Adaptation to larval crowding in Drosophila ananassae and Drosophila nasuta nasuta: increased larval competitive ability without increased larval feeding rate
Tóm tắt
The standard view of adaptation to larval crowding in fruitflies, built on results from 25 years of multiple experimental evolution studies on Drosophila melanogaster, was that enhanced competitive ability evolves primarily through increased larval feeding and foraging rate, and increased larval tolerance to nitrogenous wastes, at the cost of efficiency of food conversion to biomass. These results were at odds from the predictions of classical K-selection theory, notably the expectation that selection at high density should result in the increase of efficiency of conversion of food to biomass, and were better interpreted through the lens of α-selection. We show here that populations of D. ananassae and D. n. nasuta subjected to extreme larval crowding evolve greater competitive ability and pre-adult survivorship at high density, primarily through a combination of reduced larval duration, faster attainment of minimum critical size for pupation, greater time efficiency of food conversion to biomass and increased pupation height, with a relatively small role of increased urea/ammonia tolerance, if at all. This is a very different suite of traits than that seen to evolve under similar selection in D. melanogaster, and seems to be closer to the expectations from the canonical theory of K-selection. We also discuss possible reasons for these differences in results across the three species. Overall, the results reinforce the view that our understanding of the evolution of competitive ability in fruitflies needs to be more nuanced than before, with an appreciation that there may be multiple evolutionary routes through which higher competitive ability can be attained.
Tài liệu tham khảo
Ackermann M., Bijlsma R., James A. C., Partridge L., Zwaan B. J. and Stearns S. C. 2001 Effects of assay conditions in life-history experiments with Drosophila melanogaster. J. Evol. Biol. 14, 199–209.
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.
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.
Borash D. J., Teótonio H., Rose M. R. and Mueller L. D. 2000 Density-dependent natural selection in Drosophila: correlations between feeding rate, development time and viability. J. Evol. Biol. 13, 181–187.
Borash D. J. and Ho G. T. 2001 Patterns of selection: stress resistance and energy storage in density-dependent populations of Drosophila melanogaster. J. Insect Physiol. 47, 1349–1356.
Botella L. M., Gonzalez A. C., Moya A. and Mensua J. L. 1985 Larval stop, delayed development and survival in over-crowded cultures of Drosophila melanogaster: effect of urea and uric acid. J. Insect. Physiol. 31, 179–185.
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.
Dey S., Bose J. and Joshi A. 2012 Adaptation to larval crowding in Drosophila ananassae leads to the evolution of population stability. Ecol. Evol. 2, 941–951.
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.
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.
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.
Joshi A. and Mueller L. D. 1988 Evolution of higher feeding rate in Drosophila due to density-dependent natural selection. Evolution 42, 1090–1092.
Joshi A. and Mueller L. D. 1993 Directional and stabilizing density-dependent natural selection for pupation height in Drosophila melanogaster. Evolution 47, 176–184.
Joshi A. and Thompson J. N. 1995 Alternative routes to the evolution of competitive ability in two competing species of Drosophila. Evolution 49, 616–625.
Joshi A. and Mueller L. D. 1996 Density-dependent natural selection in Drosophila: trade-offs between resource acquisition and utilization. Evol. Ecol. 10, 463–474.
Joshi A. 1997 Laboratory studies of density-dependent selection: adaptations to crowding in Drosophila melanogaster. Curr. Sci 72, 555–562.
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.
Joshi A., Castillo R. B. and Mueller L. D. 2003 The contribution of ancestry, chance and past and ongoing selection to adaptive evolution. J. Genet. 82, 147–162.
Krijger C. L., Peters Y. C. and Sevenster J. G. 2001 Competitive ability of neotropical Drosophila predicted from larval development times. Oikos 92, 325–332.
MacArthur R. H. and Wilson E. O. 1967 The theory of island biogeography. Princeton University Press, Princeton, USA.
Mueller L. D. and Ayala A. J. 1981 Trade-off between r-selection and K-selection in Drosophila populations. Proc. Natl. Acad. Sci. USA 78, 1303–1305.
Mueller L. D. and Sweet V. F. 1986 Density-dependent natural selection in Drosophila: evolution of pupation height. Evolution 40, 1354–1356.
Mueller L. D. 1988 Evolution of competitive ability in Drosophila by density-dependent natural selection. Proc. Natl. Acad. Sci. USA 85, 4383–4386.
Mueller L. D. 1990 Density-dependent selection does not increase efficiency. Evol. Ecol. 4, 290–297.
Mueller L. D., Graves J. L. and Rose M. R. 1993 Interactions between density-dependent and age-specific selection in Drosophila melanogaster. Func. Ecol. 7, 469–479.
Mueller L. D. 1997 Theoretical and empirical examination of density-dependent selection. Annu. Rev. Ecol. Syst. 28, 269– 288.
Mueller L. D., Folk D. G., Nguyen N., Nguyen P., Lam P., Rose M. R. and Bradley T. J. 2005 Evolution of larval foraging behavior in Drosophila and its effect on growth and metabolic rates. Physiol. Entomol. 30, 262–269.
Mueller L. D. 2009 Fitness, demography, and population dynamics in laboratory experiments. In Experimental evolution: concepts, methods and applications of selection experiments (ed. T. Jr Garland and M. R. Rose), pp. 197–216. University of California Press, Berkeley, USA.
Mueller L. D., Rauser C. L. and Rose M. R. 2007 Population dynamics, life history and demography: lessons from Drosophila. Adv. Ecol. Res. 37, 77–99.
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.
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.
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.
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.
Ranganath H. A. and Aruna S. 2003 Hybridization, transgressive segregation and evolution of new genetic systems in Drosophila. J. Genet. 82, 163–177.
Rose M. R., Nusbaum T. J. and Chippindale A. K. 1996 Laboratory evolution: experimental wonderland and the Cheshire cat syndrome. In Adaptation (ed. M. R. Rose and G. V. Lauder), pp. 221–241. Academic Press, San Diego, USA.
Rose M. R., Passananti H. B., Chippindale A. K., Phelan J. P., Matos M., Teotónio H. and Mueller L. D. 2005 The effects of evolution are local: evidence from experimental evolution in Drosophila. Integr. Comp. Biol. 45, 486–491.
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.
Sharmila Bharathi N., Prasad N. G., Shakarad M. and Joshi A. 2003 Variation in adult life history and stress resistance across five species of Drosophila. J. Genet. 82, 191–205.
Sharmila Bharathi N., Prasad N. G., Shakarad M. and Joshi A. 2004 Correlates of sexual dimorphism for dry weight and development time in five species of Drosophila. J. Zool. Lond. 264, 87–95.
Sheeba V., Madhyastha N. A. A. and Joshi A. 1998 Oviposition preference for normal versus novel food resources in laboratory populations of Drosophila melanogaster. J. Biosci. 23, 93– 100.
Singh B. N. 2010 Drosophila ananassae: a good model species for genetical, behavioural and evolutionary studies. Ind. J. Exp. Biol. 48, 333–345.
Shiotsugu J., Leroi A. M., Yashiro H., Rose M. R. and Mueller L. D. 1997 The symmetry of correlated responses in adaptive evolution: an experimental study using Drosophila. Evolution 51, 163–172.
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.
StatSoft 1995 Statistica Vol. I: general conventions and statistics 1. StatSoft, Tulsa, USA.