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Density-dependent selection in Drosophila: evolution of egg size and hatching time

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Abstract

Many different laboratory studies of adaptation to larval crowding in Drosophila spp. have all yielded the evolution of pre-adult competitive ability, even though the ecological context in which crowding was experienced varied across studies. However, the evolution of competitive ability was achieved through different suites of traits in studies wherein crowding was imposed in slightly different ways. Earlier studies showed the evolution of increased competitive ability via increased larval feeding rate and tolerance to nitrogenous waste, at the cost of food to biomass conversion efficiency. However, more recent studies, with crowding imposed at relatively low food levels, showed the evolution of competitive ability via decreased larval development time and body size, and an increase in the time efficiency of conversion of food to biomass, with no change in larval feeding rate or waste tolerance. Taken together, these studies have led to a more nuanced understanding of how the specific details of larval numbers, food amounts etc. can affect which traits evolve to confer increased competitive ability. Here, we report results from a study in which egg size and hatching time were assayed on three sets of populations adapted to larval crowding experienced in slightly different ways, as well as their low density ancestral control populations. Egg size and hatching time are traits that may provide larvae with initial advantages under crowding through increased starting larval size and a temporal head-start, respectively. In each set of populations adapted to some form of larval crowding, the evolution of longer and wider eggs was seen, compared to controls, thus making egg size the first consistent correlate of the evolution of increased larval competitive ability across Drosophila populations experiencing crowding in slightly different ways. Among the crowding-adapted populations, those crowded at the lowest overall eggs/food density, but the highest density of larvae in the feeding band, showed the largest eggs, on an average. All three sets of crowding-adapted populations showed shorter average egg hatching time than controls, but the difference was significant only in the case of populations experiencing the highest feeding band density. Our results underscore the importance of considering factors other than just eggs/food density when studying the evolution of competitive ability, as also the advantages of having multiple selection regimes within one experimental set up, allowing for a more nuanced understanding of the subtlety with which adaptive evolutionary trajectories can vary across even fairly similar selection regimes.

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References

  • Azevedo R. B., Partridge L. and French V. 1997 Life-history consequences of egg size in Drosophila melanogaster. Am. Nat. 150, 250–282.

    Article  CAS  PubMed  Google Scholar 

  • Bakker K. 1961 An analysis of factors which determine success in competition for food among larvae of Drosophila melanogaster. Arch. Neerl. Zool. 14, 200–281.

    Article  Google Scholar 

  • Bakker K. 1969 Selection for rate of growth and its influence on competitive ability of larvae of Drosophila melanogaster. Neth. J. Zool. 19, 541–595.

    Article  Google Scholar 

  • Bierbaum T. J., Mueller L. D. and Ayala F. J. 1989 Density-dependent evolution of life-history traits in Drosophila melanogaster. Evolution 43, 382–392.

    PubMed  Google Scholar 

  • Bitner K., Rutledge G. A., Kezos J. N. and Mueller L. D. 2021 The effects of adaptation to urea on feeding rates and growth in Drosophila larvae. Ecol. Evol 11, 9516–9529.

    Article  PubMed  PubMed Central  Google Scholar 

  • Borash D. J., Gibbs A. G., Joshi A. and Mueller L. D. 1998 A genetic polymorphism maintained by natural selection in a temporally varying environment. Am. Nat. 151, 148–156.

    Article  CAS  PubMed  Google Scholar 

  • Burnet B., Sewell D. and Bos M. 1977 Genetic analysis of larval feeding behaviour in Drosophila melanogaster. II. Growth relations and competition between selected lines. Genet. Res. 30, 149–161.

    Article  Google Scholar 

  • Chippindale A. K., Hoang D., Service P. and Rose M. R. 1994 The evolution of development in Drosophila selected for postponed senescence. Evolution 48, 1880–1899.

    Article  PubMed  Google Scholar 

  • Chippindale A. K., Alipaz J. A., Chen H.-W. and Rose M. R. 1997 Experimental evolution of accelerated development in Drosophila. 1 Developmental speed and larval survival. Evolution 51, 1536–1551.

    Article  PubMed  Google Scholar 

  • Fellowes M. D. E., Kraaijeveld A. R. and Godfray H. C. J. 1998 Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proc. R. Soc. London B 265, 1553–1558.

    Article  CAS  Google Scholar 

  • Fellowes M. D. E., Kraaijeveld A. R. and Godfray H. C. J. 1999 Association between feeding rate and parasitoid resistance in Drosophila melanogaster. Evolution 53, 1302–1305.

    Article  CAS  PubMed  Google Scholar 

  • Guo P. Z., Mueller L. D. and Ayala F. J. 1991 Evolution of behavior by density-dependent natural selection. Proc. Natl. Acad. Sci. USA 88, 10905–10906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi A. and Mueller L. D. 1988 Evolution of higher feeding rate in Drosophila due to density-dependent natural selection. Evolution 42, 1090–1092.

    Article  PubMed  Google Scholar 

  • Joshi A. and Mueller L. D. 1993 Directional and stabilizing density-dependent natural selection for pupation height in Drosophila melanogaster. Evolution 47, 176–184.

    Article  PubMed  Google Scholar 

  • Joshi A. and Mueller L. D. 1996 Density-dependent natural selection in Drosophila: trade-offs between larval food acquisition and utilization. Evol. Ecol. 10, 463–474.

    Article  Google Scholar 

  • Joshi A., Prasad N. G. and Shakarad M. 2001 K-selection, α-selection, effectiveness, and tolerance in competition: density-dependent selection revisited. J. Genet. 80, 63–75.

    Article  CAS  PubMed  Google Scholar 

  • Joshi A., Castillo R. H. and Mueller L. D. 2003 The contribution of ancestry, chance, and past and ongoing selection to adaptive evolution. J. Genet. 82, 147–162.

    Article  PubMed  Google Scholar 

  • Kawecki T. J. 1995 Adaptive plasticity of egg size in response to competition in the cowpea weevil, Callosobruchus maculatus (Coleoptera: Bruchidae). Oecologia 102, 81–85.

    Article  PubMed  Google Scholar 

  • Kumar L. 2014 A study of female reproductive investment in populations of Drosophila melanogaster adapted to larval crowding. M.S. thesis, Indian Institute of Science Education and Research, Mohali, India.

  • MacArthur R. H. 1962 Some generalized theorems of natural selection. Proc. Natl. Acad. Sci. USA 48, 1893–1897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacArthur R. H., Wilson E. O. 1967 The theory of island biogeography Princeton University Press, Princeton.

    Google Scholar 

  • Mueller L. D. 1988 Evolution of competitive ability in Drosophila by density-dependent natural selection. Proc. Natl. Acad. Sci. USA 85, 4383–4386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller L. D. 1990 Density-dependent natural selection does not increase efficiency. Evol. Ecol. 4, 290–297.

    Article  Google Scholar 

  • Mueller L. D. 1997 Theoretical and empirical examination of density-dependent selection. Annu. Rev. Ecol. Syst. 28, 269–288.

    Article  Google Scholar 

  • Mueller L. D. 2009 Fitness, demography, and population dynamics in laboratory experiments. In Experimental evolution: concepts, methods and applications of selection experiments (ed. T. Garland Jr. and M. R. Rose), pp. 197–216. University of California Press, Berkeley.

    Google Scholar 

  • Mueller L. D. and Ayala F. J. 1981 Trade-off between r-selection and K-selection in Drosophila populations. Proc. Natl. Acad. Sci. USA 78, 1303–1305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Mueller L. D. and Cabral L. G. 2012 Does phenotypic plasticity for adult size versus food level in Drosophila melanogaster evolve in response to adaptation to different rearing densities? Evolution 66, 263–271.

    Article  PubMed  Google Scholar 

  • Mueller L. D. and Barter T. T. 2015 A model of the evolution of larval feeding rate in Drosophila driven by conflicting energy demands. Genetica 143, 93–100.

    Article  CAS  PubMed  Google Scholar 

  • Mueller L. D. and Bitner K. 2015 The evolution of ovoviviparity in a temporally varying environment. Am. Nat. 186, 708–715.

    Article  PubMed  Google Scholar 

  • Mueller L. D., Graves J. and Rose M. R. 1993 Interactions between density-dependent and age-specific selection in Drosophila melanogaster. Func. Ecol. 7, 469–479.

    Article  Google Scholar 

  • Mueller L. D., Rauser C. L. and Rose M. R. 2005 Population dynamics, life history, and demography: lessons from Drosophila. Adv. Ecol. Res. 37, 77–99.

    Article  Google Scholar 

  • Nagarajan A., Natarajan S. B., Jayaram M., Thammanna A., Chari S., Bose J., Jois S. V. and Joshi A. 2016 Adaptation to larval crowding in Drosophila ananassae and Drosophila nasuta nasuta: increased larval competitive ability without increased larval feeding rate. J. Genet. 95, 411–425.

    Article  CAS  PubMed  Google Scholar 

  • Prasad N. G. and Joshi A. 2003 What have two decades of laboratory life-history evolution studies on Drosophila melanogaster taught us? J. Genet. 82, 45–76.

    Article  CAS  PubMed  Google Scholar 

  • Prasad N. G., Shakarad M., Rajamani M. and Joshi A. 2003 Interaction between the effects of maternal and larval levels of nutrition on pre-adult survival in Drosophila melanogaster. Evol. Ecol. Res. 5, 903–911.

    Google Scholar 

  • Prasad N. G., Shakarad M., Gohil V. M., Sheeba V., Rajamani M. and Joshi A. 2000 Evolution of reduced pre-adult viability and larval growth rate in laboratory populations of Drosophila melanogaster selected for shorter development time. Genet. Res. 76, 249–259.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rajamani M., Raghavendra N., Prasad N. G., Archana N., Joshi A. and Shakarad M. 2006 Reduced larval feeding rate is a strong evolutionary correlate of rapid development in Drosophila melanogaster. J. Genet. 85, 209–212.

    Article  CAS  PubMed  Google Scholar 

  • Rasband W. S. 1997-2018 ImageJ. U.S. National Institutes of Health, Bethesda, MD, USA (https://imagej.nih.gov/ij/).

  • Sang J. H. 1949 The ecological determinants of population growth in a Drosophila culture. III. Larval and Pupal Survival. Physiol. Zool. 22, 183–202.

    CAS  PubMed  Google Scholar 

  • Santos M., Borash D. J., Joshi A., Bounlutay N. and Mueller L. D. 1997 Density-dependent natural selection in Drosophila: evolution of growth rate and body size. Evolution 51, 420–432.

    PubMed  Google Scholar 

  • Sarangi M. 2018 Ecological details mediate different paths to the evolution of larval competitive ability in Drosophila. Ph.D. thesis, Jawaharlal Nehru Centre for Advanced Scientific Research, Bengaluru, India.

  • Sarangi M., Nagarajan A., Dey S., Bose J. and Joshi A. 2016 Evolution of increased larval competitive ability in Drosophila melanogaster without increased larval feeding rate. J. Genet. 95, 491–503.

    Article  PubMed  Google Scholar 

  • Shakarad M., Prasad N. G., Gokhale K., Gadagkar V., Rajamani M. and Joshi A. 2005 Faster development does not lead to correlated evolution of greater competitive ability in Drosophila melanogaster. Biol. Lett. 1, 91–94.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shiotsugu J., Leroi A. M., Yashiro H., Rose M. R. and Mueller L. D. 1997 The symmetry of correlated selection responses in adaptive evolution: an experimental study using Drosophila. Evolution 51, 163–172.

    Article  PubMed  Google Scholar 

  • Sokolowski M. B., Pereira H. S. and Hughes K. 1997 Evolution of foraging behavior in Drosophila by density-dependent selection. Proc. Natl. Acad. Sci. USA 94, 7373–7377.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • StatSoft 1995 Statistica Vol. I: general conventions and statistics 1. StatSoft Inc., Tulsa, USA.

  • Vijendravarma R. K., Narasimha S. and Kawecki T. J. 2010 Effects of parental larval diet on egg size and offspring traits in Drosophila. Biol. Lett. 6, 238–241.

    Article  PubMed  Google Scholar 

  • Yanagi S., Saeki Y. and Tuda M. 2013 Adaptive egg size plasticity for larval competition and its limits in the seed beetle Callosobruchus chinensis. Entomol. Exp. Appl. 148, 182–187.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Sajith V. S., Ramesh Kokile, Avani Mital, Medha Rao, Bhavya Pratap Singh, Rajanna N. and Muniraju for help with the experiments, and an anonymous reviewer for helpful comments on the manuscript. S. Venkitachalam was supported by a doctoral fellowship from the Jawaharlal Nehru Centre for Advanced Scientific Research. S. Das and A. Deep were supported during their sojourn in the lab by the Jawaharlal Nehru Centre for Advanced Scientific Research’s Project Oriented Biological Education and Summer Research Fellowship Programme, respectively. This work was supported by a J. C. Bose National Fellowship from the Science and Engineering Research Board, Government of India to A. Joshi and, in part, by A. Joshi’s personal funds.

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Author notes

  1. Srijan Das

    Present address: Molecular Genetics and Plant Biology Laboratory, Biology Division, Indian Institute of Science Education and Research Pune, Dr. Homi Bhabha Road, Pune, 411 008, India

  2. Auroni Deep

    Present address: Department of Zoology, University of Delhi, North Campus, Chhatra Marg, Faculty of Science, University Enclave, Delhi, 110 007, India

Authors and Affiliations

  1. Evolutionary Biology Laboratory, Jawaharlal Nehru Centre for Advanced Scientific Research, Jakkur, Bengaluru, 560 064, India

    Srikant Venkitachalam & Amitabh Joshi

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  1. Srikant Venkitachalam
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Correspondence to Amitabh Joshi.

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Corresponding editor: Upendra Nongthomba

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Venkitachalam, S., Das, S., Deep, A. et al. Density-dependent selection in Drosophila: evolution of egg size and hatching time. J Genet 101, 13 (2022). https://doi.org/10.1007/s12041-021-01355-6

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