Abstract
There are many examples of adaptive molecular evolution in natural populations, but there is no existing method to verify which phenotypic changes were directly targeted by selection. The problem is that correlations between traits make it difficult to distinguish between direct and indirect selection. A phenotype is a direct target of selection when that trait in particular was shaped by selection to better perform a function. An indirect target of selection, also known as an evolutionary spandrel, is a phenotype that changes only because it is correlated with another trait under direct selection. Studies that mutate genes and examine the phenotypic consequences are increasingly common, and these experiments could estimate the mutational accessibility of the phenotypic changes that arise during an instance of adaptive molecular evolution. Under indirect selection, we expect phenotypes to evolve toward states that are more accessible by mutation (i.e., states with high mutational entropy). Deviation from this null expectation (evolution toward a phenotypic state rarely produced by mutation) would be compelling evidence of adaptation and could be used to distinguish direct selection from indirect selection on correlated traits. To be practical, this molecular test of adaptation requires phenotypic differences that are caused by changes in a small number of genes. These kinds of genetically-simple traits have been observed in many empirical studies of adaptive evolution. Here, we describe how to use mutational accessibility to separate spandrels from direct targets of selection and thus verify adaptive hypotheses for phenotypes that evolve by molecular changes at one or a few genes.
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References
Barros MP, Bechara E (2000) Luciferase and urate may act as antioxidant defenses in larval Pyrearinus termitilluminans (Elateridae: Coleoptera) during natural development and upon 20-hydroxyecdysone treatment. Photochem Photobiol 71:648–654
Bell G (2009) The oligogenic view of adaptation. Cold Spring Harb Symp Quant Biol 74:139–144. doi:10.1101/sqb.2009.74.003
Bloom JD, Arnold FH (2009) In the light of directed evolution: pathways of adaptive protein evolution. Proc Natl Acad Sci USA 106(Suppl 1):9995–10000. doi:10.1073/pnas.0901522106
Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178. doi:10.1038/nature02106
Bridgham JT, Ortlund EA, Thornton JW (2009) An epistatic ratchet constrains the direction of glucocorticoid receptor evolution. Nature 461:515–519. doi:10.1038/nature08249
Clark NL, Gasper J, Sekino M et al (2009) Coevolution of interacting fertilization proteins. Plos Genet 5:e1000570. doi:10.1371/journal.pgen.1000570
Colosimo PF, Hosemann KE, Balabhadra S et al (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307:1928–1933. doi:10.1126/science.1107239
Conte GL, Arnegard ME, Peichel CL, Schluter D (2012) The probability of genetic parallelism and convergence in natural populations. Proc Roy Soc Lond B 279:5039–5047. doi:10.1098/rspb.2012.2146
Cresko WA, Amores A, Wilson C et al (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci USA 101:6050–6055. doi:10.1073/pnas.0308479101
Crespi BJ (1990) Measuring the effect of natural-selection on phenotypic interaction systems. Am Nat 135:32–47
Dean AM, Thornton JW (2007) Mechanistic approaches to the study of evolution: the functional synthesis. Nat Rev Genet 8:675–688. doi:10.1038/nrg2160
Dobler S, Dalla S, Wagschal V, Agrawal AA (2012) Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase. Proc Natl Acad Sci USA 109:13040–13045. doi:10.2307/41685674?ref=no-x-route:9c57945a3d654bf0c27836b49e38d101
Feldman CR, Brodie ED, Pfrender ME (2012) Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes. Proc Natl Acad Sci 109:4556–4561. doi:10.1073/pnas.1113468109
Field SF, Matz MV (2010) Retracing evolution of red fluorescence in GFP-like proteins from faviina corals. Mol Biol Evol 27:225–233. doi:10.1093/molbev/msp230
Frankel N, Wang S, Stern DL (2012) Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution. Proc Natl Acad Sci USA 109:20975–20979. doi:10.1073/pnas.1207715109
Gallant JR, Imhoff VE, Martin A et al (2014) Ancient homology underlies adaptive mimetic diversity across butterflies. Nat Commun 5:4817. doi:10.1038/ncomms5817
Gertz J, Siggia ED, Cohen BA (2009) Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457:215–218. doi:10.1038/nature07521
Gillespie J (1984) Molecular evolution over the mutational landscape. Evolution 38:1116–1129
Gillespie J (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics 155:909–919
González C, Ray JCJ, Manhart M et al (2015) Stress-response balance drives the evolution of a network module and its host genome. Mol Syst Biol 11:827–827. doi:10.15252/msb.20156185
Gould SJ, Lewontin R (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc Roy Soc Lond B 205:581–598
Grafen A (1984) Natural selection, kin selection and group selection. In: Behavioural ecology: an evolutionary approach, pp 62–84
Harms MJ, Thornton JW (2013) Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nat Rev Genet 14:559–571. doi:10.1038/nrg3540
Hellberg ME, Dennis AB, Arbour-Reily P et al (2012) The tegula tango: a coevolutionary dance of interacting, positively selected sperm and egg proteins. Evolution 66:1681–1694. doi:10.1111/j.1558-5646.2011.01530.x
Hoekstra HE, Hirschmann RJ, Bundey RA et al (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101–104. doi:10.1126/science.1126121
Holder KK, Bull JJ (2001) Profiles of adaptation in two similar viruses. Genetics 159:1393–1404
Jiang P, Josue J, Li X et al (2012) Major taste loss in carnivorous mammals. Proc Natl Acad Sci USA 109:4956–4961. doi:10.1073/pnas.1118360109
Jiang P-P, Corbett-Detig RB, Hartl DL, Lozovsky ER (2013) Accessible mutational trajectories for the evolution of pyrimethamine resistance in the malaria parasite Plasmodium vivax. J Mol Evol 77:81–91. doi:10.1007/s00239-013-9582-z
Koufopanou V, Bell G (1991) Developmental mutants of volvox: does mutation recreate the patterns of phylogenetic diversity? Evolution 45:1806–1822
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution, pp 1210–1226
Lewontin RC (1978) Adaptation. Sci Am 239:212-8–220-222 passim
Linnen CR, Poh Y-P, Peterson BK et al (2013) Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339:1312–1316. doi:10.1126/science.1233213
Lunzer M, Miller SP, Felsheim R, Dean AM (2005) The biochemical architecture of an ancient adaptive landscape. Science 310:499–501. doi:10.1126/science.1115649
Manhart M, Morozov AV (2015) Protein folding and binding can emerge as evolutionary spandrels through structural coupling. Proc Natl Acad Sci 112:1797–1802. doi:10.1073/pnas.1415895112
Martin A, Orgogozo V (2013) The Loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67:1235–1250. doi:10.1111/evo.12081
Maynard Smith J (1978) Optimization theory in evolution. Ann Rev Ecol Syst 9:31–56
Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23:23–35
Mayr E (1983) How to carry out the adaptationist program? Am Nat 121:324–334
McDonald MJ, Gehrig SM, Meintjes PL et al (2009) Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183:1041–1053. doi:10.1534/genetics.109.107110
Musset L, Le Bras J, Clain J (2007) Parallel evolution of adaptive mutations in Plasmodium falciparum mitochondrial DNA during atovaquone-proguanil treatment. Mol Biol Evol 24:1582–1585. doi:10.1093/molbev/msm087
Nachman MW, Hoekstra HE, D’Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100:5268–5273. doi:10.1073/pnas.0431157100
Nielsen R (2009) Adaptionism-30 years after Gould and Lewontin. Evolution 63:2487–2490. doi:10.1111/j.1558-5646.2009.00799.x
O’Maille PE, Malone A, Dellas N et al (2008) Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases. Nat Chem Biol 4:617–623. doi:10.1038/nchembio.113
Orr HA, Coyne JA (1992) The genetics of adaptation: a reassessment. Am Nat 140:725–742. doi:10.1086/285437
Overstreet CM, Yuan TZ, Levin AM et al (2012) Self-made phage libraries with heterologous inserts in the Mtd of Bordetella bronchiseptica. Prot Eng Des Sel 25:145–151. doi:10.1093/protein/gzr068
Owen CR, Bradshaw H (2011) Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae). Arthropod-Plant Interactions, pp 1–10
Parichy DM, Johnson SL (2001) Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol 211:319–328
Pál G, Kouadio J-LK, Artis DR et al (2006) Comprehensive and quantitative mapping of energy landscapes for protein-protein interactions by rapid combinatorial scanning. J Biol Chem 281:22378–22385. doi:10.1074/jbc.M603826200
Pearson K (1903) Mathematical contributions to the theory of evolution. XI. On the influence of natural selection on the variability and correlation of organs. Philosophical Transactions of the Royal Society of London Series A, Containing Papers of a Mathematical or Physical Character 200:1–66
Rebeiz M, Pool JE, Kassner VA et al (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326:1663–1667. doi:10.1126/science.1178357
Reed RD, Papa R, Martin A et al (2011) optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137–1141. doi:10.1126/science.1208227
Rosenblum EB, Parent CE (2014) The molecular basis of phenotypic convergence. Ann Rev Ecol Evol Syst 45:203–226. doi:10.1146/annurev-ecolsys-120213-091851
Scott JK, Smith GP (1990) Searching for peptide ligands with an epitope library. Science 249:386–390
Shapiro MD, Marks ME, Peichel CL et al (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–723. doi:10.1038/nature02415
Shen Y-Y, Liang L, Li G-S et al (2012) Parallel evolution of auditory genes for echolocation in bats and toothed whales. Plos Genet 8:e1002788. doi:10.1371/journal.pgen.1002788.t001
Shoval O, Sheftel H, Shinar G et al (2012) Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space. Science 336:1157–1160. doi:10.1126/science.1217405
Springer S, Crespi BJ (2007) Adaptive gamete-recognition divergence in a hybridizing Mytilus population. Evolution 61:772–783. doi:10.1111/j.1558-5646.2007.00073.x
Springer S, Crespi BJ, Swanson WJ (2011) Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture. Mol Ecol 20:2240–2257. doi:10.1111/j.1365-294X.2011.05116.x
Springer S, Diaz SL, Gagneux P (2014) Parallel evolution of a self-signal: humans and new world monkeys independently lost the cell surface sugar Neu5Gc. Immunogenetics 66:671–674. doi:10.1007/s00251-014-0795-0
Stadler BM, Stadler PF, Wagner GP, Fontana W (2001) The topology of the possible: formal spaces underlying patterns of evolutionary change. J Theor Biol 213:241–274. doi:10.1006/jtbi.2001.2423
Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution 62:2155–2177. doi:10.1111/j.1558-5646.2008.00450.x
Stolz U, Velez S, Wood KV et al (2003) Darwinian natural selection for orange bioluminescent color in a Jamaican click beetle. Proc Natl Acad Sci USA 100:14955–14959. doi:10.1073/pnas.2432563100
Storz JF, Sabatino SJ, Hoffmann FG et al (2007) The molecular basis of high-altitude adaptation in deer mice. Plos Genet 3:e45. doi:10.1371/journal.pgen.0030045
Szendro IG, Franke J, de Visser JAGM, Krug J (2013) Predictability of evolution depends nonmonotonically on population size. Proc Natl Acad Sci USA 110:571–576. doi:10.1073/pnas.1213613110
Thompson JF, Geoghegan KF, Lloyd DB et al (1997) Mutation of a protease-sensitive region in firefly luciferase alters light emission properties. J Biol Chem 272:18766–18771. doi:10.1074/jbc.272.30.18766
Thorn KS, Bogan AA (2001) ASEdb: a database of alanine mutations and their effects on the free energy of binding in protein interactions. Bioinformatics 17:284–285
Tokuriki N, Stricher F, Schymkowitz J et al (2007) The stability effects of protein mutations appear to be universally distributed. J Mol Biol 369:1318–1332. doi:10.1016/j.jmb.2007.03.069
Wagner GP, Zhang J (2011) The pleiotropic structure of the genotype-phenotype map: the evolvability of complex organisms. Nat Rev Genet 12:204–213. doi:10.1038/nrg2949
Weinreich DM, Delaney NF, Depristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111–114. doi:10.1126/science.1123539
Weinreich DM, Watson RA, Chao L (2005) Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165–1174
Weiss GA, Watanabe CK, Zhong A et al (2000) Rapid mapping of protein functional epitopes by combinatorial alanine scanning. Proc Natl Acad Sci USA 97:8950–8954. doi:10.1073/pnas.160252097
Wells JA (1990) Additivity of mutational effects in proteins. Biochemistry 29:8509–8517
Wessinger CA, Rausher MD (2015) Ecological transition predictably associated with gene degeneration. Mol Biol Evol 32:347–354. doi:10.1093/molbev/msu298
Wichman HA, Badgett MR, Scott LA et al (1999) Different trajectories of parallel evolution during viral adaptation. Science 285:422–424
Williams GC (1966) Adaptation and natural selection. Princeton University Press
Wood KV, Lam YA, McElroy WD, Seliger HH (1989) Bioluminescent click beetles revisited. J Biolumin Chemilumin 4:31–39. doi:10.1002/bio.1170040110
Zhang J (2006) Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys. Nat Genet 38:819–823. doi:10.1038/ng1812
Zhen Y, Aardema ML, Medina EM et al (2012) Parallel molecular evolution in an herbivore community. Science 337:1634–1637. doi:10.1126/science.1226630
Zhu G, Golding GB, Dean AM (2005) The selective cause of an ancient adaptation. Science 307:1279–1282. doi:10.1126/science.1106974
Acknowledgements
SAS is grateful to WJ Swanson, J Tyerman, F Breden, and HD Bradshaw for helpful discussions. An NSERC PGSD International Graduate Fellowship to SAS supported this work. MM was supported by NIH grant F32 GM116217. AVM and SAS are grateful to Pierre Pontarotti for his extraordinary hospitality, which enabled the exchange of ideas that ultimately made this work possible.
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Springer, S.A., Manhart, M., Morozov, A.V. (2016). Separating Spandrels from Phenotypic Targets of Selection in Adaptive Molecular Evolution. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-41324-2_18
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