Section: Evolutionary Biology
Topic:
Evolution,
Biology of interactions,
Ecology
Mutualists construct the ecological conditions that trigger the transition from parasitism
Corresponding author(s): Garnier, Jimmy (jimmy.garnier@univ-smb.fr)
10.24072/pcjournal.139 - Peer Community Journal, Volume 2 (2022), article no. e41.
Get full text PDF Peer reviewed and recommended by PCI
The evolution of mutualism between hosts and initially parasitic symbionts represents a major transition in evolution. Although vertical transmission of symbionts during host reproduction and partner control both favour the stability of mutualism, these mechanisms require specifically evolved features that may be absent in the first place. Therefore, the first steps of the transition from parasitism to mutualism may suffer from the cost of mutualism at the organismic level. We hypothesize that spatial structure can lead to the formation of higher selection levels favouring mutualism. This resembles the evolution of altruism, with the additional requirement that the offspring of mutualistic hosts and symbionts must co-occur often enough. Using a spatially explicit agent-based model we demonstrate that, starting from a parasitic system with global dispersal, the joint evolution of mutualistic effort and local dispersal of hosts and symbionts leads to a stable coexistence between parasites and mutualists. The evolution of local dispersal mimics vertical transmission and triggers the formation of mutualistic clusters, counteracting the organismic selection level of parasites that maintain global dispersal. The transition occurs when mutualistic symbionts increase the density of hosts, which strengthens competition between hosts and disfavours hosts inhabiting areas dominated by parasitic symbionts: mutualists construct the ecological conditions that allow their own spread. Therefore, the transition to mutualism may come from an eco-evolutionary feedback loop involving spatially structured population dynamics.
Type: Research article
Ledru, Léo 1; Garnier, Jimmy 2; Rhor, Matthias 1; Nous, Camille 1, 2, 3; Ibanez, Sébastien 1
CC-BY 4.0
@article{10_24072_pcjournal_139,
author = {Ledru, L\'eo and Garnier, Jimmy and Rhor, Matthias and Nous, Camille and Ibanez, S\'ebastien},
title = {Mutualists construct the ecological conditions that trigger the transition from parasitism},
journal = {Peer Community Journal},
eid = {e41},
publisher = {Peer Community In},
volume = {2},
year = {2022},
doi = {10.24072/pcjournal.139},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.139/}
}
TY - JOUR AU - Ledru, Léo AU - Garnier, Jimmy AU - Rhor, Matthias AU - Nous, Camille AU - Ibanez, Sébastien TI - Mutualists construct the ecological conditions that trigger the transition from parasitism JO - Peer Community Journal PY - 2022 VL - 2 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.139/ DO - 10.24072/pcjournal.139 ID - 10_24072_pcjournal_139 ER -
%0 Journal Article %A Ledru, Léo %A Garnier, Jimmy %A Rhor, Matthias %A Nous, Camille %A Ibanez, Sébastien %T Mutualists construct the ecological conditions that trigger the transition from parasitism %J Peer Community Journal %D 2022 %V 2 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.139/ %R 10.24072/pcjournal.139 %F 10_24072_pcjournal_139
Ledru, Léo; Garnier, Jimmy; Rhor, Matthias; Nous, Camille; Ibanez, Sébastien. Mutualists construct the ecological conditions that trigger the transition from parasitism. Peer Community Journal, Volume 2 (2022), article no. e41. doi : 10.24072/pcjournal.139. https://peercommunityjournal.org/articles/10.24072/pcjournal.139/
PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100143
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Evolutionary models of mutualism, Mutualism, Oxford University Press, 2015, pp. 57-76 | DOI
[2] Population structure reduces benefits from partner choice in mutualistic symbiosis, Proceedings of the Royal Society B: Biological Sciences, Volume 284 (2017) no. 1850 | DOI
[3] The cancellation effect at the group level, Evolution, Volume 74 (2020) no. 7, pp. 1246-1254 | DOI
[4] Symbiotic bacteria enable insect to use a nutritionally inadequate diet, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2008) no. 1658, pp. 987-991 | DOI
[5] Empty sites can promote altruistic behavior, Evolution, Volume 62 (2008) no. 6, pp. 1335-1344 | DOI
[6] Multiple infections and the evolution of virulence, Ecology Letters, Volume 16 (2013) no. 4, pp. 556-567 | DOI
[7] The ecology of mycorrhizae, Cambridge University Press, 1991
[8] Positive plant–soil feedback trigger tannin evolution by niche construction: A spatial stoichiometric model, Journal of Ecology, Volume 108 (2019) no. 1, pp. 378-391 | DOI
[9] The Emergence of Cooperation among Egoists, American Political Science Review, Volume 75 (1981) no. 2, pp. 306-318 | DOI
[10] Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 33, pp. 10169-10176 | DOI
[11] Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism, Ecology Letters, Volume 12 (2009) no. 1, pp. 13-21 | DOI
[12] Achieving a multi-strain symbiosis: strain behavior and infection dynamics, The ISME Journal, Volume 13 (2018) no. 3, pp. 698-706 | DOI
[13] Costs of dispersal, Biological Reviews, Volume 87 (2011) no. 2, pp. 290-312 | DOI
[14] Local Interactions Select for Lower Pathogen Infectivity, Science, Volume 315 (2007) no. 5816, pp. 1284-1286 | DOI
[15] Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes, PLOS Biology, Volume 13 (2015) no. 8 | DOI
[16] How to be a fig wasp parasite on the fig–fig wasp mutualism, Current Opinion in Insect Science, Volume 8 (2015), pp. 34-40 | DOI
[17] Conditional outcomes in mutualistic interactions, Trends in Ecology & Evolution, Volume 9 (1994) no. 6, pp. 214-217 | DOI
[18] The Contribution of Ant-Plant Protection Studies to Our Understanding of Mutualism, Biotropica, Volume 30 (1998) no. 2, pp. 150-161 | DOI
[19] Mutualism, Oxford University Press, 2015 | DOI
[20] The evolution of plant–insect mutualisms, New Phytologist, Volume 172 (2006) no. 3, pp. 412-428 | DOI
[21] Positive interactions among alpine plants increase with stress, Nature, Volume 417 (2002) no. 6891, pp. 844-848 | DOI
[22] The descent of man, and selection in relation to sex, D. Appleton and company, New York, 1871 | DOI
[23] A resource ratio theory of cooperation, Ecology Letters, Volume 13 (2010) no. 3, pp. 349-359 | DOI
[24] Evolution of Host Life-History Traits in a Spatially Structured Host-Parasite System, The American Naturalist, Volume 179 (2012) no. 1, pp. 52-63 | DOI
[25] Why are most rhizobia beneficial to their plant hosts, rather than parasitic?, Microbes and Infection, Volume 6 (2004) no. 13, pp. 1235-1239 | DOI
[26] Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae), Journal of Evolutionary Biology, Volume 12 (1999) no. 4, pp. 822-831 | DOI
[27] On the origin of species by sympatric speciation, Nature, Volume 400 (1999) no. 6742, pp. 354-357 | DOI
[28] Evolutionary cycling in predator-prey interactions: population dynamics and the red queen, Journal of Theoretical Biology, Volume 176 (1995) no. 1, pp. 91-102 | DOI
[29] The evolution of interspecific mutualisms, Proceedings of the National Academy of Sciences, Volume 95 (1998) no. 15, pp. 8676-8680 | DOI
[30] Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 16, pp. 4006-4014 | DOI
[31] Microbial evolution and transitions along the parasite–mutualist continuum, Nature Reviews Microbiology, Volume 19 (2021) no. 10, pp. 623-638 | DOI
[32] Selection for protection in an ant–plant mutualism: host sanctions, host modularity, and the principal–agent game, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1586, pp. 595-602 | DOI
[33] Population structure influences sexual conflict in wild populations of water striders, Behaviour, Volume 147 (2010) no. 12, pp. 1615-1631 | DOI
[34] Transitions in individuality through symbiosis, Current Opinion in Microbiology, Volume 31 (2016), pp. 191-198 | DOI
[35] The Tragedy of the Commons: Twenty-two years later, Human Ecology, Volume 18 (1990) no. 1, pp. 1-19 | DOI
[36] Diversification of Transmission Modes and the Evolution of Mutualism, The American Naturalist, Volume 166 (2005) no. 5, pp. 613-627 | DOI
[37] Cheating and the evolutionary stability of mutualisms, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1493, pp. 773-780 | DOI
[38] Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 368 (2013) no. 1610 | DOI
[39] Group Formation, Relatedness, and the Evolution of Multicellularity, Current Biology, Volume 23 (2013) no. 12, pp. 1120-1125 | DOI
[40] The evolution of host-symbiont dependence, Nature Communications, Volume 8 (2017) no. 1 | DOI
[41] A general model for the evolution of mutualisms, Journal of Evolutionary Biology, Volume 19 (2006) no. 4, pp. 1283-1293 | DOI
[42] Genetics of Mutualism: The Evolution of Altruism between Species, Journal of Theoretical Biology, Volume 170 (1994) no. 4, pp. 393-400 | DOI
[43] Evolution of Mutualistic Symbiosis without Vertical Transmission, Theoretical Population Biology, Volume 55 (1999) no. 3, pp. 309-323 | DOI
[44] A Symbiotic View of Life: We Have Never Been Individuals, The Quarterly Review of Biology, Volume 87 (2012) no. 4, pp. 325-341 | DOI
[45] Godfrey-Smith P , CJ Goodnight , E Clarke , S Okasha , T Pradeau , A Gardner , M van Baalen , A Hamilton , J Fewell , and M Haber (2013). From Groups to Individuals: Evolution and Emerging Individuality. MIT Press.
[46] When Does Evolution By Natural Selection Prevent Extinction?, Evolution, Volume 49 (1995) no. 1, pp. 201-207 | DOI
[47] Multilevel selection: the evolution of cooperation in non-kin groups, Population Ecology, Volume 47 (2005) no. 1, pp. 3-12 | DOI
[48] The Structure of Evolutionary Theory, Harvard University Press, 2002 | DOI
[49] The Units of Evolutionary Transition, Selection, Volume 1 (2001) no. 1-3, pp. 67-80 | DOI
[50] The genetical evolution of social behaviour. I, Journal of Theoretical Biology, Volume 7 (1964) no. 1, pp. 1-16 | DOI
[51] The genetical evolution of social behaviour. II, Journal of Theoretical Biology, Volume 7 (1964) no. 1, pp. 17-52 | DOI
[52] Innate social aptitudes of man: an approach from evolutionary genetics In: in Nar- row roads of gene land. Vol. 1: Evolution of social behaviour (1975), pp. 315-352
[53] Dispersal in stable habitats, Nature, Volume 269 (1977) no. 5629, pp. 578-581 | DOI
[54] Short- vs. Long-range Disperser: the Evolutionarily Stable Allocation in a Lattice-Structured Habitat, Journal of Theoretical Biology, Volume 201 (1999) no. 3, pp. 171-187 | DOI
[55] Extremal animals, Journal of Combinatorics, Information System Sciences, Volume 1 (1976), pp. 1-8
[56] Novel cooperation experimentally evolved between species, Evolution, Volume 64 (2010), pp. 2166-2172 | DOI
[57] The Tragedy of the Commons, Science, Volume 162 (1968) no. 3859, pp. 1243-1248 | DOI
[58] Extensions of "The Tragedy of the Commons", Science, Volume 280 (1998) no. 5364, pp. 682-683 | DOI
[59] The evolution of mutualisms: exploring the paths between conflict and cooperation, Trends in Ecology amp; Evolution, Volume 14 (1999) no. 2, pp. 49-53 | DOI
[60] The coevolution of cooperation and dispersal in social groups and its implications for the emergence of multicellularity, BMC Evolutionary Biology, Volume 8 (2008) no. 1 | DOI
[61] Individuality and Selection, Annual Review of Ecology and Systematics, Volume 11 (1980) no. 1, pp. 311-332 | DOI
[62] Long-Distance Rescue and Slow Extinction Dynamics Govern Multiscale Metapopulations, The American Naturalist, Volume 186 (2015) no. 4, pp. 460-469 | DOI
[63] The Evolution of Ecosystem Phenotypes, Biological Theory, Volume 15 (2020) no. 2, pp. 91-106 | DOI
[64] Functioning of mycorrhizal associations along the mutualism-parasitism continuum, New Phytologist, Volume 135 (1997) no. 4, pp. 575-585 | DOI
[65] Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism, Ecology Letters, Volume 18 (2015) no. 11, pp. 1270-1284 | DOI
[66] The fundamental role of competition in the ecology and evolution of mutualisms, Annals of the New York Academy of Sciences, Volume 1256 (2012) no. 1, pp. 66-88 | DOI
[67] Differential contribution of frugivores to complex seed dispersal patterns, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 9, pp. 3278-3282 | DOI
[68] Reversal of mutualism in a leafflower-leafflower moth association: the possible driving role of a third-party partner, Biological Journal of the Linnean Society, Volume 116 (2015) no. 3, pp. 507-518 | DOI
[69] Local facilitation, bistability and transitions in arid ecosystems, Theoretical Population Biology, Volume 71 (2007) no. 3, pp. 367-379 | DOI
[70] Evolution of Local Facilitation in Arid Ecosystems, The American Naturalist, Volume 172 (2008) no. 1 | DOI
[71] The Evolution of Restraint in Structured Populations: Setting the Stage for an Egalitarian Major Transition, The Major Transitions in Evolution Revisited, The MIT Press, 2011, pp. 127-140 | DOI
[72] Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons', Nature, Volume 442 (2006) no. 7098, pp. 75-78 | DOI
[73] Host sanctions and the legume–rhizobium mutualism, Nature, Volume 425 (2003) no. 6953, pp. 78-81 | DOI
[74] Rapid evolution of microbe-mediated protection against pathogens in a worm host, The ISME Journal, Volume 10 (2016) no. 8, pp. 1915-1924 | DOI
[75] The spatial spread of altruism versus the evolutionary response of egoists, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 267 (2000) no. 1456, pp. 1979-1985 | DOI
[76] Phenotypic plasticity in size of ant-domatia, Scientific Reports, Volume 10 (2020) no. 1 | DOI
[77] An introduction to niche construction theory, Evolutionary Ecology, Volume 30 (2016) no. 2, pp. 191-202 | DOI
[78] Adaptive Evolution of Social Traits: Origin, Trajectories, and Correlations of Altruism and Mobility, The American Naturalist, Volume 165 (2005) no. 2, pp. 206-224 | DOI
[79] The adaptive dynamics of altruism in spatially heterogeneous populations, Evolution, Volume 57 (2003) no. 1, pp. 1-17 | DOI
[80] Group selection and kin selection: Two concepts but one process, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 16, pp. 6736-6739 | DOI
[81] Short range co-operativity competing with long range inhibition explains vegetation patterns, Acta Oecologica, Volume 20 (1999) no. 3, pp. 171-183 | DOI
[82] Survival of the Systems, Trends in Ecology amp; Evolution, Volume 36 (2021) no. 4, pp. 333-344 | DOI
[83] Lewontin RC (1982). Organism and environment. IC Plotkin (Ed.), Learning, development and culture: Essays in evolutionary epistemology.
[84] Gene, organism and environment, Evolution from molecules to men, Volume 273 (1983), p. 975
[85] Evolution in structured populations: beyond the kin versus group debate, Trends in Ecology amp; Evolution, Volume 26 (2011) no. 4, pp. 193-201 | DOI
[86] From Infanticide to Parental Care: Why Spatial Structure Can Help Adults Be Good Parents, The American Naturalist, Volume 170 (2007) no. 2 | DOI
[87] Self-structuring in spatial evolutionary ecology, Ecology Letters, Volume 11 (2008) no. 3, pp. 277-295 | DOI
[88] Evolutionary emergence of size-structured food webs, Proceedings of the National Academy of Sciences, Volume 102 (2005) no. 16, pp. 5761-5766 | DOI
[89] Selective feedback between dispersal distance and the stability of mutualism, Oikos, Volume 121 (2012) no. 3, pp. 442-448 | DOI
[90] Positive, negative, and net effects in grass–shrub interactions in mediterranean semiarid grasslands, Ecology, Volume 84 (2003) no. 12, pp. 3186-3197 | DOI
[91] Margulis L and D Sagan (2002). Acquiring genomes: a theory of the origins of species. en. 1st ed. New York, NY: Basic Books. ISBN: 978-0-465-04391-0.
[92] Group selection and kin selection: formally equivalent approaches, Trends in Ecology amp; Evolution, Volume 26 (2011) no. 7, pp. 325-332 | DOI
[93] The Importance of Microbes in Animal Development: Lessons from the Squid-Vibrio Symbiosis, Annual Review of Microbiology, Volume 68 (2014) no. 1, pp. 177-194 | DOI
[94] How should we define ‘fitness’ for general ecological scenarios?, Trends in Ecology amp; Evolution, Volume 7 (1992) no. 6, pp. 198-202 | DOI
[95] Population Viscosity and the Evolution of Altruism, Journal of Theoretical Biology, Volume 204 (2000) no. 4, pp. 481-496 | DOI
[96] Social polymorphism is favoured by the co-evolution of dispersal with social behaviour, Nature Ecology amp; Evolution, Volume 2 (2018) no. 1, pp. 132-140 | DOI
[97] On the difficult evolutionary transition from the free-living lifestyle to obligate symbiosis, PLOS ONE, Volume 15 (2020) no. 7 | DOI
[98] Group Selection, Altruism, and Structured-Deme Models, The American Naturalist, Volume 126 (1985) no. 2, pp. 212-230 | DOI
[99] Niche Construction, Princeton University Press, 2013 | DOI
[100] Evolution and the Levels of Selection, Oxford University Press, 2006 | DOI
[101] The Relation between Kin and Multilevel Selection: An Approach Using Causal Graphs, The British Journal for the Philosophy of Science, Volume 67 (2016) no. 2, pp. 435-470 | DOI
[102] Reversal of Mutualism as a Mechanism for Adaptive Radiation in Yucca Moths, The American Naturalist, Volume 156 (2000) no. S4 | DOI
[103] Simple Models of Assortment through Environmental Feedback, Artificial Life, Volume 13 (2007) no. 1, pp. 1-9 | DOI
[104] A Mechanism for the Evolution of Altruism among Nonkin: Positive Assortment through Environmental Feedback, The American Naturalist, Volume 160 (2002) no. 2, pp. 205-213 | DOI
[105] The relative contribution of individual and kin selection to the evolution of density-dependent dispersal rates, Evolutionary Ecology Research, Volume 9 (2007), pp. 41-50
[106] Co-evolution between sociality and dispersal: The role of synergistic cooperative benefits, Journal of Theoretical Biology, Volume 312 (2012), pp. 44-54 | DOI
[107] Quantitative Genetics, Inclusive Fitness, and Group Selection, The American Naturalist, Volume 139 (1992) no. 3, pp. 540-558 | DOI
[108] Cooperators Since Life Began, The Quarterly Review of Biology, Volume 72 (1997) no. 2, pp. 184-188 | DOI
[109] Relatedness and the fraternal major transitions, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Volume 355 (2000) no. 1403, pp. 1647-1655 | DOI
[110] Problems of multi-species organisms: endosymbionts to holobionts, Biology amp; Philosophy, Volume 31 (2016) no. 6, pp. 855-873 | DOI
[111] The Ecology and Evolution of Ant-Plant Interactions, University of Chicago Press, 2007 | DOI
[112] Self‐Organization of Vegetation in Arid Ecosystems, The American Naturalist, Volume 160 (2002) no. 4, pp. 524-530 | DOI
[113] Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution, Biological Theory, Volume 13 (2018) no. 1, pp. 44-65 | DOI
[114] Evolution of Marine Symbiosis--A Simple Cost-Benefit Model, Ecology, Volume 56 (1975) no. 5, pp. 1201-1208 | DOI
[115] Origins of cheating and loss of symbiosis in wildiBradyrhizobium/i, Journal of Evolutionary Biology, Volume 23 (2010) no. 5, pp. 1075-1089 | DOI
[116] The Evolution of Cooperation, The Quarterly Review of Biology, Volume 79 (2004) no. 2, pp. 135-160 | DOI
[117] Host control over infection and proliferation of a cheater symbiont, Journal of Evolutionary Biology, Volume 23 (2010) no. 9, pp. 1919-1927 | DOI
[118] Pathways to mutualism breakdown, Trends in Ecology amp; Evolution, Volume 21 (2006) no. 10, pp. 585-592 | DOI
[119] Evolutionary transitions in bacterial symbiosis, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. supplement_2, pp. 10800-10807 | DOI
[120] The persistence of vertically transmitted fungi in grass metapopulations, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1498, pp. 1397-1403 | DOI
[121] Evolution of endophyte?plant symbioses, Trends in Plant Science, Volume 9 (2004) no. 6, pp. 275-280 | DOI
[122] The state of affairs in the kingdom of the Red Queen, Trends in Ecology amp; Evolution, Volume 23 (2008) no. 8, pp. 439-445 | DOI
[123] Clone mixtures and a pacemaker: new facets of Red-Queen theory and ecology, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1493, pp. 761-772 | DOI
[124] Horizontal versus vertical transmission of parasites in a stochastic spatial model, Mathematical Biosciences, Volume 168 (2000) no. 1, pp. 1-8 | DOI
[125] Evolution of mutualism from parasitism in experimental virus populations, Evolution, Volume 72 (2018) no. 3, pp. 707-712 | DOI
[126] Evolution of parasitism and mutualism between filamentous phage M13 andiEscherichia coli/i, PeerJ, Volume 4 (2016) | DOI
[127] Towards a general theory of group selection, Evolution, Volume 67 (2012) no. 6, pp. 1561-1572 | DOI
[128] Group Selection and Kin Selection, Nature, Volume 201 (1964) no. 4924, pp. 1145-1147 | DOI
[129] Smith JM (1998). Evolutionary genetics. Oxford University Press.
[130] Sober E and DS Wilson (1999). Unto others: The evolution and psychology of unselfish behavior. Harvard University Press.
[131] Sober E (1984). The nature of selection: evolutionary theory in philosophical focus. University of Chicago Press.
[132] Artifact, Cause and Genic Selection, Philosophy of Science, Volume 49 (1982) no. 2, pp. 157-180 | DOI
[133] Dynamics of host-parasite interactions with horizontal and vertical transmissions in spatially heterogeneous environment, Physica A: Statistical Mechanics and its Applications, Volume 517 (2019), pp. 452-458 | DOI
[134] Toward major evolutionary transitions theory 2.0, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 33, pp. 10104-10111 | DOI
[135] The major transitions in evolution, WH Freeman Spektrum, Oxford, UK, 1995
[136] The evolution of intermediate castration virulence and ant coexistence in a spatially structured environment, Ecology Letters, Volume 12 (2009) no. 12, pp. 1306-1316 | DOI
[137] Overlapping generations can promote altruistic behavior, Evolution, Volume 54 (2000) no. 4, pp. 1135-1141 | DOI
[138] Local densities connect spatial ecology to game, multilevel selection and inclusive fitness theories of cooperation, Journal of Theoretical Biology, Volume 380 (2015), pp. 414-425 | DOI
[139] Geographic structure and dynamics of coevolutionary selection, Nature, Volume 417 (2002) no. 6890, pp. 735-738 | DOI
[140] The distribution of positive and negative species interactions across environmental gradients on a dual-lattice model, Journal of Theoretical Biology, Volume 241 (2006) no. 4, pp. 896-902 | DOI
[141] Does mobility decrease cooperation?, Journal of Theoretical Biology, Volume 244 (2007) no. 4, pp. 722-728 | DOI
[142] The Unit of Selection in Viscous Populations and the Evolution of Altruism, Journal of Theoretical Biology, Volume 193 (1998) no. 4, pp. 631-648 | DOI
[143] Kin Selection: Its Components, Science, Volume 210 (1980) no. 4470, pp. 665-667 | DOI
[144] Hard and soft selection revisited, Evolution, Volume 29 (1975) no. 3, pp. 465-473 | DOI
[145] Coevolutionary Arms Races and the Conditions for the Maintenance of Mutualism, The American Naturalist, Volume 198 (2021) no. 2, pp. 195-205 | DOI
[146] From Parasite to Mutualist: Rapid Evolution of Wolbachia in Natural Populations of Drosophila, PLoS Biology, Volume 5 (2007) no. 5 | DOI
[147] Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown, Proceedings of the National Academy of Sciences, Volume 115 (2018) no. 20, pp. 5229-5234 | DOI
[148] Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 33, pp. 10262-10269 | DOI
[149] Sanctions and mutualism stability: why do rhizobia fix nitrogen?, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1492, pp. 685-694 | DOI
[150] The Role of Seed Dispersal in the Evolution of Mycorrhizae, Oikos, Volume 78 (1997) no. 2 | DOI
[151] Horizontally acquired mutualisms, an unsolved problem in ecology?, Oikos, Volume 92 (2001) no. 2, pp. 377-384 | DOI
[152] Group Selection and Assortative Interactions, The American Naturalist, Volume 149 (1997) no. 2, pp. 336-351 | DOI
[153] Can altruism evolve in purely viscous populations?, Evolutionary Ecology, Volume 6 (1992) no. 4, pp. 331-341 | DOI
[154] Reintroducing group selection to the human behavioral sciences, Behavioral and Brain Sciences, Volume 17 (1994) no. 4, pp. 585-608 | DOI
[155] A theory of group selection., Proceedings of the National Academy of Sciences, Volume 72 (1975) no. 1, pp. 143-146 | DOI
[156] What is wrong with absolute individual fitness?, Trends in Ecology amp; Evolution, Volume 19 (2004) no. 5, pp. 245-248 | DOI
[157] Reviving the superorganism, Journal of Theoretical Biology, Volume 136 (1989) no. 3, pp. 337-356 | DOI
[158] Evolution of mutualism through spatial effects, Journal of Theoretical Biology, Volume 226 (2004) no. 4, pp. 421-428 | DOI
[159] The natural occurrence of secondary bacterial symbionts in aphids, Ecological Entomology, Volume 41 (2015) no. 1, pp. 13-26 | DOI
Cited by Sources: