Skip to main content
SpringerLink
Log in

Study of Natural Genetic Variation in Early Fitness Traits Reveals Decoupling Between Larval and Pupal Developmental Time in Drosophila melanogaster

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Characterizing the relationships between genotype and phenotype for developmental adaptive traits is essential to understand the evolutionary dynamics underlying biodiversity. In holometabolous insects, the time to reach the reproductive stage and pupation site preference are two such traits. Here we characterize aspects of the genetic architecture for Developmental Time (decomposed in Larval and Pupal components) and Pupation Height using lines derived from three natural populations of Drosophila melanogaster raised at two temperatures. For all traits, phenotypic differences and variation in plasticity between populations suggest adaptation to the original thermal regimes. However, high variability within populations shows that selection does not exhaust genetic variance for these traits. This could be partly explained by local adaptation, environmental heterogeneity and modifications in the genetic architecture of traits according to environment and ontogenetic stage. Indeed, our results show that the genetic factors affecting Developmental Time and Pupation Height are temperature-specific. Varying relationships between Larval and Pupal Developmental Time between and within populations also suggest stage-specific modifications of genetic architecture for this trait. This flexibility would allow for a somewhat independent evolution of adaptive traits at different environments and life stages, favoring the maintenance of genetic variability and thus sustaining the traits’ evolvabilities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Angilletta, M., Steury, T., & Sears, M. (2004). Temperature, growth rate, and body size in ectotherms: Fitting pieces of a life-history puzzle. Integrative and Comparative Biology, 44, 498–509.

    PubMed  Google Scholar 

  • Arbeitman, M. N., Furlong, E. E., Imam, F., Johnson, E., Null, B. H., et al. (2002). Gene expression during the life cycle of Drosophila melanogaster. Science, 297, 2270–2275.

    CAS  PubMed  Google Scholar 

  • Artieri, C. G., & Singh, R. S. (2010). Molecular evidence for increased regulatory conservation during metamorphosis, and against deleterious cascading effects of hybrid breakdown in Drosophila. BMC Biology, 8, 26.

    PubMed  PubMed Central  Google Scholar 

  • Atchley, W. R., Gaskins, C. T., & Anderson, D. (1976). Statistical properties of ratios. I. Empirical results. Systematic Biology, 25, 137–148.

    Google Scholar 

  • Bauer, S. J., & Sokolowski, M. B. (1985). A genetic analysis of path length and pupation height in a natural population of Drosophila melanogaster. Canadian Journal of Genetics and Cytology, 27, 334–340.

    Google Scholar 

  • Beltramí, M., Medina-Muñoz, M. C., Arce, D., & Godoy-Herrera, R. (2010). Drosophila pupation behavior in the wild. Evolutionary Ecology, 24, 347–358.

    Google Scholar 

  • Bharathi, N. S., Prasad, N. G., Shakarad, M., & Joshi, A. (2004). Correlates of sexual dimorphism for dry weight and development time in five species of Drosophila. Journal of Zoology, 264, 87–95.

    Google Scholar 

  • Bryant, E. H. (1969). A system favoring evolution of holometabolous development. Annals of the Entomological Society of America, 62, 1087–1091.

    Google Scholar 

  • Bürger, R., & Gimelfarb, A. (2002). Fluctuating environments and the role of mutation in maintaining quantitative genetic variation. Genetics Research, 80, 31–46.

    Google Scholar 

  • Carreira, V. P., Imberti, M., Mensch, J., & Fanara, J. J. (2013). Gene-by-temperature interactions and candidate plasticity genes for morphological traits in Drosophila melanogaster. PLoS ONE, 8(7), e70851.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Casares, P., & Carracedo, M. C. (1987). Pupation height in Drosophila: Sex differences and influence of larval developmental time. Behavior Genetics, 17, 523–535.

    CAS  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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. In M. R. Rose, H. B. Passananti & M. Matos (eds.), Methuselah flies: A case study in the evolution of aging (pp. 413–435). Singapore: World Scientific Press.

    Google Scholar 

  • 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, 133–145.

    PubMed  Google Scholar 

  • Conner, J. C., & Hartl, D. L. (2004). A primer of ecological genetics. Sunderland: Sinauer Associates Incorporated.

    Google Scholar 

  • Davidowitz, G., & Nijhout, H. F. (2004). The physiological basis of reaction norms: The interaction between growth rate, the duration of growth and body size. Integrative and Comparative Biology, 44, 443–449.

    PubMed  Google Scholar 

  • Del Pino, F., Jara, C., Pino, L., & Godoy-Herrera, R. (2014). The neuro-ecology of Drosophila pupation behavior. PLoS ONE, 9(7), e102159.

    PubMed  PubMed Central  Google Scholar 

  • Del Pino, F., Salgado, E., & Godoy-Herrera, R. (2012). Plasticity and genotype x environment interactions for locomotion of Drosophila melanogaster larvae. Behavior Genetics, 42, 162–169.

    PubMed  Google Scholar 

  • DeWitt, J., & Scheiner, S. M. (2004). Phenotypic plasticity: Functional and conceptual approaches. Oxford: Oxford University Press.

    Google Scholar 

  • Dillon, M., Wang, G., Garrity, P. A., & Huey, R. B. (2009). Thermal preference in Drosophila. Journal of Thermal Biology, 34, 109–119.

    PubMed  PubMed Central  Google Scholar 

  • Ebenman, B. (1987). Niche differences between age classes and intraspecific competition in age-structured populations. Journal of Theoretical Biology, 124, 25–33.

    Google Scholar 

  • Edgar, B. A. (2006). How flies get their size: Genetics meets physiology. Nature Reviews Genetics, 7, 907–916.

    CAS  PubMed  Google Scholar 

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics (4th ed.). Essex: Longman.

    Google Scholar 

  • Fallis, L. C., Fanara, J. J., & Morgan, T. J. (2014). Developmental thermal plasticity among Drosophila melanogaster populations. Journal of Evolutionary Biology, 27, 557–564.

    CAS  PubMed  Google Scholar 

  • Fanara, J. J., Folguera, G., Fernandez Iriarte, P., Mensch, J., & Hasson, E. (2006). Genotype by environment interactions in viability and developmental time in populations of cactophilic Drosophila. Journal of Evolutionary Biology, 19, 900–906.

    CAS  PubMed  Google Scholar 

  • Fanara, J. J., & Hasson, E. (2001). Oviposition acceptance and fecundity schedule in the cactophilic sibling species Drosophila buzzatii. and D. koepferae on their natural hosts. Evolution, 55, 2615–2619.

    CAS  PubMed  Google Scholar 

  • Flatt, T. (2005). The evolutionary genetics of canalization. The Quarterly Review of Biology, 80, 287–316.

    PubMed  Google Scholar 

  • Flatt, T., & Heyland, A. (2011). Mechanisms of life history evolution: The genetics and physiology of life history traits and trade-offs. Oxford: Oxford University Press.

    Google Scholar 

  • Folguera, G., Mensch, J., Muñoz, J. L., Ceballos, S. G., Hasson, E., & Bozinovic, F. (2010). Ontogenetic stage-dependent effect of temperature on developmental and metabolic rates in a holometabolous insect. Journal of Insect Physiology, 56, 1679–1684.

    CAS  PubMed  Google Scholar 

  • Gerstein, M. B., Rozowsky, J., Yan, K. K., Wang, D., Cheng, C., et al. (2014). Comparative analysis of the transcriptome across distant species. Nature, 512, 445–448.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilchrist, G. W., Jeffers, L. M., West, B., Folk, D. G., Suess, J., & Huey, R. B. (2008). Clinal patterns of desiccation and starvation resistance in ancestral and invading populations of Drosophila subobscura. Evolutionary Applications, 1, 513–523.

    PubMed  PubMed Central  Google Scholar 

  • Goldstein, D. B., & Pollock, D. D. (1997). Launching microsatellites: A review of mutation processes and methods of phylogenetic inference. Journal of Heredity, 88, 335–342.

    CAS  PubMed  Google Scholar 

  • Hansen, T. F. (2006). The evolution of genetic architecture. Annual Review of Ecology, Evolution, and Systematics, 37, 123–157.

    Google Scholar 

  • Houle, D. (1992). Comparing evolvability and variability of quantitative traits. Genetics, 130, 195–204.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, W., Massouras, A., Inoue, Y., Peiffer, J., Ràmia, M., et al. (2014). Natural variation in genome architecture among 205 Drosophila melanogaster genetic reference panel lines. Genome Research, 24, 1193–1208.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jumbo-Lucioni, P., Ayroles, J. F., Chambers, M. M., Jordan, K. W., Leips, J., Mackay, T. F., & De Luca, M. (2010). Systems genetics analysis of body weight and energy metabolism traits in Drosophila melanogaster. BMC Genomics, 11, 297.

    PubMed  PubMed Central  Google Scholar 

  • Kingsolver, J. G., & Huey, R. B. (2008). Size, temperature, and fitness: Three rules. Evolutionary Ecology Research, 10, 251–268.

    Google Scholar 

  • Lavagnino, N., Anholt, R. R. H., & Fanara, J. J. (2008). Variation in genetic architecture of olfactory behavior among wild-derived populations of Drosophila melanogaster. Journal of Evolutionary Biology, 21, 988–996.

    CAS  PubMed  Google Scholar 

  • Lavagnino, N., & Fanara, J. J. (2016). Changes across development influence visible and cryptic natural variation of Drosophila melanogaster olfactory response. Evolutionary Biology, 43, 96–108.

    Google Scholar 

  • Long, T. A. F., Pischedda, A., Stewart, A. D., & Rice, W. R. (2009). A cost of sexual attractiveness to high-fitness females. PLoS Biology, 7(12), e1000254.

    PubMed  PubMed Central  Google Scholar 

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits (p. 663). Sunderland: Sinauer Associates, Inc.

    Google Scholar 

  • Mackay, T. F. C. (2001). The genetic architecture of quantitative traits. Annual Review of Genetics, 35, 303–339.

    CAS  PubMed  Google Scholar 

  • Mackay, T. F. C., Richards, S., Stone, E. A., Barbadilla, A., Ayroles, J. F., et al. (2012). The Drosophila melanogaster genetic reference panel. Nature, 482, 173–178.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Markow, T. A. (1979). A survey of intra- and interspecific variation for pupation height in Drosophila. Behavior Genetics, 9, 209–217.

    CAS  PubMed  Google Scholar 

  • Matzkin, L. M., Watts, T. D., & Markow, T. A. (2007). Desiccation resistance in four Drosophila species: Sex and population effects. Fly, 1, 268–273.

    PubMed  Google Scholar 

  • McMahon, D. P., & Hayward, A. (2016). Why grow up? A perspective on insect strategies to avoid metamorphosis. Ecological Entomology, 41, 505–515.

    Google Scholar 

  • Melo, D., Porto, A., Cheverud, J. M., & Marroig, G. (2016). Modularity: Genes, development, and evolution. Annual Review of Ecology, Evolution, and Systematics, 47, 463–486.

    PubMed  PubMed Central  Google Scholar 

  • Mensch, J., Carreira, V. P., Lavagnino, N., Goenaga, J., Folguera, G., Hasson, E., & Fanara, J. J. (2010). State-specifics effects of candidate heterochronic genes on variation in developmental time along an altitudinal cline of Drosophila melanogaster. PLoS ONE, 5(6), e11229.

    PubMed  PubMed Central  Google Scholar 

  • 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, 78.

    PubMed  PubMed Central  Google Scholar 

  • Minelli, A., Brena, C., Deflorian, G., Maruzzo, D., & Fusco, G. (2006). From embryo to adult—beyond the conventional periodization of arthropod development. Development Genes and Evolution, 216, 373–383.

    PubMed  Google Scholar 

  • Minelli, A., & Fusco, G. (2010). Developmental plasticity and the evolution of animal complex life cycles. Philosophical Transactions of the Royal Society B, 365, 631–640.

    Google Scholar 

  • Mirth, C. K., & Riddiford, L. M. (2007). Size assessment and growth control: How adult size is determined in insects. Bioessays, 29, 344–355.

    CAS  PubMed  Google Scholar 

  • Moran, N. (1994). Adaptation and constraint in the complex life cycles of animals. Annual Review of Ecology and Systematics, 25, 573–600.

    Google Scholar 

  • Mousseau, T. A., & Roff, D. A. (1987). Natural selection and the heritability of fitness components. Heredity, 59, 181–197.

    PubMed  Google Scholar 

  • Mueller, L. D., & Sweet, V. F. (1986). Density-dependent natural selection in Drosophila: Evolution of pupation height. Evolution, 40, 1354–1356.

    PubMed  Google Scholar 

  • 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, e0117280.

    PubMed  PubMed Central  Google Scholar 

  • Nunney, L. (1996). The response to selection for fast larval development in Drosophila melanogaster and its effect on adult weight: An example of a fitness trade-off. Evolution, 50, 1193–1204.

    PubMed  Google Scholar 

  • Nunney, L. (2007). Pupal period and adult size in Drosophila melanogaster: A cautionary tale of contrasting correlations between two sexually dimorphic traits. Journal of Evolutionary Biology, 20, 141–151.

    CAS  PubMed  Google Scholar 

  • Nylin, S., & Gotthard, K. (1998). Plasticity in life-history traits. Annual Review of Entomology, 43, 63–83.

    CAS  PubMed  Google Scholar 

  • Paranjpe, D. A., Anitha, D., Chandrashekaran, M. K., Joshi, A., & Sharma, V. K. (2005). Possible role of eclosion rhythm in mediating the effects of light-dark environments on pre-adult development in Drosophila melanogaster. BMC Developmental Biology, 5, 5.

    PubMed  PubMed Central  Google Scholar 

  • Partridge, L., Barrie, B., Fowler, K., & French, V. (1994). Thermal evolution of pre-adult life history traits in Drosophila melanogaster. Journal of Evolutionary Biology, 7, 645–663.

    Google Scholar 

  • Partridge, L., & Fowler, K. (1992). Direct and correlated response to selection on age at reproduction in Drosophila melanogaster. Evolution, 46, 76–91.

    PubMed  Google Scholar 

  • Prasad, N. G., Shakarad, M., Anitha, D., Rajamani, M., & Joshi, A. (2001). Correlated responses to selection for faster development and early reproduction in Drosophila: The evolution of larval traits. Evolution, 55, 1363–1372.

    CAS  PubMed  Google Scholar 

  • Rewitz, K. F., Yamanaka, N., & O’Connor, M. B. (2013). Chapter one—Developmental checkpoints and feedback circuits time insect maturation. Current Topics in Developmental Biology, 103, 1–33.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riedl, C. A., Riedl, M., Mackay, T. F., & Sokolowski, M. B. (2007). Genetic and behavioral analysis of natural variation in Drosophila melanogaster pupation position. Fly, 1, 23–32.

    PubMed  Google Scholar 

  • Rodrigues, M. A., Martins, N. E., Balancé, L. F., Broom, L. N., Dias, A. J., Fernandes, A. S. D., Rodrigues, F., Sucena, E., & Mirth, C. K. (2015). Drosophila melanogaster larvae make nutritional choices that minimize developmental time. Journal of Insect Physiology, 81, 69–80.

    CAS  PubMed  Google Scholar 

  • Roff, D. A. (1992). The evolution of life histories: Theory and analysis. New York: Chapman & Hall.

    Google Scholar 

  • Sasaki, A., & Ellner, S. (1997). Quantitative genetic variance maintained by fluctuating selection with overlapping generations: Variance components and covariances. Evolution, 51, 682–696.

    PubMed  Google Scholar 

  • Schlichting, C., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland: Sinauer Associates Incorporated.

    Google Scholar 

  • Shingleton, A. W., Das, J., Vinicius, L., & Stern, D. L. (2005). The temporal requirements for insulin signaling during development in Drosophila. PLoS Biology, 3(9), e289.

    PubMed  PubMed Central  Google Scholar 

  • Singh, B. N., & Pandey, M. B. (1993). Evidence for additive polygenic control of pupation heigh in Drosophila ananassae. Hereditas, 119, 111–116.

    CAS  PubMed  Google Scholar 

  • Sokolowski, M. B., & Hansell, R. I. (1983). Elucidating the behavioral phenotype of Drosophila melanogaster larvae: Correlations between larval foraging strategies and pupation height. Behavior Genetics, 13, 267–280.

    CAS  PubMed  Google Scholar 

  • Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology, 3, 259–268.

    Google Scholar 

  • Stearns, S. C. (1992). The evolution of life histories. Oxford: Oxford University Press.

    Google Scholar 

  • Trotta, V., Calboli, F. C., Ziosi, M., Guerra, D., Pezzoli, M. C., David, J. R., & Cavicchi, S. (2006). Thermal plasticity in Drosophila melanogaster: A comparison of geographic populations. BMC Evolutionary Biology, 6, 67.

    PubMed  PubMed Central  Google Scholar 

  • Truman, J. W., & Riddiford, L. M. (1999). The origins of insect metamorphosis. Nature, 401, 447–452.

    CAS  PubMed  Google Scholar 

  • van Noordwijk, A. J., & de Jong, G. (1986). Acquisition and allocation of resources: Their influence on variation in life history tactics. American Naturalist, 128, 137–142.

    Google Scholar 

  • Wagner, G. P., Booth, G., & Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution, 51(2), 329–347.

    PubMed  Google Scholar 

  • Welbergen, P., & Sokolowski, M. (1994). Development time and pupation behavior in the Drosophila melanogaster subgroup (Diptera: Drosophilidae). Journal of Insect Behavior, 7, 263–277.

    Google Scholar 

  • Werenkraut, V., Hasson, E., Oklander, L., & Fanara, J. J. (2008). A comparative study of competitive ability between two cactophilic species in their natural hosts. Austral Ecology, 33, 663–671.

    Google Scholar 

  • Yang, A. S. (2001). Modularity, evolvability, and adaptive radiations: A comparison of the hemi- and holometabolous insects. Evolution & Development, 3, 59–72.

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from Agencia Nacional de Promoción Científica y Tecnológica (FONCyT, PICT) and Consejo Nacional de Ciencia y Técnica (CONICET). MAPZ and VEO are recipients of doctoral scholarships from CONICET (Argentina) and JJF is a member of Carrera del Investigador Cientifico of CONICET (Argentina).

Author information

Authors and Affiliations

  1. Departamento de Ecologia, Genetica y Evolucion - IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires Ciudad Universitaria, Pabellon II, 1428, Buenos Aires, Argentina

    M. A. Petino Zappala, V. E. Ortiz & J. J. Fanara

Authors
  1. M. A. Petino Zappala
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. E. Ortiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. J. Fanara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. J. Fanara.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petino Zappala, M.A., Ortiz, V.E. & Fanara, J.J. Study of Natural Genetic Variation in Early Fitness Traits Reveals Decoupling Between Larval and Pupal Developmental Time in Drosophila melanogaster. Evol Biol 45, 437–448 (2018). https://doi.org/10.1007/s11692-018-9461-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-018-9461-z

Keywords

Search

Navigation