Variation, Sex, and Social Cooperation: Molecular Population Genetics of the Social Amoeba

English version České info

Dictyostelium discoideum is a eukaryotic microbial model system for multicellular development, cell–cell signaling, and social behavior. Key models of social evolution require an understanding of genetic relationships between individuals across the genome or possibly at specific genes, but the nature of variation within D. discoideum is largely unknown. We re-sequenced 137 gene fragments in wild North American strains of D. discoideum and examined the levels and patterns of nucleotide variation in this social microbial species. We observe surprisingly low levels of nucleotide variation in D. discoideum across these strains, with a mean nucleotide diversity (π) of 0.08%, and no strong population stratification among North American strains. We also do not find any clear relationship between nucleotide divergence between strains and levels of social dominance and kin discrimination. Kin discrimination experiments, however, show that strains collected from the same location show greater ability to distinguish self from non-self than do strains from different geographic areas. This suggests that a greater ability to recognize self versus non-self may arise among strains that are more likely to encounter each other in nature, which would lead to preferential formation of fruiting bodies with clonemates and may prevent the evolution of cheating behaviors within D. discoideum populations. Finally, despite the fact that sex has rarely been observed in this species, we document a rapid decay of linkage disequilibrium between SNPs, the presence of recombinant genotypes among natural strains, and high estimates of the population recombination parameter ρ. The SNP data indicate that recombination is widespread within D. discoideum and that sex as a form of social interaction is likely to be an important aspect of the life cycle.

Vyšlo v časopise: Variation, Sex, and Social Cooperation: Molecular Population Genetics of the Social Amoeba. PLoS Genet 6(7): e32767. doi:10.1371/journal.pgen.1001013
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001013

Souhrn

Zdroje

1. HamiltonWD

1964 The genetical evolution of social behavior. J Theor Biol 7 1 52

2. MichodR

2007 Evolution of individuality during the transition from unicellular to multicellular life. Proc Natl Acad Sci USA 104 8613 8618

3. CrespiBJ

2001 The evolution of social behavior in microorganisms. Trends Ecol Evol 16 178 183

4. GriffinA

WestSA

2002 Kin selection: fact or fiction. Trends Ecol Evol 17 15 21

5. KessinRH

2001 Dictyostelium - Evolution, cell biology, and the development of multicellularity Cambridge, UK Cambridge Univ. Press

6. EichingerL

2005 The genome of the social amoeba Dictyostelium discoideum. Nature 435 43 57

7. ChisholmRL

FirtelRA

2004 Insights into morphogenesis from a simple developmental system. Nature Rev Mol, Cell Biol 5 531 541

8. FosterKR

FortunatoA

StrassmannJE

QuellerDC

2002 The costs and benefits of being a chimera. Proc Roy Soc London B 269 2357 2362

9. FosterKR

ShaulskyG

StrassmannJE

QuellerDC

ThompsonCRL

2004 Pleiotropy as a mechanism to stabilize cooperation. Nature 431 693 696

10. QuellerDC

PonteE

BozzaroS

StrassmannJE

2003 Single-gene greenbeard effects in the social amoeba, Dictyostelium discoideum. Science 299 105 106

11. SantorelliL

ThompsonC

VillegasE

SvetzJ

DinhC

2008 Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451 1107 1110

12. StrassmannJE

ZhuY

QuellerDC

2000 Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408 965 967

13. FortunatoA

StrassmannJE

Santorelli, LL

QuellerDC

2003 Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum. Mol Ecol 12 1031 1038

14. GilbertOM

FosterKR

MehdiabadiNJ

StrassmannJE

QuellerDC

2007 High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc Natl Acad Sci USA 104 8913 8917

15. OstrowskiEA

KatohM

ShaulskyG

QuellerDC

StrassmannJE

2008 Kin discrimination increases with genetic distance in a social amoeba. PLOS Biol 6 e287 doi:10.1371/journal.pbio.0060287

16. BenabentosR

HiroseS

SucgangR

CurkT

KatohM

2009 Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol 19 567 572

17. RaperKB

1984 The Dictyostelids Princeton, NJ Princeton University Press

18. WallaceMA

RaperKB

1979 Genetic exchanges in the macrocysts of Dictyostelium discoideum. J Gen Microbiol 113 327 337

19. ErdosGW

RaperKB

VogenLK

1973 Mating types and macrocyst formation in Dictyostelium discoideum. Proc Nat Acad Sci USA 70 1828 1830

20. FrancisD

1998 High frequency recombination during the sexual cycle of Dictyostelium discoideum. Genetics 148 1829 1832

21. International SNP Map Working Group 2001 A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409 928 933

22. CaicedoAL

WilliamsonSH

HernandezRD

BoykoA

Fledel-AlonA

2007 Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3 e163 doi:10.1371/journal.pgen.0030163

23. TajimaF

1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585 595

24. LêS

JosseJ

HussonF

2008 FactoMineR: An R package for multivariate analysis. J Stat Soft 25 5

25. WakeleyJ

1997 Using the variance of pairwise differences to estimate the recombination rate. Genet Res 69 45 48

26. McVeanG

AwadallaP

FearnheadP

2002 A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160 1231 1241

27. McConnellR

MiddlemistS

ScalaC

StrassmannJE

QuellerDC

2007 An unusually low microsatellite mutation rate in Dictyostelium discoideum, an organism with unusually abundant microsatellites. Genetics 177 1499 1507

28. BonnerJT

1982 Evolutionary strategies and developmental constraints in the cellular slime molds. Am Nat 119 530 552

29. KessinRH

GundersenGG

ZaydfudimV

GrimsonM

1996 How cellular slime molds evade nematodes. Proc Natl Acad Sci USA 93 4857 4861

30. SuthersHB

1985 Ground-feeding migratory songbirds as cellular slime mold distribution vectors. Oecologia 65 526 530

31. GilbertOM

QuellerDC

StrassmannJE

2009 Discovery of a large clonal patch of a social amoeba: Implications for social evolution. Mol Ecol 18 1273 1281

32. HussMJ

1989 Dispersal of cellular slime molds by two soil invertebrates. Mycologia 81 677 682

33. SmithMH

2004 Genotypic diversity and population structure in Dictyostelium discoideum. M.A. Thesis, Rice University, Houston, Texas

34. DawkinsR

1976 The Selfish Gene Oxford Oxford University Press

35. GardnerA

WestSA

2010 Greenbeards. Evolution 64 25 38

36. VosM

VelicerG

2009 Social conflict in centimeter- and global-scale populations of the bacterium Myxococcus xanthus. Curr Biol 19 1763 1767

37. LewisKE

O'DayDH

1994 Cannibalistic sexual phagocytosis in Dictyostelium discoideum is modulated by adenosine via an A2-like receptor. Cellular Signalling 6 217 222

38. RozenS

SkaletskyHJ

2000 Primer3 on the WWW for general users and for biologist programmers.

KrawetzS

MisenerS

Bioinformatics Methods and Protocols: Methods in Molecular Biology Totowa, NJ Humana Press

39. OlsenKM

CaicedoAL

PolatoN

McClungA

McCouchS

2006 Selection under domestication: Evidence for a sweep in the rice waxy genomic region. Genetics 173 975 983

40. WattersonGA

1975 On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7 256 276

41. TajimaF

1983 Evolutionary relationship of DNA sequences in finite populations. Genetics 105 437 460

42. HudsonRR

SlatkinM

MaddisonWP

1992 Estimation of levels of gene flow from DNA sequence data. Genetics 132 583 589

43. ThorntonK

2003 Libsequence: A C++ class library for evolutionary genetic analysis. Bionformatics 19 2325 2327

44. HillWG

RobertsonA

1968 Linkage disequilibrium in finite populations. Theor Appl Genet 38 226 231

45. FalushD

StephensM

PritchardJK

2003 Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164 1567 1587

46. EvannoG

RegnautS

GoudetJ

2005 Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol Ecol 14 2611 2620

47. FelsensteinJ

1989 PHYLIP – Phylogeny Inference Package (Version 3.2). Cladistics 5 164 166

48. KimuraM

1980 A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111 120

49. HudsonRR

KaplanN

1985 Statistical properties of the number of recombination events in the history of a sample. Genetics 111 147 164

50. RonaghiM

UhlenM

MyrenP

1998 A sequencing method based on real-time pyrophosphate. Science 281 363 365

51. QuellerDC

GoodnightKF

1989 Estimation of genetic relatedness using allozyme data. Evolution 43 258 275

52. SchultzBB

1985 Levene's test for relative variation. Sys Zool 34 449 456