The coevolution of cooperation and dispersal in social groups and its implications for the emergence of multicellularity

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  Hochberg, Michael E ^a,b,c   Rankin, Daniel J ^d   Taborsky, Michael ^d  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b SANTA FE INSTITUTE   (United States)

^c NATIONAL CENTER FOR ECOLOGICAL ANALYSIS AND SYNTHESIS   (United States)

^d UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOLOGY; CELL STRUCTURE; COEVOLUTION; COOPERATION; DISPERSION; GERM LINE; KIN SELECTION; LIFESTYLE; SOCIAL BEHAVIOR; BIOLOGICAL MODEL; EVOLUTION; GENETIC SELECTION; PHENOTYPE; POPULATION DYNAMICS;

COOPERATIVE BEHAVIOR; EVOLUTION; MODELS, GENETIC; PHENOTYPE; POPULATION DYNAMICS; SELECTION (GENETICS);

EID: 51649128132     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-238     Document Type: Article

References (210)

1. LW Buss, The Evolution of Individuality Princeton: Princeton University Press 1987
2. Cooperation and conflict in the evolution of individuality. II. Conflict mediation. RE Michod, Proc R Soc Lond B 1996 263 813 822 10.1098/rspb.1996.0121 8760489
3. Cooperation and conflict in the evolution of individuality. III. Transitions in the unit of fitness. RE Michod D Roze, Mathematical and Computational Biology: Computational Morphogenesis, Hierarchical Complexity, and Digital Evolution Providence: American Mathematical Society, Nehaniv CL, 1999 47 92
4. Cooperation and conflict in the evolution of individuality IV. Conflict mediation and evolvability in Volvox carteri. RE Michod AM Nedelcu D Roze, Biosystems 2003 69 95 114 10.1016/S0303-2647(02)00133-8 12689724
5. J Maynard Smith E Szathmary, The Major Transitions in Evolution New York: WH Freeman 1995
6. Size and complexity among multicellular organisms. G Bell AO Mooers, Biol J Linn Soc 1997 60 345 363 10.1111/j.1095-8312.1997.tb01500.x
7. The Origins of Multicellularity. JT Bonner, Integr Biol 1998 1 27 36 10.1002/(SICI)1520-6602(1998)1:1<27::AID-INBI4>3.0.CO;2-6
8. The evolution of multicellularity: A minor major transition. RK Grosberg RR Strathmann, Ann Rev Ecol Syst 2007 38 621 654 10.1146/annurev.ecolsys.36. 102403.114735
9. A twelve-step program for evolving multicellularity and a division of labor. DL Kirk, Bioessays 2005 27 299 310 10.1002/bies.20197 15714559
10. Relatedness and the fraternal major transitions. DC Queller, Phil Trans Roy Soc Lond B 2000 355 1647 1655 10.1098/rstb.2000.0727 11127911
11. Theory of group selection. DS Wilson, Proc Natl Acad Sci USA 1975 72 143 146 1054490 10.1073/pnas.72.1.143
12. The origin and early evolution of germ cells as illustrated in the Volvocales. G Bell, The Origin and Evolution of Sex New York: Liss, Halvorson H, Monroy A, 1985 221 56
13. An evolutionary scenario for the transition to undifferentiated multicellularity. T Pfeiffer S Bonhoeffer, Proc Natl Acad Sci USA 2003 100 1095 1098 12547910 10.1073/pnas.0335420100
14. The group covariance effect and fitness trade-offs during evolutionary transitions. RE Michod, Proc Natl Acad Sci USA 2006 103 9113 9117 16751277 10.1073/pnas.0601080103
15. R Michod, Darwinian Dynamics Princeton; Princeton University Press 1999
16. Cooperation and conflict during the origin of multicellularity. RE Michod, Genetic and Cultural Evolution of Cooperation Cambridge: MIT Press, Hammerstein P, 2003 261 307
17. Parasite diversity and the evolution of diploidy, multicellularity and anisogamy. LD Hurst, J theor Biol 1990 144 429 443 10.1016/S0022-5193(05)80085-2 2402151
18. Soma and germ: an experimental approach using Volvox. V Koufopanou G Bell, Proc R Soc London Ser B 1993 254 107 13 10.1098/rspb.1993.0134
19. Mutation and selection within the individual. SP Otto IM Hastings, Genetica 1998 102/103 507 24 10.1023/A:1017074823337 9766963
20. Host control of symbiont transmission: the separation of symbionts into germ and soma. SA Frank, Am Nat 1996 148 1113 1124 10.1086/285974
21. Integration of signaling information in controlling cell-fate decisions in Dictyostelium. RA Firtel, Genes and Development 1995 9 1427 1444 10.1101/gad.9.12.1427
22. Altruism, cheating, and anitcheater adaptations in cellular slime molds. RE Hudson JE Aukema C Rispe D Roze, Am Nat 2002 160 31 43 10.1086/340613 18707497
23. Pleiotropy as a mechanism to stabilize cooperation. KR Foster G Shaulsky JE Strassmann DC Queller CRL Thompson, Nature 2004 431 693 696 10.1038/nature02894 15470429
24. Natural chimerism in colonial urochordates. B Rinkevich, Journal of Experimental Marine Biology and Ecology 2005 322 93 109 10.1016/j.jembe.2005.02. 020
25. Breeder-helper conflict in a cichlid fish with broodcare helpers - an experimental analysis. M Taborsky, Behaviour 1985 95 45 75 10.1163/ 156853985X00046
26. Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. S Balshine-Earn FC Neat H Reid M Taborsky, Behavioral Ecology 1998 5 432 438 10.1093/beheco/9.5.432
27. Experimental manipulation of helping in a cooperative breeder: helpers 'pay to stay' by pre-emptive appeasement. R Bergmüller M Taborsky, Animal Behaviour 2005 69 19 28 10.1016/j.anbehav.2004.05.009
28. Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. R Bergmüller D Heg M Taborsky, Proc R Soc Lond B 2005 272 325 331 10.1098/rspb.2004.2960 15705559
29. Trade-offs between extraterritorial prospecting and helping in a cooperative mammal. AJ Young AA Carlson T Clutton-Brock, Animal Behaviour 2005 70 829 837 10.1016/j.anbehav.2005.01.019
30. When to parasitize? A dynamic optimization model of reproductive strategies in a cooperative breeder. E Skubic M Taborsky JM McNamara AI Houston, J theor Biol 2004 227 487 501 10.1016/j.jtbi.2003.11.021 15038984
31. Dispersal, eviction, and conflict in meerkats (Suricata suricatta): an evolutionarily stable strategy model. PA Stephens AF Russell AJ Young WJ Sutherland TH Clutton-Brock, Am Nat 2005 165 120 35 10.1086/426597 15729644
32. A dispersive morph in the naked mole-rat. MJ O'Riain JUM Jarvis CG Faulkes, Nature 1996 380 619 621 10.1038/380619a0 8602260
33. Morphological castes in a vertebrate. MJ O'Riain JUM Jarvis R Alexander R Buffenstein C Peeters, PNAS 2000 97 13194 13197 11087866 10.1073/pnas.97.24. 13194
34. Energetics reveals physiologically distinct castes in a eusocial mammal. M Scantlebury JR Speakman MK Oosthuizen TJ Roper NC Bennett, Nature 2006 440 795 797 10.1038/nature04578 16598257
35. Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: Two components to a lifetime of socially induced infertility. NC Bennett CG Faulkes AJ Molteno, Proc R Soc Lond B 1996 263 1599 1603 10.1098/rspb.1996.0234
36. Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. FM Clarke CC Faulkes, Animal Behaviour 2001 61 311 324 10.1006/anbe.2000.1573
37. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. GJ Velicer YTN Yu, Nature 2003 425 75 78 10.1038/nature01908 12955143
38. Tragedy of commons. G Hardin, Science 1968 162 1243 1248 10.1126/science.162.3859.1243
39. The tragedy of the commons in evolutionary biology. DJ Rankin K Bargum H Kokko, Trends Ecol Evol 2007 22 643 651 17981363
40. Kinship, recognition, disease, and intelligence: constraints of social evolution. WD Hamilton, Animal Societies: Theories and Facts Tokyo: Jpn Sci Soc, Ito J, Brown JL, Kikkawa K, 1987 81 102
41. A general model for kin selection. DC Queller, Evolution 1992 46 376 80 10.2307/2409858
42. SA Frank, Foundations of social evolution Princeton: Princeton University Press 1998
43. The evolution of reciprocal altruism. RL Trivers, Q Rev Biol 1971 46 35 57 10.1086/406755
44. Repression of competition and the evolution of cooperation. SA Frank, Evolution 2003 57 693 705 12778541
45. The unit of selection in viscous populations and the evolution of altruism. M van Baalen DA Rand, J theor Biol 1998 143 631 648 10.1006/jtbi.1998.0730
46. Cooperation and competition between relatives. SA West I Pen AS Griffin, Science 2002 296 72 75 10.1126/science.1065507 11935015
47. Graph topology plays a determinant role in the evolution of cooperation. FC Santos JF Rodrigues JM Pacheco, Proc Royal Soc London B 2006 273 51 55 10.1098/rspb.2005.3272
48. Do animals really recognize kin? A Grafen, Anim Behav 1990 39 42 54 10.1016/S0003-3472(05)80724-9
49. Socially mediation speciation. ME Hochberg B Sinervo SP Brown, Evolution 2003 57 154 158 12643576
50. Altruism via kin-selection strategies that rely on arbitrary tags with which they co-evolve. R Axelrod RA Hammond A Grafen, Evolution 2004 58 1833 48 15446434
51. The evolution of social behavior in microorganism. BJ Crespi, Trends Ecol Evol 2001 16 178 83 10.1016/S0169-5347(01)02115-2 11245940
52. The evolution of cooperation. J Sachs IG Mueller TP Wilcox JJ Bull, Q Rev Biol 2004 79 135 60 10.1086/383541 15232949
53. The evolution of cooperation and altruism - a general framework and a classification of models. L Lehmann L Keller, J Evol Biol 2006 19 1365 1376 10.1111/j.1420-9101.2006.01119.x 16910958
54. Evolutionary explanations for cooperation. SA West AS Griffin A Gardner, Current Biology 2007 17 R661 R672 10.1016/j.cub.2007.06.004 17714660
55. How many kinds of individuals are there? B Santelices, Trends Ecol Evol 1999 14 152 155 10.1016/S0169-5347(98)01519-5 10322523
56. The origin of metazoan complexity: Porifera as integrated animals. WEG Müller, Integrative and Comparative Biology 2003 43 3 10 10.1093/icb/43.1.3
57. The costs and benefits of being a chimera. KR Foster A Fortunato JE Strassmann DC Queller, Proc R Soc London Ser B 2002 269 2357 62 10.1098/rspb.2002.2163
58. Reviving the superorganism. DS Wilson E Sober, J theor Biol 1989 136 337 356 10.1016/S0022-5193(89)80169-9 2811397
59. The relation between multilocus population genetics and social evolution theory. A Gardner SA West NH Barton, Am Nat 2007 169 207 226 10.1086/510602 17211805
60. L Keller Ed, Levels of Selection in Evolution Princeton; Princeton University Press 1999
61. Cooperation and conflict in social groups: insights from geographic variation. S Helms Cahan, Anim Behav 2001 61 819 825 10.1006/anbe.2000.1671
62. How to make a kin selection model. PD Taylor SA Frank, J theor Biol 1996 180 27 37 10.1006/jtbi.1996.0075 8763356
63. Social trajectories and the evolution of social behavior. S Helms Cahan DT Blumstein L Sundstrom J Liebig A Griffin, Oikos 2002 96 206 216 10.1034/j.1600-0706.2002.960202.x
64. Evolutionary strategies and developmental constraints in the cellular slime molds. JT Bonner, American Naturalist 1982 119 530 552 10.1086/283930
65. A life-history approach to group living and social contracts between individuals. P Nonacs, Ann Zool Fenn 2001 38 239 254
66. The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. M Taborsky, J Heredity 2001 92 100 110 10.1093/jhered/92.2. 100
67. DA Roff, The Evolution of Life Histories New York: Chapman & Hall 1992
68. Physiology and ecology of dispersal polymorphism in insects. AJ Zera RF Denno, Ann Rev Entom 1997 42 207 230 10.1146/annurev.ento.42.1.207 15012313
69. The physiology of life history trade-offs in animals. AJ Zera LG Harshman, Ann Rev Ecol Syst 2001 32 95 126 10.1146/annurev.ecolsys.32.081501. 114006
70. Intermediary metabolism and life-history trade-offs: Differential metabolism of amino acids underlies the dispersal-reproduction trade-off in a wing-polymorphic cricket. AJ Zera ZW Zhao, Am Nat 2006 167 889 900 10.1086/503578
71. A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. GA Langellotto RF Denno JR Ott, Ecology 2000 81 865 875
72. Evolutionary trade-offs between reproduction and dispersal in populations at expanding range boundaries. CL Hughes JK Hill C Dytham, Proc R Soc Lond B 2003 270 S147 S150 10.1098/rsbl.2003.0049
73. Kin selection and virulence in the evolution of protocells and parasites. SA Frank, Proc R Soc Lond B 1994 258 153 161 10.1098/rspb.1994.0156
74. The kin composition of social groups: Trading group size for degree of altruism. L Avilés JA Fletcher AD Cutter, Am Nat 2004 164 132 144 10.1086/422263 15278839
75. Behavioral ecology - Breeding together: Kin selection and mutualism in cooperative vertebrates. TH Clutton-Brock, Science 2002 296 69 72 10.1126/science.296.5565.69 11935014
76. Demography, altruism, and the benefits of budding. A Gardner SA West, J Evol Biol 2006 19 1707 1716 10.1111/j.1420-9101.2006.01104.x 16911000
77. Evolutionary progress and the levels of selection. J Maynard Smith, Evolutionary Progress Chicago: University of Chicago Press, Nitecki MH, 1989 219 230
78. LA Dugatkin, Cooperation Among Animals an Evolutionary Perspective Oxford: Oxford University Press 1997
79. Evolution of cooperation and conflict in experimental bacterial populations. PB Rainey K Rainey, Nature 2003 425 72 74 10.1038/nature01906 12955142
80. Character displacement promotes cooperation in bacterial biofilms. MA Brockhurst ME Hochberg T Bell A Buckling, Current Biology 2006 16 2030 2034 10.1016/j.cub.2006.08.068 17055982
81. Dispersal in stable habitats. WD Hamilton RM May, Nature 1977 269 578 581 10.1038/269578a0
82. Dispersal polymorphisms in subdivided populations. SA Frank, J theor Biol 1986 122 303 309 10.1016/S0022-5193(86)80122-9 3626575
83. The genetical evolution of social behavior, I & II. WD Hamilton, J theor Biol 1964 1 1 52 10.1016/0022-5193(64)90038-4
84. Group selection and kin selection: Two concepts but one process. L Lehmann L Keller S West D Roze, Proc Natl Acad Sci USA 2007 104 6736 6739 17416674 10.1073/pnas.0700662104
85. Altruism in viscous populations - an inclusive fitness model. PD Taylor, Evol Ecol 1992 6 352 356 10.1007/BF02270971
86. Host-symbiont conflict over the mixing of symbiotic lineages. SA Frank, Proc R Soc Lond B 1996 263 339 344 10.1098/rspb.1996.0052
87. Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. P Dierkes M Taborsky U Kohler, Behav Ecol 1999 10 510 515 10.1093/beheco/10.5.510
88. Punishment allows the evolution of cooperation (or anything else) in sizable groups. R Boyd PJ Richerson, Ethol Sociobiol 1992 13 171 195 10.1016/0162-3095(92)90032-Y
89. Bacterial biofilms: From the natural environment to infectious diseases. L Hall-Stoodley JW Costerton P Stoodley, Nature Reviews Microbiology 2004 2 95 108 10.1038/nrmicro821 15040259
90. Cooperation and conflict in microbial biofilms. JB Xavier KR Foster, Proc Natl Acad Sci USA 2007 104 876 881 17210916 10.1073/pnas.0607651104
91. Variation in individual investment strategies among social animals. J Komdeur, Ethology 2006 112 729 747 10.1111/j.1439-0310.2006.01243.x
92. Altruism and related phenomena mainly in the social insects. WD Hamilton, Ann Rev Ecol Syst 1972 3 193 232 10.1146/annurev.es.03.110172.001205
93. Evolution of dispersal and life history strategies - Tetrahymena ciliates. EJ Fjerdingstad N Schtickzelle P Manhes A Gutierrez J Clobert, BMC Evolutionary Biology 2007 7 133 17683620 10.1186/1471-2148-7-133
94. Unrelated helpers will not fully compensate for costs imposed on breeders when they pay to stay. IM Hamilton M Taborsky, Proc R Soc Lond B 2005 272 445 454 10.1098/rspb.2004.2961
95. Contingent movement and cooperation evolve under generalized reciprocity. IM Hamilton M Taborsky, Proc R Soc Lond B 2005 272 2259 2267 10.1098/rspb.2005.3248
96. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. GJ Velicer L Kroos RE Lenski, PNAS 1998 95 12376 12380 9770494 10.1073/pnas.95.21.12376
97. Altruism and social cheating in the social amoeba Dictyostelium discoideum. JE Strassmann Y Zhu DC Queller, Nature 2000 408 965 967 10.1038/35050087 11140681
98. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. O Gilbert KR Foster NJ Mehdiabadi JE Strassmann DC Queller, Proceedings of the National Academy of Sciences 2007 104 8913 8917 10.1073/pnas.0702723104
99. Costs and benefits of genetic heterogeneity within organisms. M Pineda-Krch K Lehtilä J Evol Biol 2004 17 1167 77 10.1111/j.1420-9101.2004. 00808.x 15525396
100. The robustness of Hamilton's rule with inbreeding and dominance: kin selection and fixation probabilities under partial sibmating. D Roze F Rousset, The American Naturalist 2004 164 214 231 10.1086/422202 15278845
101. The evolution of parasite dispersal, transmission, and virulence in spatial host populations. M Kamo M Boots, Evol Ecol Res 2006 8 1333 1347
102. PW Ewald, Evolution of Infectious Disease Oxford: Oxford University Press 1994
103. Models of parasite virulence. SA Frank, Q Rev Biol 1996 71 37 78 10.1086/419267 8919665
104. The spatial spread of altruism versus the evolutionary response of egoists. JC Koella, Proc R Soc Lond B 2000 267 1979 1985 10.1098/rspb.2000.1239
105. A mechanism for the evolution of altruism among nonkin: Positive assortment through environmental feedback. JW Pepper BB Smuts, Am Nat 2002 160 205 213 10.1086/341018 18707487
106. Group selection and assortative interactions. DS Wilson LA Dugatkin, Am Nat 1997 149 336 351 10.1086/285993
107. Know when to walk away: contingent movement and the evolution of cooperation. CA Aktipis, J theor Biol 2004 231 249 260 10.1016/j.jtbi.2004.06. 020 15380389
108. Adaptive evolution of social traits: Origin, trajectories, and correlations of altruism and mobility. J-F Le Galliard R Ferrière U Dieckmann, Am Nat 2005 165 206 224 10.1086/427090 15729651
109. Seeking the ultimate and proximate causes of Volvox multicellularity and cellular differentiation. DL Kirk, Integrative and Comparative Biology 2003 43 247 253 10.1093/icb/43.2.247
110. Unity from conflict. PB Rainey, Nature 2007 446 616 10.1038/446616a 17410161
111. Sex and the evolution of intrahost competition in RNA virus 6. PE Turner L Chao, Genetics 1998 150 523 532 9755186
112. Escape from prisoner's dilemma in RNA phage 6. PE Turner L Chao, American Naturalist 2003 161 497 505 10.1086/367880 12699226
113. Structured habitats and the evolution of anticompetitor toxins in bacteria. L Chao BR Levin, Proc Natl Acad Sci USA 1981 78 6324 6328 7031647 10.1073/pnas.78.10.6324
114. Bacteriocins: evolution, ecology and application. MA Riley JE Wertz, Annual Review of Microbiology 2002 56 117 137 10.1146/annurev.micro.56.012302. 161024 12142491
115. The phenotypic and fitness effects of colicin resistance in Escherichia coli K-12. M Feldgarden MA Riley, Evolution 1999 53 1019 1027 10.2307/2640807
116. Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. M Klausen M Gjermansen JU Kreft T Tolker-Nielsen, Fems Microbiology Letters 2006 261 1 11 10.1111/j.1574-6968.2006.00280.x 16842351
117. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. mutational origins of wrinkly spreader diversity. E Bantinaki R Kassen CG Knight Z Robinson AJ Spiers PB Rainey, Genetics 2007 176 441 453 17339222 10.1534/genetics.106.069906
118. Gliding motility in bacteria: insights from studies of Myxococcus xanthus. AM Spormann, Microbiol Mol Biol Rev 1999 63 621 641 10477310
119. Exploitative and hierarchical antagonism in a cooperative bacterium. F Fiegna GJ Velicer, Plos Biology 2005 3 1980 1987 10.1371/journal.pbio.0030370
120. Evolution of an obligate social cheater to a superior cooperator. F Fiegna YTN Yu SV Kadam GJ Velicer, Nature 2006 441 310 314 10.1038/nature04677 16710413
121. Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. M Vos GJ Velicer, Applied and Environmental Microbiology 2006 72 3615 3625 10.1128/AEM.72.5.3615-3625.2006
122. Immunity to K1 killer toxin: internal TOK1 blockade. F Sesti TM Shih N Nikolaeva SA Goldstein, Cell 2001 105 637 644 10.1016/S0092-8674(01)00376-2 11389833
123. The Prisoner's Dilemma and polymorphism in yeast SUC genes. D Greig M Travisano, Proceedings of the Royal Society of London B 2004 271 S25 S26 10.1098/rsbl.2003.0083 15101409
124. The prisoner's dilemma and polymorphism in yeast SUC genes. D Greig M Travisano, Proc R Soc Lond B 2004 271 S25 S26 10.1098/rsbl.2003.0083 15101409
125. Resource competition and social conflict in experimental populations of yeast. RC MacLean I Gudelj, Nature 2006 441 498 501 10.1038/nature04624 16724064
126. Heterocytosis in cellular slime molds. MF Filosa, American Naturalist 1962 96 73 91
127. Somatic cell parasitism and the evolution of somatic tissue compatibility. LW Buss, Proceedings of the National Academy of Sciences of the United States of America-Biological Sciences 1982 79 5337 5341 10.1073/pnas.79.17.5337
128. Developmental cheating and the evolutionary biology of Dictyostelium and Myxococcus. DN Dao RH Kessin HL Ennis, Microbiology-Uk 2000 146 1505 1512
129. Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. HL Ennis DN Dao SU Pukatzki RH Kessin, Proceedings of the National Academy of Sciences of the United States of America 2000 97 3292 3297 10725352 10.1073/pnas.050005097
130. Fruiting body architecture, spore capsule contents, selfishness, and heterocytosis in the cellular slime mold Dictyostelium discoideum. JA Hilson SA Kolmes LF Nellis, EtholEcolEvol 1994 6 529 535
131. Co-occurrence in nature of different clones of the social amoeba, Dictyostelium discoideum. A Fortunato JE Strassmann L Santorelli DC Queller, Molecular Ecology 2003 12 1031 1038 10.1046/j.1365-294X.2003.01792.x 12753221
132. Cooperation and conflict in the social amoeba, Dictyostelium discoideum. DC Queller KR Foster A Fortunato JE Strassmann T Kikuchi T Kubo S Higashi, Social insects and sociogenetics Sapporo: Hokkaido University Press 2003 173 200
133. A cost to chimerism in Dictyostelium discoideum on natural substrates. DI Castillo GT Switz KR Foster DC Queller JE Strassmann, Evolutionary Ecology Research 2005 7 263 271
134. Exploiting new terrain: an advantage to sociality in the slime mold Dictyostelium discoideum. JJ Kuzdzal-Fick KR Foster DC Queller JE Strassmann, Behavioral Ecology 2007 18 433 437 10.1093/beheco/arl102
135. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. LA Santorelli CRL Thompson e Villegas J Svetz C Dinh A Parikh R Sucgang A Kuspal JE Strassmann DC Queller G Shaulsky, Nature 2008 doi:10.1038/nature06558 18272966
136. Sexual differentiation in Volvox aureus. WH Darden, Journal of Protozoology 1966 13 239 255 5953846
137. The ontogeny and phylogeny of cellular differentiation in Volvox. DL Kirk, Trends in Genetics 1988 4 32 36 10.1016/0168-9525(88)90063-7 3072717
138. The genetic program for germ-soma differentiation in Volvox. DL Kirk, Annual Review of Genetics 1997 31 359 380 10.1146/annurev.genet.31.1.359 9442900
139. Seeking the ultimate and proximate causes of Volvox multicellularity and cellular differentiation. DL Kirk, Integrative and Comparative Biology 2003 43 247 253 10.1093/icb/43.2.247
140. The evolution of soma in the Volvocales. V Koufopanou, American Naturalist 1994 143 907 931 10.1086/285639
141. A review on the evolution of development in Volvox: morphological and physiological aspects. AG Desnitski, European Journal of Protistology 1995 31 241 247
142. The evolutionary origin of an altruistic gene. AM Nedelcu RE Michod, Molecular Biology and Evolution 2006 23 1460 1464 10.1093/molbev/msl016
143. A hydrodynamics approach to the evolution of multicellularity: Flagellar motility and germ-soma differentiation in volvocalean green algae. CA Solari JO Kessler RE Michod, American Naturalist 2006 167 537 554 10.1086/501031 16670996
144. Evolution of individuality during the transition from unicellular to multicellular life. RE Michod, Proceedings of the National Academy of Sciences of the United States of America 2007 104 8613 8618 17494748 10.1073/pnas. 0701489104
145. Life-history and ultrastructure of a new marine species of Proterospongia (Choanoflagellida). BSC Leadbeater, Journal of the Marine Biological Association of the United Kingdom 1983 63 135 160
146. Redox control and the evolution of multicellularity. NW Blackstone, Bioessays 2000 22 947 953 10.1002/1521-1878(200010)22:10<947::AID- BIES10>CO;2-W 10984721
147. Choanoflagellates, choanocytes, and animal multicellularity. M Maldonado, Invertebrate Biology 2004 123 1 22
148. Lehrbuch der speziellen Zoologie; Wirbellose. A Kaestner, Stuttgart: Fischer Verlag 1969 1
149. The amoeboid movement of dissociated sponge cells. PS Galtsoff, Biological Bulletin 1923 45 153 161 10.2307/1536625
150. Sponge aggregation: model for studies on cell-cell interactions. WJ Kuhns G Weinbaum R Turner MM Burger, Annals of the New York Academy of Sciences 1974 234 58 74 10.1111/j.1749-6632.1974.tb53021.x 4528735
151. The cell biology of sponges. TL Simpson, New York: Springer 1984
152. Sexual reproduction in Chondrilla australiensis (Porifera: demospongiae). KM Usher DC Sutton S Toze J Kuo J Fromont, Marine and Freshwater Research 2004 55 123 134 10.1071/MF03058
153. Sponge development and antiquity of animal pattern formation. BM Degnan SP Leys C Larroux, Integrative and Comparative Biology 2005 45 335 341 10.1093/icb/45.2.335
154. Mode of reproduction, recruitment, and genetic subdivision in the brooding sponge Haliclona sp. S Whalan MS Johnson E Harvey C Battershill, Marine Biology 2005 146 425 433 10.1007/s00227-004-1466-8
155. Two different evolutionary origins of stem cell systems and their molecular basis. K Agata E Nakajima N Funayama N Shibata YUY Saito, Seminars in Cell & Developmental Biology 2006 17 503 509 10.1016/j.semcdb.2006.05.004 16807003
156. Experimentelle untersuchungen uber stockentwicklung, polypendifferenzierung und sexualchimaren bei Hydractinia echinata. W Müller, Roux' Archiv fur Ent 1964 155 181 268 10.1007/BF00573905
157. Hydroid allorecognition regulates competition at both the level of the colony and the level of the cell lineage. LW Buss MA Shenk JJ Marchalonis C Reinish, Defense molecules New York: Liss 1990 85 105
158. Ontogenetic changes in fusibility in the colonial hydroid Hydractinia symbiolongicarpus. MA Shenk LW Buss, J Exp Zool 1991 257 80 86 10.1002/jez.1402570111
159. Evolutionary genetics of allorecognition in the colonial marine hydroid Hydractinia symbiolongicarpus. RK Grosberg DR Levitan BB Cameron, Evolution 1996 50 2221 2240 10.2307/2410693
160. Developmental insights into the origin of complex colonial Hydrozoans. P Cartwright, Integr Comp Biol 2003 43 82 86 10.1093/icb/43.1.82
161. Social organization within clones of sea-anemone Anthopleura elegantissima. L Francis, Biological Bulletin 1976 150 361 376 10.2307/1540678
162. Behind anemone lines: factors affecting division of labour in the social cnidarian Anthopleura elegantissima. DJ Ayre RK Grosberg, Animal Behaviour 2005 70 97 110 10.1016/j.anbehav.2004.08.022
163. Zur kenntnis des Polymorphismus der Bryozoen. Die avicularien der Cheilostomata Anasca. L Silen, Zool Bidr Upps 1938 17 149 366
164. Polymorphism. L Silen RM Woollacott RL Zimmer, Biology of Bryozoans New York: Academic Press 1977 183 231
165. British Anascan Bryozoans. JS Ryland PJ Hayward, London: Academic Press 1977 412145
166. The evolution of polymorphism in colonial invertebrates and social insects. CD Harvell, Quarterly Review of Biology 1994 69 155 185 10.1086/418538
167. Sexual differentiation and germ cell transfer in the colonial ascidian Botryllus schlosseri. A Sabbadin G Zaniolo, J Exp Zool 1979 207 289 304 10.1002/jez.1402070212
168. Coexistence and possible parasitism of somatic and germ-cell lines in chimeras of the colonial urochordate Botryllus schlosseri. Z Pancer H Gershon B Rinkevich, Biological Bulletin 1995 189 106 112 10.2307/1542460
169. Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. DS Stoner B Rinkevich IL Weissman, Proceedings of the National Academy of Sciences of the United States of America 1999 96 9148 9153 10430910 10.1073/pnas.96.16.9148
170. Environmental split between germ cell parasitism and somatic cell synergism in chimeras of a colonial urochordate. B Rinkevich I Yankelevich, The Journal of Experimental Biology 2004 207 3531 3536 10.1242/jeb.01184 15339949
171. Evidence for sperm dysfunction as mechanism of segretation distortion in Drosophila melanogaster. DL Hartl Y Hiraizumi JF Crow, Proceedings of the National Academy of Sciences of the United States of America 1967 58 2240 2245 5242201 10.1073/pnas.58.6.2240
172. Suppressor systems of segregation distorter (SD) chromosomes in natural populations of Drosophila melanogaster. Y Hiraizumi AM Thomas, Genetics 1984 106 279 292 17246192
173. Truncated RanGAP encoded by the segregation distorter locus of Drosophila. C Merrill L Bayraktaroglu A Kusano B Ganetzky, Science 1999 283 1742 1745 10.1126/science.283.5408.1742 10073941
174. The sex-ratio trait in Drosophila simulans: Geographical distribution of distortion and resistance. A Atlan H Mercot C Landre C Montchamp-Moreau, Evolution 1997 51 1886 1895 10.2307/2411010
175. Mouse T-haplotypes. LM Silver, Annual Review of Genetics 1985 19 179 208 3909941
176. The influence of genetic background and the homologous chromosome-17 on T-haplotype transmission ratio distortion in mice. GR Gummere PJ McCormick D Bennett, Genetics 1986 114 235 245 3770466
177. Putting the brake on drive: meiotic drive of t haplotypes in natural populations of mice. KG Ardlie, Trends in Genetics 1998 14 189 193 10.1016/S0168-9525(98)01455-3 9613203
178. Help or disperse? Cooperation in termites influenced by food conditions. J Korb S Schmidinger, Behavioral Ecology and Sociobiology 2004 56 89 95 10.1007/s00265-004-0757-x
179. Evolution of eusociality and the soldier caste in termites: a validation of the intrinsic benefit hypothesis. EA Roux J Korb, Journal of Evolutionary Biology 2004 17 869 875 10.1111/j.1420-9101.2004.00727.x 15271087
180. Eusociality in Australian gall thrips. BJ Crespi, Nature 1992 359 724 726 10.1038/359724a0
181. High relatedness and inbreeding in two species of haplodiploid eusocial thrips (Insecta: Thysanoptera) revealed by microsatellite analysis. TW Chapman B Crespi, Behavioral Ecology and Sociobiology 1998 43 301 306 10.1007/s002650050495
182. High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips. TW Chapman BJ Crespi BD Kranz MP Schwarz, Proceedings of the National Academy of Sciences of the United States of America 2000 97 1648 1650 10660681 10.1073/pnas.020510097
183. The evolution of soldier reproduction in social thrips. TW Chapman BD Kranz KL Bejah DC Morris MP Schwarz BJ Crespi, Behavioral Ecology 2002 13 519 525 10.1093/beheco/13.4.519
184. Reproductive division of labour coevolves with gall size in Australian thrips with soldiers. TE Wills TW Chapman BD Kranz MP Schwarz, Naturwissenschaften 2001 88 526 529 10.1007/s00114-001-0273-z 11824226
185. WA Foster, Behavioral Ecology and Sociobiology 1990 27 421 430 10.1007/BF00164069
186. The evolution of soldiers in aphids. DL Stern WA Foster, Biological Reviews of the Cambridge Philosophical Society 1996 71 27 79 10.1111/j.1469-185X.1996.tb00741.x 8603120
187. Genetic conflict and conditional altruism in social aphid colonies. P Abbot JH Withgott NA Moran, Proceedings of the National Academy of Sciences of the United States of America 2001 98 12068 12071 11562469 10.1073/pnas.201212698
188. Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae). PCD Johnson JA Whitfield WA Foster W Amos, Molecular Ecology 2002 11 1525 1531 10.1046/j.1365-294X.2002.01530.x 12144671
189. Worker policing in the honeybee. FLW Ratnieks PK Visscher, Nature 1989 342 796 797 10.1038/342796a0
190. A quantitative study of worker reproduction in honeybee colonies. PK Visscher, Behavioral Ecology and Sociobiology 1989 25 247 254 10.1007/BF00300050
191. Reproductive conflict in honey bees: A stalemate of worker egg-laying and policing. PK Visscher, Behavioral Ecology and Sociobiology 1996 39 237 244 10.1007/s002650050286
192. Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. AB Barron BP Oldroyd FLW Ratnieks, Behavioral Ecology and Sociobiology 2001 50 199 208 10.1007/s002650100362
193. Conflict resolution in insect societies. FLW Ratnieks KR Foster T Wenseleers, Annual Review of Entomology 2006 51 581 608 10.1146/annurev.ento.51. 110104.151003 16332224
194. Virgin queens in stingless bee (Apidae, Meliponinae) colonies - a review. VL Imperatriz-Fonseca R Zucchi, Apidologie 1995 26 231 244 10.1051/apido: 19950305
195. Mate number, kin selection and social conflicts in stingless bees and honeybees. JM Peters DC Queller VL Imperatriz-Fonseca DW Roubik JE Strassmann, Proceedings of the Royal Society of London Series B-Biological Sciences 1999 266 379 384 10.1098/rspb.1999.0648
196. Broodcare helpers in the cichlid fish Lamprologus-brichardi - their costs and benefits. M Taborsky, Anim Behav 1984 32 1236 1252 10.1016/S0003-3472(84) 80241-9
197. Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. P Dierkes D Heg M Taborsky E Skubic R Achmann, Ecology Letters 2005 8 968 975 10.1111/j.1461-0248.2005.00801.x
198. Cooperative breeding in the Lake Tanganyika cichlid Julidochromis ornatus. D Heg Z Bachar, Environmental Biology of Fishes 2006 76 265 281 10.1007/s10641-006-9032-5
199. Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. D Heg Z Bachar L Brouwer M Taborsky, Proc R Soc Lond B 2004 271 2367 2374 10.1098/rspb.2004.2855
200. Communal activities among white-winged choughs Corcorax melanorhamphos. I Rowley, Ibis 1978 120 178 197 10.1111/j.1474-919X.1978.tb06774.x
201. Helping is costly to young birds in cooperatively breeding white-winged choughs. R Heinsohn A Cockburn, Proceedings of the Royal Society of London Series B-Biological Sciences 1994 256 293 298 10.1098/rspb.1994.0083
202. Coalitions of relatives and reproductive skew in cooperatively breeding white-winged choughs. R Heinsohn P Dunn S Legge M Double, Proceedings of the Royal Society of London Series B-Biological Sciences 2000 267 243 249 10.1098/rspb.2000.0993
203. Cooperative enhancement of reproductive success in white-winged choughs. RG Heinsohn, Evolutionary Ecology 1992 6 97 114 10.1007/BF02270705
204. Deception by helpers in cooperatively breeding white-winged choughs and its experimental manipulation. CRJ Boland R Heinsohn A Cockburn, Behavioral Ecology and Sociobiology 1997 41 251 256 10.1007/s002650050386
205. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. JUM Jarvis, Science 1981 212 571 573 10.1126/science.7209555 7209555
206. Queen activation of lazy workers in colonies of the eusocial naked mole-rat. HK Reeve, Nature 1992 358 147 149 10.1038/358147a0 1614546
207. Eusociality has evolved independently in 2 genera of bathyergid mole-rats, but occurs in no other subterranean mammal. JUM Jarvis NC Bennett, Behavioral Ecology and Sociobiology 1993 33 253 260 10.1007/BF02027122
208. Mammalian eusociality: a family affair. JUM Jarvis MJ O'Riain NC Bennett PW Sherman, Trends EcolEvol 1994 9 46 51
209. African Mole-rats Ecology and Eusociality. NC Bennett CG Faulkes, Cambridge: Cambridge Univ Press 2000
210. Eusociality in African mole-rats: new insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis). TM Burland NC Bennett JUM Jarvis CG Faulkes, Proceedings of the Royal Society of London Series B-Biological Sciences 2002 269 1025 1030 10.1098/rspb.2002.1978