Rapid increase in viability due to new beneficial mutations in Drosophila melanogaster

Abstract

It is usually assumed that new beneficial mutations are extremely rare. Yet, few experiments have been performed in multicellular organisms that measure the effect of new beneficial mutations on viability and other measures of fitness. In most experiments, it is difficult to clearly distinguish whether adaptations have occurred due to selection on new beneficial mutations or on preexisting genetic variation. Using a modification of a Dobzhansky and Spassky (Evolution 1:191-216, 1947) assay to study change in viability over generations, we have observed an increase in viability in lines homozygous for the second and third chromosomes of Drosophila melanogaster in 6-26 generations due to the occurrence of new beneficial mutations in population sizes of 20, 100 and 1,000. The lines with the lowest initial viability responded the fastest to new beneficial mutations. These results show that new beneficial mutations, along with selection, can quickly increase viability and fitness even in small populations. Hence, new advantageous mutations may play an important role in adaptive evolution in higher organisms.

Adaptation of Drosophila melanogaster to increased NaCl concentration due to dominant beneficial mutations

“…In previous studies, D. melanogaster evolved to tolerate 5-7% NaCl (Wallace 1982;Frankham et al 1999;Azad and Woodruff 2007). This outcome provides experimental evidence that new beneficial mutations, along with selection, can allow a population to adapt quickly to novel stressful environments, suggesting that the influence of new beneficial mutations might be larger than usually assumed (Nei 2007;Peck 1994;Li 1997;Kondrashov 1998;Wolch et al 2001;Shaw et al 2000Shaw et al , 2002Joseph and Hall 2004;Orr 1998Orr , 2005aOrr , b, 2009Orr , 2010Pelz et al 2005;Lynch 2007;Azad et al 2010;Sniegowski and Gerrish 2010). This adaptive process may also be preceded by compensatory mutations and rare back mutations that may reduce the harmful effects of some mutations (Kimura 1985;Whitlock and Otto 1999;Estes and Lynch 2003;Kern and Kontrashov 2004;Charlesworth and Eyre-Walker 2007).…”

“…Drosophila stocks Two D. melanogaster stocks were used in this study: (1) yIB (yellow inbred flies marked with the yellow-body mutation (y, 1-0.0, cytological position 1A5), which had undergone single-pair sibling matings for 150-190 generations and was, therefore, homozygous (the homozygosity of the yIB stock was confirmed by microsatellite analysis, as discussed in Azad et al 2010); 2) w; Kr lf-1 /CyO; D/TM3, Ser that had phenotypic markers on the X, second, and third chromosomes (w = white, white eyes; 1-1.5, 3B6; Kr lf-1 = Kruppel, altered eye structure, 2-107.6, 60F5; Cy = Curly, curly wings, 2-6.1, 23A4-23B2; D = Dichaete, extended wings, 3-40.7, 70D3; and Ser = Serrate, wings with marginal excisions, 3-92.5, 97E6. CyO and TM3 are balancer chromosomes that contain multiple inversions (Lindsley and Zimm 1992).…”

“…Selection acting on standing genetic variation and on new mutations is responsible for adaptations to new environments. Yet, the magnitude of the role of preexisting variation vs. new mutations is unknown (Haldane 1932;Fisher 1930;Maynard Smith 1976;Hill 1982;Nei 2007;Gillespie 1991Gillespie , 2006Hartl and Taubes 1998;Orr 1998Orr , 2005aOrr , b, 2009Orr , 2010Orr and Betancourt 2001;Yedid and Bell 2002;Bull and Otto 2005;Rokyta et al 2005;Houle and Kondrashov 2006; Barrett and Schluter 2007;Lynch 2007;Brookfield 2009;Stoltzfus and Yampolsky 2009;Woodruff and Zhang 2009;Azad et al 2010;Lynch and Abegg 2010;Pritchard et al 2010 and references therein). To estimate the effect of mutation on adaptations, genetic variation in the founding populations should be eliminated by using homozygous isogenic stocks so that fitness changes and selection responses over generations can be attributed to new beneficial mutations (Knight and Robertson 1957;Hollingdale and Baker 1971;Caballero et al 1991;Hill and Caballero 1992;Mackay et al 1994;Bataillon 2000;Azad et al 2010).…”

“…Although it is usually argued that the rate of beneficial mutations is low, major adaptive changes can be caused by such mutations or by compensatory mutations (Dobzhansky and Spassy 1947;Kimura 1985;Phillips 1997;Kondrashov 1998;Whitlock and Otto 1999;Bataillon 2000;Shaw et al 2000Shaw et al , 2002Imhof and Schlotterer 2001;Zeyl and DeVisser 2001;Rozen et al 2002;Estes and Lynch 2003;Joseph and Hall 2004;Orr 1998Orr , 2005aOrr , b, 2009Orr , 2010Pelz et al 2005; Barrett et al 2006Barrett et al , 2007Betancourt and Bolback 2006;Gillespie 2006;Eyre-Walker and Keightley 2007;Silander et al 2007;Ferenci 2008;Bell and Gonzalez 2009;Barrick et al 2009;Bell and Gonzalez 2009;Stanek et al 2009;Azad et al 2010).…”

Fitness of Arabidopsis Thaliana Mutation Accumulation Lines Whose Spontaneous Mutations Are Known

“…Supporting the existence of an appreciable proportion of beneficial mutations, the five sequenced MA lines frequently outperformed the founder in five additional field trials under an array of conditions (Table 1). Others have recently detected high rates of beneficial mutations, up to 15% in viruses (Burch and Chao 1999, 2000; Silander et al 2007), up to 13% in yeast (Hall et al 2008, Hall and Joseph 2010), and a significant number in D. melanogaster (Azad et al 2010), counter to the view of Keightley and Lynch (2003).…”