Opposite environmental and genetic influences on body size in North American Drosophila pseudoobscura

BMC Evolutionary Biology

Nina Wedell¹  Tom A R Price²  Alastair J Wilson¹  Alison Skeats¹  Michelle L Taylor¹ 

[1] College of Life and Environmental Sciences, Biosciences, University of Exeter, Penryn Campus, Penryn TR10 9FE, Cornwall, UK;Institute of Integrative Biology, University of Liverpool, Crown Street, Liverpool L69 7ZB, UK

关键词: Drosophila pseudoobscura;    Selection;    Phenotypic plasticity;    Local selection;    Bergmann clines;    Temperature-size rule;   

Others  :  1158249
DOI  :  10.1186/s12862-015-0323-3

 received in 2014-11-28, accepted in 2015-02-24,  发布年份 2015

【 摘 要 】

Background

Populations of a species often differ in key traits. However, it is rarely known whether these differences are associated with genetic variation and evolved differences between populations, or are instead simply a plastic response to environmental differences experienced by the populations. Here we examine the interplay of plasticity and direct genetic control by investigating temperature-size relationships in populations of Drosophila pseudoobscura from North America. We used 27 isolines from three populations and exposed them to four temperature regimes (16°C, 20°C, 23°C, 26°C) to examine environmental, genetic and genotype-by-environment sources of variance in wing size.

Results

By far the largest contribution to variation in wing size came from rearing temperature, with the largest flies emerging from the coolest temperatures. However, we also found a genetic signature that was counter to this pattern as flies originating from the northern, cooler population were consistently smaller than conspecifics from more southern, warmer populations when reared under the same laboratory conditions.

Conclusions

We conclude that local selection on body size appears to be acting counter to the environmental effect of temperature. We find no evidence that local adaptation in phenotypic plasticity can explain this result, and suggest indirect selection on traits closely linked with body size, or patterns of chromosome inversion may instead be driving this relationship.

【 授权许可】

   
2015 Taylor et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

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【 参考文献 】

• [1]West-Eberhard MJ: Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 1989, 20:249-78.
• [2]Debat V, David P: Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 2001, 16:555-61.
• [3]Moczek AP, Sultan S, Foster S, Ledόn-Rettig C, Dworkin I, Nijhout HF, et al.: The role of developmental plasticity in evolutionary innovation. Proc R Soc Lond B 2011, 278:2705-13.
• [4]Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP: Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 2010, 25:459-67.
• [5]Agrawal AA: Phenotypic plasticity in the interactions and evolution of species. Science 2001, 294:321-6.
• [6]Bretman A, Gage MJG, Chapman T: Quick-change artists: male plastic behavioural responses to rivals. Trends Ecol Evol 2011, 26:467-73.
• [7]Ghalambor CK, McKay JK, Carroll SP, Reznick DN: Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 2007, 21:394-407.
• [8]Via S, Lande R: Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 1985, 39:505-22.
• [9]Brommer JE: Variation in plasticity of personality traits implies that the ranking of personality measures changes between environmental contexts: calculating the cross-environmental correlation. Behav Ecol Sociobiol 2013, 67:1709-18.
• [10]Candolin U, Wong B: Behavioural responses to a changing world. Oxford University Press, Oxford; 2012.
• [11]Dingemanse NJ, Wolf M: Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 2013, 85:1031-9.
• [12]Sevenster JG: Equations or organisms? A comment on Berrigan and Charnov. Oikos 1995, 73:405-7.
• [13]Forster J, Hirst AG, Atkinson D: How do organisms change size with changing environment? The importance of reproductive method and ontogenetic timing. Funct Ecol 2011, 25:1024-31.
• [14]Forster J, Hirst AG: The temperature-size rule emerges from ontogenetic differences between growth and development rates. Funct Ecol 2012, 26:483-92.
• [15]Machac A, Zrzavy J, Smrckova J, Storch D: Temperature dependence of evolutionary diversification: differences between two contrasting model taxa support the metabolic theory of ecology. J Evol Biol 2012, 25:2449-56.
• [16]Gotthard K, Nylin S: Adaptive plasticity and plasticity as an adaptation. A selective review in animal morphology and life history. Oikos 1995, 74:3-17.
• [17]Gilchrist GW, Huey RB, Balanya J, Pascual M, Serra L: A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura. Evolution 2004, 58:768-80.
• [18]Gilchrist GW, Huey RB: Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura. Integ Comp Biol 2004, 44:461-70.
• [19]Powell AM, Davis MD, Powell JR: Phenotypic plasticity across 50MY of evolution: Drosophila wing size and temperature. J Insect Physiol 2010, 56:380-2.
• [20]Blanckenhorn WU, Demont M: Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integ Comp Biol 2004, 44:413-24.
• [21]Kivela SM, Valimaki P, Carrasco D, Maenpaa MI, Oksanen J: Latitudinal insect body size clines revisited: a critical evaluation of the saw-toothed model. J Anim Ecol 2011, 80:1184-95.
• [22]Conover DO, Shultz ET: Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 1995, 10:248-52.
• [23]Kingsolver JG, Pfennig DW: Individual-level selection as a cause of Cope’s rule of phyletic size increase. Evolution 2004, 58:1608-12.
• [24]Andersson M: Sexual selection. Princeton University Press, NJ, US; 1994.
• [25]Coyne J, Bundgaard J, Prout T: Geographic variation of tolerance to environmental stress in Drosophila pseudoobscura. Am Nat 1983, 122:474-88.
• [26]Kellermann V, van Heerwaarden B, Sgro CM, Hoffmann AA: Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 2009, 325:1244-6.
• [27]Anderson WW: Genetic divergence in body size among experimental populations of Drosophila pseudoobscura kept at different temperatures. Evolution 1973, 27:278-84.
• [28]Matzke MA, Druger M: Divergence between two populations of Drosophila pseudoobscura. Evolution 1977, 31:597-602.
• [29]Price TAR, Bretman A, Gradilla AC, Reger J, Taylor ML, Giraldo-Perez P, et al.: Does polyandry control population sex ratio via regulation of a selfish gene? Proc R Soc Lond B 2014, 281:20133259.
• [30]Kraushaar U, Goudet J, Blanckenhorn WU: Geographical and altitudinal population genetic structure of two dung fly species with contrasting mobility and temperature preference. Heredity 2002, 89:99-106.
• [31]Gupta AP, Lewontin RC: A study of reaction norms in natural populations of Drosophila pseudoobscura. Evolution 1982, 36:934-48.
• [32]Sokoloff A: Geographic variation of quantitative characters in populations of Drosophila pseudoobscura. Evolution 1965, 19:300-10.
• [33]Sokoloff A: Morphological variation in natural and experimental populations of Drosophila pseudoobscura and Drosophila persimilis. Evolution 1966, 20:49-71.
• [34]Meisel RP, Schaeffer SW: Meiotic transmission of Drosophila pseudoobscura chromosomal arrangements. PLoS One 2007, 2:e530.
• [35]Herrera P, Taylor ML, Skeats A, Price TAR, Wedell N: Can patterns of chromosome inversions in Drosophila pseudoobscura predict polyandry across a geographical cline? Ecol Evol 2014, 4:3072-81.
• [36]David JR, Gibert P, Legout H, Petavy G, Capy P, Moreteau B: Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 2005, 94:3-12.
• [37]Griffiths JA, Schiffer M, Hoffmann AA: Clinal variation and laboratory adaptation in the rainforest species Drosophila birchii for stress resistance, wing size, wing shape and development time. J Evol Biol 2005, 18:213-22.
• [38]Hoffmann AA, Hallas R, Sinclair C, Mitrovski P: Levels of variation in stress resistance in Drosophila among strains, local populations, and geographic regions: patterns for desiccation, starvation, cold resistance, and associated traits. Evolution 2001, 55:1621-30.
• [39]Gebhardt MD, Anderson WW: Temperature related fertility selection on body size and the sex-ratio gene arrangement in Drosophila pseudoobscura. Gen Res 1993, 62:63-75.
• [40]Lynch M, Walsh B: Genetics and analysis of quantitative traits. Sinauer Associates, Inc, Massachusetts, USA; 1998.
• [41]Price TAR, Hoskyns RA, Rapley H, Evans J, Wedell N: Temperature effects on male fertility cannot explain the distribution of a selfish genetic element. Funct Ecol 2012, 26:657-65.
• [42]Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N: Remating in the laboratory reflects rates of polyandry in the wild. Anim Behav 2011, 82:1381-6.
• [43]National Climatic Data Centre (NOAA). [www.ncdc.noaa.gov/data-access/land-based-station-data]
• [44]Gilchrist AS, Partridge L: A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster. Genetics 1999, 153:1775-87.
• [45]Abramoff MD, Magalhaes PJ, Ram SJ: Image processing with Image J. Biophoton Int 2004, 11:36-42.
• [46]Wedell Polyandry Website. [http://biosciences.exeter.ac.uk/wedellpolyandry/]
• [47]ASREML. [http://www.vsni.co.uk/software/asreml/]