Bias and Evolution of the Mutationally Accessible Phenotypic Space in a Developmental System
Genetic and developmental architecture may bias the mutationally available phenotypic spectrum. Although such asymmetries in the introduction of variation may influence possible evolutionary trajectories, we lack quantitative characterization of biases in mutationally inducible phenotypic variation, their genotype-dependence, and their underlying molecular and developmental causes. Here we quantify the mutationally accessible phenotypic spectrum of the vulval developmental system using mutation accumulation (MA) lines derived from four wild isolates of the nematodes Caenorhabditis elegans and C. briggsae. The results confirm that on average, spontaneous mutations degrade developmental precision, with MA lines showing a low, yet consistently increased, proportion of developmental defects and variants. This result indicates strong purifying selection acting to maintain an invariant vulval phenotype. Both developmental system and genotype significantly bias the spectrum of mutationally inducible phenotypic variants. First, irrespective of genotype, there is a developmental bias, such that certain phenotypic variants are commonly induced by MA, while others are very rarely or never induced. Second, we found that both the degree and spectrum of mutationally accessible phenotypic variation are genotype-dependent. Overall, C. briggsae MA lines exhibited a two-fold higher decline in precision than the C. elegans MA lines. Moreover, the propensity to generate specific developmental variants depended on the genetic background. We show that such genotype-specific developmental biases are likely due to cryptic quantitative variation in activities of underlying molecular cascades. This analysis allowed us to identify the mutationally most sensitive elements of the vulval developmental system, which may indicate axes of potential evolutionary variation. Consistent with this scenario, we found that evolutionary trends in the vulval system concern the phenotypic characters that are most easily affected by mutation. This study provides an empirical assessment of developmental bias and the evolution of mutationally accessible phenotypes and supports the notion that such bias may influence the directions of evolutionary change.
Vyšlo v časopise:
Bias and Evolution of the Mutationally Accessible Phenotypic Space in a Developmental System. PLoS Genet 6(3): e32767. doi:10.1371/journal.pgen.1000877
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000877
Souhrn
Genetic and developmental architecture may bias the mutationally available phenotypic spectrum. Although such asymmetries in the introduction of variation may influence possible evolutionary trajectories, we lack quantitative characterization of biases in mutationally inducible phenotypic variation, their genotype-dependence, and their underlying molecular and developmental causes. Here we quantify the mutationally accessible phenotypic spectrum of the vulval developmental system using mutation accumulation (MA) lines derived from four wild isolates of the nematodes Caenorhabditis elegans and C. briggsae. The results confirm that on average, spontaneous mutations degrade developmental precision, with MA lines showing a low, yet consistently increased, proportion of developmental defects and variants. This result indicates strong purifying selection acting to maintain an invariant vulval phenotype. Both developmental system and genotype significantly bias the spectrum of mutationally inducible phenotypic variants. First, irrespective of genotype, there is a developmental bias, such that certain phenotypic variants are commonly induced by MA, while others are very rarely or never induced. Second, we found that both the degree and spectrum of mutationally accessible phenotypic variation are genotype-dependent. Overall, C. briggsae MA lines exhibited a two-fold higher decline in precision than the C. elegans MA lines. Moreover, the propensity to generate specific developmental variants depended on the genetic background. We show that such genotype-specific developmental biases are likely due to cryptic quantitative variation in activities of underlying molecular cascades. This analysis allowed us to identify the mutationally most sensitive elements of the vulval developmental system, which may indicate axes of potential evolutionary variation. Consistent with this scenario, we found that evolutionary trends in the vulval system concern the phenotypic characters that are most easily affected by mutation. This study provides an empirical assessment of developmental bias and the evolution of mutationally accessible phenotypes and supports the notion that such bias may influence the directions of evolutionary change.
Zdroje
1. LynchM
2007 The evolution of genetic networks by non-adaptive processes. Nat Rev Genetics 8 803 813
2. LandeR
1980 Maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet Res 26 221 235
3. SteppanSJ
PhillipsPC
HouleD
2002 Comparative quantitative genetics: evolution of the G matrix. TREE 17 320 327
4. EstesS
PhillipsPC
2006 Variation in pleiotropy and the mutational underpinnings of the G-matrix. Evolution 60 2655 2660
5. KeightleyPD
Eyre-WalkerA
1999 Terumi Mukai and the riddle of deleterious mutation rates. Genetics 153 515 523
6. JonesAG
ArnoldSJ
BürgerR
2007 The mutation matrix and the evolution of evolvability. Evolution 61 727 745
7. JonesAG
ArnoldSJ
BuergerR
2003 Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution 57 1747 1760
8. BeginM
SchoenDJ
2007 Transposable elements, mutational correlations, and population divergence in Caenorhabditis elegans. Evolution 61 1062 1070
9. HouleD
HughesKA
HoffmasterDK
IharaJ
AssimacopolousS
1994 The effects of spontaneous mutation on quantitative traits. 1. Variances and covariances of life-history traits. Genetics 138 773 785
10. EstesS
AjieBC
LynchM
PhillipsPC
2005 Spontaneous mutational correlations for life-history, morphological and behavioral characters in Caenorhabditis elegans. Genetics 170 645 653
11. GouldSJ
1977 Ontogeny and Phylogeny. Cambridge, MA Belknap Press
12. Maynard SmithJ
BurianR
KauffmanS
AlberchP
CampbellJ
1985 Developmental constraints and evolution. Q Rev Biol 60 265 287
13. ArthurW
2004 Biased embryos and evolution. Cambridge Cambridge University Press
14. ThomsonKS
1985 Essay review: The relationship between development and evolution. Oxford Surveys in Evolutionary Biology 2 220 233
15. YampolskyLY
StoltzfusA
2001 Bias in the introduction of variation as an orienting factor in evolution. Evol Dev 3 73 83
16. ArthurW
2004 The effect of development on the direction of evolution: toward a twenty-first century consensus. Evol Dev 6 282 288
17. PsujekS
BeerRD
2008 Developmental bias in evolution: evolutionary accessibility of phenotypes in a model evo-devo system. Evol Dev 10 375 390
18. StoltzfusA
2006 Mutationism and the dual causation of evolutionary change. Evol Dev 8 304 317
19. StoltzfusA
YampolskyLY
2009 Climbing mount probable: mutation as a cause of nonrandomness in evolution. J Hered 100 637 647
20. SchluterD
1996 Adaptive radiation along genetic lines of least resistance. Evolution 50 1766 1774
21. SternDL
OrgogozoV
2009 Is genetic evolution predictable? Science 323 746 751
22. McDonaldMJ
GehrigSM
MeintjesPL
ZhangX-X
RaineyPB
2009 Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183 1041 1053
23. AlberchP
GaleE
1985 A developmental analysis of an evolutionary trend: Digital reduction in amphibians. Evolution 39 8 23
24. Dichtel-DanjoyM-L
FélixM-A
2004 Phenotypic neighborhood and micro-evolvability. TIG 20 268 276
25. BaerCF
ShawF
StedingC
BaumgartnerM
HawkinsA
2005 Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes. Proc Natl Acad Sci USA 102 5785 5790
26. WoodruffRC
ThompsonJN
SeegerMA
SpiveyWE
1984 Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster. Heredity 53 223 234
27. MukaiT
BabaM
AkiyamaM
UowakiN
KusakabeS
1985 Rapid change in mutation rate in a local population of Drosophila melanogaster. Proc Natl Acad Sci USA 82 7671 7675
28. BaerCF
PhillipsN
OstrowD
AvalosA
BlantonD
2006 Cumulative effects of spontaneous mutations for fitness in Caenorhabditis: role of genotype, environment and stress. Genetics 174 1387 1395
29. OstrowD
PhillipsN
AvalosA
BlantonD
BoggsA
2007 Mutational bias for body size in rhabditid nematodes. Genetics 176 1653 1661
30. PhillipsN
SalomonM
CusterA
OstrowD
BaerC
2009 Spontaneous Mutational and Standing Genetic (Co)variation at Dinucleotide Microsatellites in Caenorhabditis briggsae and Caenorhabditis elegans. Molecular Biology and Evolution 26
31. SternbergPW
2005 Vulval development. Wormbook. ed. The C. elegans Research Community. doi/10.1895/wormbook.1.6.1, http://www.wormbook.org
32. FélixM-A
WagnerA
2008 Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity 100 132 140
33. BraendleC
MillozJ
FélixM-A
2008 Mechanisms and evolution of environmental responses in Caenorhabditis elegans. Curr Topics Dev Biol 80 171 207
34. BraendleC
FélixM-A
2008 Plasticity and errors of a robust developmental system in different environments. Dev Cell 15 714 724
35. MillozJ
DuveauF
NuezI
FélixM-A
2008 Intraspecific evolution of the intercellular signaling network underlying a robust developmental system. Genes Dev 22 3064 3075
36. SulstonJE
WhiteJG
1980 Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev Biol 78 577 597
37. DelattreM
FélixM-A
2001 Polymorphism and evolution of vulval precursor cell lineages within two nematode genera, Caenorhabditis and Oscheius. Curr Biol 11 631 643
38. FélixM-A
2007 Cryptic quantitative evolution of the vulva intercellular signaling network in Caenorhabditis. Curr Biol 17 103 114
39. KiontkeK
BarrièreA
KolotuevI
PodbilewiczB
SommerRJ
2007 Trends, stasis and drift in the evolution of nematode vulva development. Curr Biol 17 1925 1937
40. VassilievaLL
LynchM
1999 The rate of spontaneous mutation for life-history traits in Caenorhabditis elegans. Genetics 151 119 129
41. YooAS
BaisC
GreenwaldI
2004 Crosstalk between the EGFR and LIN-12/Notch pathways in C. elegans vulval development. Science 303 663 666
42. AzevedoRBR
KeightleyPD
Laurén-MäättäC
VassilievaLL
LynchM
2002 Spontaneous mutational variation for body size in Caenorhabditis elegans. Genetics 162 755 765
43. DenverDR
MorrisK
LynchM
ThomasWK
2004 High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome. Nature 430 679 682
44. SternbergPW
HorvitzHR
1986 Pattern formation during vulval development in Caenorhabditis elegans. Cell 44 761 772
45. BaerCF
2008 Quantifying the decanalizing effects of spontaneous mutations in rhabditid nematodes. Am Nat 172 272 281
46. DworkinI
2005 Canalization, cryptic variation, and developmental buffering: a critical examination and analytical perspective.
HallgrimssonB
HallBK
Variation - A central concept in biology: Elsevier Inc 131 158
47. HouleD
MorikawaB
LynchM
1996 Comparing mutational variabilities. Genetics 143 1467 1483
48. SalomonMP
OstrowD
PhillipsN
BlantonD
BourW
2009 Comparing mutational and standing genetic variability for fitness and size in Caenorhabditis briggsae and C. elegans. Genetics 183 685 692
49. Joyner-MatosJ
UpadhyayA
SalomonMP
GrigaltchikV
BaerCF
2009 Genetic (Co)variation for life span in rhabditid nematodes: role of mutation, selection, and history. J Gerontol A Biol Sci Med Sci 1134 1145
50. SchmalhausenII
1949 Factors of Evolution: The Theory of Stabilizing Selection. Chicago Univ of Chicago Press
51. WagnerGP
BoothG
Bagheri-ChaichianH
1997 A population genetic theory of canalization. Evolution 51 329 347
52. BarrièreA
FélixM-A
2005 Natural variation and population genetics of C. elegans. Wormbook. ed. The C. elegans Research Community, doi/10.1895/wormbook.1.43.1, http://www.wormbook.org
53. EisenmannDM
MaloofJN
SimskeJS
KenyonC
KimSK
1998 The β-catenin homolog BAR-1 and LET-60 Ras coordinately regulate the Hox gene lin-39 during Caenorhabditis elegans vulval development. Development 125 3667 3680
54. GreenwaldIS
SternbergPW
HorvitzHR
1983 The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34 435 444
55. FondonJWI
GarnerHR
2004 Molecular origins of rapid and continuous morphological evolution. Proc Natl Acad Sci USA 101 18058 18063
56. FlattT
2005 The evolutionary genetics of canalization. Q Rev Biol 80 287 316
57. DolginES
FélixM-A
CutterAD
2008 Hakuna Nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity 100 304 315
58. DichtelM-L
Louvet-ValléeS
VineyME
FélixM-A
SternbergPW
2001 Control of vulval cell division number in the nematode Oscheius/Dolichorhabditis sp. CEW1. Genetics 157 183 197
59. WoodWB
1988 The nematode Caenorhabditis elegans. Cold Spring Harbor, New York Cold Spring Harbor Laboratory
60. CutterAD
FélixM-A
BarrièreA
CharlesworthD
2006 Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics 173 2021 2031
61. FergusonEL
SternbergPW
HorvitzHR
1987 A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans. Nature 326 259 267
62. WolfingerR
O'ConnellM
1993 Generalized linear mixed models: a pseudo-likelihood approach. Journal of Statistical Computation and Simulation 4 233 243
63. EfronB
TibshiraniRJ
1993 An introduction to the bootstrap. New York Chapman and Hall
64. LynchM
WalshB
1998 Genetics and analysis of quantitative traits: Sinauer Associates, Inc.
65. FalconerDS
1989 Introduction to Quantitative Genetics. New York John Wiley Sons
66. KnappSJ
BridgesWCJr
YangMH
1989 Nonparametric confidence interval estimators for heritability and expected selection response. Genetics 121 891 898
67. SokalRR
RohlfFJ
1981 Biometry, 3nd edition. New York W.H. Freeman and Cie
68. SulstonJ
HorvitzHR
1977 Postembryonic cell lineages of the nematode Caenorhabditis elegans. Dev Biol 56 110 156
69. InoueT
OzHS
WilandD
GharibS
DeshpandeR
2004 C. elegans LIN-18 is a Ryk ortholog and functions in parallel to LIN-17/Frizzled in Wnt signaling. Cell 118 795 806
70. FergusonE
HorvitzHR
1985 Identification and characterization of 22 genes that affect the vulval cell lineages of Caenorhabditis elegans. Genetics 110 17 72
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