vøllestad, L. A., & Primmer, C. R. (2018). Modularity facilitates flexible tuning of plastic and evolutionary gene expression responses during early divergence. Genome Biology and Evolution, 10(1), 77–93. https://doi.org/10.1093/gbe/evx278
Massey, J. H., & Wittkopp, P. J. (2016). The genetic basis of pigmentation differences within and between Drosophila species. Current topics in developmental biology, 119, 27–61. https://doi.org/10.1016/bs.ctdb.2016.03.004
Matuszewski, S., Hermisson, J., & Kopp, M. (2015). Catch me if you can: Adaptation from standing genetic variation to a moving phenotypic optimum. Genetics, 200(4), 1255–1274. https://doi.org/10.1534/genetics.115.178574
Maurano, M. T., Humbert, R., Rynes, E., Thurman, R. E., Haugen, E., Wang, H., & Stamatoyannopoulos, J. A. (2012). Systematic localization of common disease-associated variation in regulatory DNA. Science, 337(6099), 1190–1195. https://doi.org/10.1126/science.1222794
Mensch, J., Carreira, V., Lavagnino, N., Goenaga, J., Folguera, G., Hasson, E., et al. (2010). Stage-specific effects of candidate heterochronic genes on variation in developmental time along an altitudinal cline of Drosophila melanogaster. PLoS ONE, 5(6), e11229. https://doi.org/10.1371/journal.pone.0011229
Mensch, J., Lavagnino, N., Carreira, V. P., Massaldi, A., Hasson, E., & Fanara, J. J. (2008). Identifying candidate genes affecting developmental time in Drosophila melanogaster: Pervasive pleiotropy and gene-by-environment interaction. BMC Developmental Biology, 8(1), 1–12. https://doi.org/10.1186/1471-213X-8-78
Mirth, C. K., Tang, H. Y., Makohon-Moore, S. C., Salhadar, S., Gokhale, R. H., Warner, R. D., & Shingleton, A. W. (2014). Juvenile hormone regulates body size and perturbs insulin signaling in Drosophila. Proceedings of the National Academy of Sciences, 111(19), 7018–7023. https://doi.org/10.1073/pnas.1313058111
Mirth, C., Truman, J. W., & Riddiford, L. M. (2005). The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Current Biology, 15(20), 1796–1807. https://doi.org/10.1016/j.cub.2005.09.017
Mołoń, M., Dampc, J., Kula-Maximenko, M., Zebrowski, J., Mołoń, A., Dobler, R., & Skoczowski, A. (2020). Effects of temperature on lifespan of Drosophila melanogaster from different genetic backgrounds: Links between metabolic rate and longevity. InSects, 11(8), 470. https://doi.org/10.3390/insects11080470
Morgante, F., Sørensen, P., Sorensen, D. A., Maltecca, C., & Mackay, T. F. (2015). Genetic architecture of micro-environmental plasticity in Drosophila melanogaster. Scientific Reports, 5(1), 1–10. https://doi.org/10.1038/srep09785
Mueller, L., & Sweet, V. (1986). Density-dependent natural selection in Drosophila: Evolution of pupation height. Evolution, 40(6), 1354–1356. https://doi.org/10.2307/2408963
Müller, G. B. (2007). Evo–devo: Extending the evolutionary synthesis. Nature Reviews Genetics, 8(12), 943–949. https://doi.org/10.1038/nrg2219
Narasimha, S., Kolly, S., Sokolowski, M. B., Kawecki, T. J., & Vijendravarma, R. K. (2015). Prepupal building behavior in Drosophila melanogaster and its evolution under resource and time constraints. PLoS ONE, 10(2), e0117280. https://doi.org/10.1371/journal.pone.0117280
Nijhout, H. F., Riddiford, L. M., Mirth, C., Shingleton, A. W., Suzuki, Y., & Callier, V. (2014). The developmental control of size in insects. Wiley Interdisciplinary Reviews: Developmental Biology, 3, 113–134.
Nylin, S., & Gotthard, K. (1998). Plasticity in life-history traits. Annual Review of Entomology, 43(1), 63–83. https://doi.org/10.1146/annurev.ento.43.1.63
Ørsted, M., Rohde, P. D., Hoffmann, A. A., Sørensen, P., & Kristensen, T. N. (2018). Environmental variation partitioned into separate heritable components. Evolution, 72(1), 136–152. https://doi.org/10.1111/evo.13391
Paaby, A., & Gibson, G. (2016). Cryptic genetic variation in evolutionary developmental genetics. Biology (basel), 5(2), 28. https://doi.org/10.3390/biology5020028
Partridge, L., & Fowler, K. (1992). Direct and correlated responses to selection on age at reproduction in Drosophila melanogaster. Evolution, 46(1), 76. https://doi.org/10.1111/j.1558-5646.1992.tb01986.x
Petino Zappala, M. A., Ortiz, V. E., & Fanara, J. J. (2018). Study of natural genetic variation in early fitness traits reveals decoupling between larval and pupal developmental time in Drosophila melanogaster. Evolutionary Biology., 45(4), 437–448. https://doi.org/10.1007/s11692-018-9461-z
Petino Zappala, M. A., Satorre, I., & Fanara, J. J. (2019). Stage- and thermal-specific genetic architecture for preadult viability in natural populations of Drosophila melanogaster. Journal of Evolutionary Biology. https://doi.org/10.1111/jeb.13448
Raff, R. A. (2000). Evo-devo: The evolution of a new discipline. Nature Reviews Genetics, 1(1), 74–79. https://doi.org/10.1038/35049594
Rice, S. H. (1998). The evolution of canalization and the breaking of Von Baer’s laws: Modeling the evolution of development with epistasis. Evolution, 52(3), 647–656. https://doi.org/10.1111/j.1558-5646.1998.tb03690.x
Riedl, C. L., Riedl, M., Mackay, T. F. C., & Sokolowski, M. B. (2007). Genetic and behavioral analysis of natural variation in Drosophila melanogaster pupation position. Fly (austin), 1(1), 23–32. https://doi.org/10.4161/fly.3830
Rockman, M. V. (2012). The QTN program and the alleles that matter for evolution: All that’s gold does not glitter. Evolution, 66, 1–17. https://doi.org/10.1111/j.1558-5646.2011.01486.x
Roff, D. A. (2002). Life history evolution. Sinauer Associates.
Rolandi, C., Lighton, J. R., de la Vega, G. J., Schilman, P. E., & Mensch, J. (2018). Genetic variation for tolerance to high temperatures in a population of Drosophila melanogaster. Ecology and Evolution, 8(21), 10374–10383. https://doi.org/10.1002/ece3.4409
Schlichting, C. D. (2008). Hidden reaction norms, cryptic genetic variation, and evolvability. Annals of the New York Academy of Sciences, 1133(1), 187–203. https://doi.org/10.1196/annals.1438.010
Schlichting, C. D. (2021). 15. Plasticity and evolutionary theory: Where We are and where we should be going. In D. W. Pfennig (Ed.), Phenotypic plasticity & evolution: Causes, consequences, controversies. (Vol. 367). Berlin: Taylor & Francis.
Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sinauer Associates Inc.
Schnebel, E. M., & Grossfield, J. (1986). The influence of light on pupation height in Drosophila. Behavior Genetics, 16(3), 407–413. https://doi.org/10.1007/BF01071320
Simons, A. M. (2014). Playing smart vs. playing safe: The joint expression of phenotypic plasticity and potential bet hedging across and within thermal environments. Journal of Evolutionary Biology., 27(6), 1047–1056. https://doi.org/10.1111/jeb.12378
Simons, A. M., & Johnston, M. O. (1997). Developmental instability as a bet-hedging strategy. Oikos, 80(2), 401–406. https://doi.org/10.2307/3546608
Sokolowski, M. B., & Hansell, R. I. (1983). Elucidating the behavioral phenotype of Drosophila melanogaster larvae: Correlations between larval foraging strategies and pupation height. Behavioral Genetics., 13(3), 267–280. https://doi.org/10.1007/BF01071872
Stearns, S. C. (1992). The evolution of life histories. Oxford University Press.
Trotta, V., Calboli, F. C., Ziosi, M., Guerra, D., Pezzoli, M. C., David, J. R., et al. (2006). Thermal plasticity in Drosophila melanogaster: A comparison of geographic populations. BMC Evolutionary Biology., 6(1), 67. https://doi.org/10.1186/1471-2148-6-67
Varón-González, C., Pallares, L. F., Debat, V., & Navarro, N. (2019). Mouse skull mean shape and shape robustness rely on different genetic architectures and different loci. Frontiers in Genetics, 10, 64. https://doi.org/10.3389/fgene.2019.00064
Wagner, G. P., Pavlicev, M., & Cheverud, J. M. (2007). The road to modularity. Nature Reviews Genetics, 8(12), 921–931. https://doi.org/10.1038/nrg2267
Welbergen, P., & Sokolowski, M. B. (1994). Development time and pupation behavior in the Drosophila melanogaster subgroup (Diptera: Drosophilidae). Journal of Insect Behavior, 7(3), 263–277. https://doi.org/10.1007/BF01989734
Whiteman, N. K. (2022). Evolution in small steps and giant leaps. Evolution, 76(s1), 67–77. https://doi.org/10.1111/evo.14432
Wijngaarden, P. J., & Brakefield, P. M. (2001). Lack of response to artificial selection on the slope of reaction norms for seasonal polyphenism in the butterfly Bicyclus anynana. Heredity, 87(4), 410–420. https://doi.org/10.1046/j.1365-2540.2001.00933.x
Yadav, P., & Sharma, V. K. (2014). Correlated changes in life history traits in response to selection for faster pre-adult development in the fruit fly Drosophila melanogaster. Journal of Experimental Biology, 217(4), 580–589. https://doi.org/10.1242/jeb.093864
Yamamichi, M. (2022). How does genetic architecture affect eco-evolutionary dynamics? A theoretical perspective. Philosophical Transactions of the Royal Society B. https://doi.org/10.1098/rstb.2020.0504
Yang, A. S. (2001). Modularity, evolvability, and adaptive radiations: A comparison of the hemi-and holometabolous insects. Evolution & Development, 3(2), 59–72. https://doi.org/10.1046/j.1525-142x.2001.003002059.x
Acknowledgements
We thank Trudy Mackay (Clemson Center for Human Genetics, Greenwood, SC, USA) for providing us with some of the lines used in this work. This work was supported by grants PICT-2012-0640 and PICT-2016-2256 from Agencia Nacional de Promoción Científica y Tecnológica (FONCyT, PICT) and PIP 112-201101-00717 from Consejo Nacional de Ciencia y Técnica (CONICET).
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MAPZ: collected data, performed analyses and wrote the main manuscript text. JM: collected data and performed analyses. VC: collected data and performed analyses. IS collected data and performed analyses. JJF: designed and directed this study, collected data and performed analyses. All authors reviewed and approved the manuscript.
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Petino Zappala, M.A., Mensch, J., Carreira, V. et al. Genome Wide Association Studies of Early Fitness Traits in Drosophila melanogaster Unveil Plasticity and Decoupling of Different Aspects of Phenotype. Evol Biol 51, 69–81 (2024). https://doi.org/10.1007/s11692-023-09619-y
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DOI: https://doi.org/10.1007/s11692-023-09619-y