1932

Abstract

Evolution has been viewed as occurring primarily through selection among individuals. We present a framework based on multilevel selection for evaluating evolutionary change from individuals to communities, with supporting empirical evidence. Essential to this evaluation is the role that interspecific indirect genetic effects play in shaping community organization, in generating variation among community phenotypes, and in creating community heritability. If communities vary in phenotype, and those phenotypes are heritable and subject to selection at multiple levels, then a community view of evolution must be merged with mainstream evolutionary theory. Rapid environmental change during the Anthropocene will require a better understanding of these evolutionary processes, especially selection acting at the community level, which has the potential to eliminate whole communities while favoring others.

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2020-11-02
2024-03-29
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Literature Cited

  1. Allan GJ, Shuster SM, Woolbright S, Walker F, Meneses N et al. 2012. Interspecific indirect genetic effects (IIGEs): linking genetics and genomics to community ecology and ecosystem processes. Trait-Mediated Indirect Interactions: Ecological and Evolutionary Perspectives T Ohgushi, O Schmitz, RD Holt 295–323 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  2. Antonovics J. 1992. Toward community genetics. Plant Resistance to Herbivores and Pathogens RS Fritz, EL Simms 426–49 Chicago: Univ. Chicago Press
    [Google Scholar]
  3. Bailey JK, Wooley SC, Lindroth RL, Whitham TG 2006. Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol. Lett. 9:78–85
    [Google Scholar]
  4. Bangert RK, Allan GJ, Turek RJ, Wimp GM, Meneses N et al. 2006a. From genes to geography: a genetic similarity rule for arthropod community structure at multiple geographic scales. Mol. Ecol. 15:4215–28
    [Google Scholar]
  5. Bangert RK, Turek RJ, Rehill B, Allan GJ, Wimp GM et al. 2006b. A genetic similarity rule determines arthropod community structure. Mol. Ecol. 15:1379–92
    [Google Scholar]
  6. Bangert RK, Lonsdorf EV, Wimp GM, Shuster SM, Fischer DG et al. 2008. Genetic structure of a foundation species: scaling community phenotypes from the individual to the region. Heredity 100:121–31
    [Google Scholar]
  7. Barbour MA, Erlandson S, Peay K, Locke B, Jules ES, Crutsinger GM 2019. Trait plasticity is more important than genetic variation in determining species richness of associated communities. J. Ecol. 107:350–60
    [Google Scholar]
  8. Barbour MA, Fortuna MA, Bascompte J, Nicholson JR, Julkunen-Tiitto R et al. 2016. Genetic specificity of a plant–insect food web: implications for linking genetic variation to network complexity. PNAS 113:2128–33
    [Google Scholar]
  9. Barbour RC, Forster LG, Baker SC, Steane DA, Potts BM 2009a. Biodiversity consequences of genetic variation in bark characteristics within a foundation tree species. Conserv. Biol. 23:1146–55
    [Google Scholar]
  10. Barbour RC, O'Reilly-Wapstra JM, De Little DW, Jordan GJ, Steane DA et al. 2009b. A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology 90:1762–72
    [Google Scholar]
  11. Becker WA. 1985. Manual of Quantitative Genetics Pullman, WA: Academic, 4th ed..
  12. Berg MP, Ellers J. 2010. Trait plasticity in species interactions: a driving force of community dynamics. Evol. Ecol. 24:617–29
    [Google Scholar]
  13. Bordenstein SR, Theis KR. 2015. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLOS Biol 13:e1002226
    [Google Scholar]
  14. Brusca RC, Wiens JF, Meyer WM, Eble J, Franklin K, Overpeck JT, Moore W 2013. Dramatic response to climate change in the Southwest: Robert Whittaker's 1963 Arizona mountain plant transect revisited. Ecol. Evol. 3:3307–19
    [Google Scholar]
  15. Busby PE, Lamit LJ, Keith AR, Newcombe G, Gehring CA et al. 2015. Genetics-based interactions among plants, pathogens and herbivores define arthropod community structure. Ecology 96:1974–84
    [Google Scholar]
  16. Busby PE, Newcombe G, Dirzo R, Whitham TG 2013. Genetic basis of pathogen community structure for foundation species in a common garden and in the wild. J. Ecol. 101:867–77
    [Google Scholar]
  17. Chadde SW, Kay CE. 1991. Tall willow communities on Yellowstone's northern range: a test of the “natural regulation” paradigm. The Greater Yellowstone Ecosystem RB Keiter, MS Boyce 231–62 New Haven, CT: Yale Univ. Press
    [Google Scholar]
  18. Clarke KR. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117–43
    [Google Scholar]
  19. Compson ZG, Hungate BA, Whitham TG, Meneses N, Busby PE et al. 2016. Plant genotype influences aquatic–terrestrial ecosystem linkages through timing and composition of insect emergence. Ecosphere 7:e01331
    [Google Scholar]
  20. Cooper HF, Grady KC, Cowan JA, Best RJ, Allan GJ, Whitham TG 2019. Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost. Glob. Change Biol. 25:187–200
    [Google Scholar]
  21. Crow JF. 1958. Some possibilities for measuring selection intensities in man. Hum. Biol. 30:1–13
    [Google Scholar]
  22. Crutsinger GM. 2016. A community genetics perspective: opportunities for the coming decade. New Phytol 210:65–70
    [Google Scholar]
  23. Darwin C. 1859. On the Origin of Species by Means of Natural Selection London: Murray
  24. Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP et al. 2018. The ecological importance of intraspecific variation. Nat. Ecol. Evol. 2:57–64
    [Google Scholar]
  25. Douglas AE, Werren JH. 2016. Holes in the hologenome: why host–microbe symbioses are not holobionts. mBio 7:e02099–15
    [Google Scholar]
  26. Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586–608
    [Google Scholar]
  27. Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K et al. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front. Ecol. Environ. 3:479–86
    [Google Scholar]
  28. Estes JA, Burdin A, Doak DF 2016. Sea otters, kelp forests, and the extinction of Steller's sea cow. PNAS 113:880–85
    [Google Scholar]
  29. Evans LM, Allan GJ, Shuster SM, Woolbright SA, Whitham TG 2008. Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore. Evolution 62:3027–40
    [Google Scholar]
  30. Evans LM, Kaluthota S, Pearce DW, Allan GJ, Floate K et al. 2016. Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods. Ecol. Evol. 6:4565–81
    [Google Scholar]
  31. Faith DP, Minchin PR, Belbin L 1987. Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68
    [Google Scholar]
  32. Falconer DS, McKay TFC. 1996. Introduction to Quantitative Genetics New York/London: Longman, 4th ed..
  33. Ferrier SM, Bangert RK, Hersch-Green E, Bailey JK, Allan GJ, Whitham TG 2012. Unique arthropod communities on different host–plant genotypes results in greater arthropod diversity. Arthropod Plant Interact 6:187–95
    [Google Scholar]
  34. Fischer DG, Chapman SK, Classen AT, Gehring CA, Grady KC et al. 2014. Plant genetic effects on soils under climate change. Plant Soil 379:1–19
    [Google Scholar]
  35. Fordyce JA. 2006. The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J. Exp. Biol. 209:2377–83
    [Google Scholar]
  36. Foster KR, Schluter J, Coyte KZ, Rakoff-Nahoum S 2017. The evolution of the host microbiome as an ecosystem on a leash. Nature 548:43–51
    [Google Scholar]
  37. Gehring CA, Flores-Rentería D, Sthultz CM, Leonard TM, Flores-Rentería L et al. 2014. Plant genetics and interspecific competitive interactions determine ectomycorrhizal fungal community responses to climate change. Mol. Ecol. 23:1379–91
    [Google Scholar]
  38. Gehring CA, Sthultz CM, Flores-Rentería L, Whipple AV, Whitham TG 2017. Tree genetics defines fungal partner communities that may confer drought tolerance. PNAS 114:11169–74
    [Google Scholar]
  39. Gilbert SF, Sapp J, Tauber AI 2012. A symbiotic view of life: We have never been individuals. Q. Rev. Biol. 87:325–41
    [Google Scholar]
  40. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD 2010. A framework for community interactions under climate change. Trends Ecol. Evol. 25:325–31
    [Google Scholar]
  41. Goodnight CJ. 1990a. Experimental studies of community evolution. I. The response to selection at the community level. Evolution 44:1614–24
    [Google Scholar]
  42. Goodnight CJ. 1990b. Experimental studies of community evolution. II. The ecological basis of the response to community selection. Evolution 44:1625–36
    [Google Scholar]
  43. Goodnight CJ. 1995. Epistasis and the increase in additive genetic variance: implications for phase 1 of Wright's shifting balance process. Evolution 49:502–11
    [Google Scholar]
  44. Goodnight CJ. 2000. Heritability at the ecosystem level. PNAS 97:9365–66
    [Google Scholar]
  45. Goodnight CJ, Craig DM. 1996. The effect of coexistence on competitive outcome in Tribolium castaneum and Tribolium confusum. . Evolution 50:1241–50
    [Google Scholar]
  46. Goodnight CJ, Schwartz JM, Stevens L 1992. Contextual analysis of models of group selection, soft selection, hard selection, and the evolution of altruism. Am. Nat. 140:743–61
    [Google Scholar]
  47. Grady KC, Wood TE, Kolb TE, Hersch-Green E, Shuster SM et al. 2017. Local biotic adaptation of trees and shrubs to plant neighbors. Oikos 126:583–93
    [Google Scholar]
  48. Griffing B. 1967. Selection in reference to biological groups. I. Individual and group selection applied to populations of unordered groups. Aust. J. Biol. Sci. 20:127–40
    [Google Scholar]
  49. Herlihy D. 1974. The Family in Renaissance Italy. Forums Hist. 125. St. Charles, MO: Forum Press
    [Google Scholar]
  50. Hersch EI, Phillips PC. 2004. Power and potential bias in field studies of natural selection. Evolution 58:479–85
    [Google Scholar]
  51. Hubbell SP. 2001. The Unified Neutral Theory of Biodiversity and Biogeography Princeton, NJ: Princeton Univ. Press
  52. Hubbell SP. 2005. Neutral theory in community ecology and the hypothesis of functional equivalence. Funct. Ecol. 19:166–72
    [Google Scholar]
  53. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M 2008. Ecological consequences of genetic diversity. Ecol. Lett. 11:609–23
    [Google Scholar]
  54. Janzen DH. 1980. When is it coevolution. ? Evolution 34:611–12
    [Google Scholar]
  55. Johnson MTJ, Stinchcombe JR. 2007. An emerging synthesis between community ecology and evolutionary biology. Trends Ecol. Evol. 780:1–8
    [Google Scholar]
  56. Keith AR, Bailey JK, Lau MK, Whitham TG 2017. Genetics-based interactions of foundation species affect community diversity, stability, and network structure. Proc. R. Soc. B 284:20162703
    [Google Scholar]
  57. Keith AR, Bailey JK, Whitham TG 2010. A genetic basis to community repeatability and stability. Ecology 11:3398–406
    [Google Scholar]
  58. Lamit LJ, Busby PE, Lau MK, Compson ZG, Wojtowicz T et al. 2015a. Tree genotype mediates covariance among diverse communities from microbes to arthropods. J. Ecol. 103:840–50
    [Google Scholar]
  59. Lamit LJ, Holeski LM, Flores-Rentería L, Whitham TG, Gehring CA 2016. Tree genotype influences ectomycorrhizal fungal community structure: ecological and evolutionary implications. Fungal Ecol 24:124–34
    [Google Scholar]
  60. Lamit LJ, Lau MK, Reese Næsborg R, Wojtowicz T, Whitham TG, Gehring CA 2015b. Genotype variation in bark texture drives lichen community assembly across multiple environments. Ecology 96:960–71
    [Google Scholar]
  61. Lamit LJ, Lau MK, Sthultz CM, Wooley SC, Whitham TG, Gehring CA 2014. Tree genotype and genetically-based growth traits structure twig endophyte communities. Am. J. Bot. 101:467–78
    [Google Scholar]
  62. Lande R, Arnold SJ. 1983. The measurement of selection on correlated characters. Evolution 37:1210–26
    [Google Scholar]
  63. Lau MK, Keith AR, Borrett SR, Shuster SM, Whitham TG 2016. Genotypic variation in foundation species generates network structure that may drive community dynamics and evolution. Ecology 97:733–42
    [Google Scholar]
  64. LCR-MSCP. 2004. Lower Colorado River Multi-Species Conservation Program, Vol. 2: habitat conservation plan Final Rep., LCR-MSCP Sacramento, CA:
    [Google Scholar]
  65. Levin SA, Sege LA, Adler FR 1990. Diffuse coevolution in plant–herbivore communities. Theor. Popul. Biol. 37:171–91
    [Google Scholar]
  66. Lewontin RC. 1970. The units of selection. Annu. Rev. Ecol. Syst. 1:1–18
    [Google Scholar]
  67. Lynch M, Walsh B. 1998. Genetics and Analysis of Quantitative Traits Sunderland, MA: Sinauer
  68. Minchin PR. 1987. An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107
    [Google Scholar]
  69. Mopper S. 1996. Adaptive genetic structure in phytophagous insect populations. Trends Ecol. Evol. 11:235–38
    [Google Scholar]
  70. Mopper S, Stiling P, Landau K, Simberloff D, Van Zant P 2000. Spatiotemporal variation in leafminer population structure and adaptation to individual oak trees. Ecology 81:1577–87
    [Google Scholar]
  71. Moran NA, Sloan DB. 2015. The hologenome concept: helpful or hollow. ? PLOS Biol 13:e1002311
    [Google Scholar]
  72. Mueller RC, Scudder CM, Porter ME, Trotter RT, Gehring CA, Whitham TG 2005. Differential tree mortality in response to severe drought: evidence for long-term vegetation shifts. J. Ecol. 93:1085–93
    [Google Scholar]
  73. Neuhauser C, Andow DA, Heimpel GE, May G, Shaw RG, Wagenius S 2003. Community genetics: expanding the synthesis of ecology and genetics. Ecology 84:545–58
    [Google Scholar]
  74. Ostry M, McNabb H. 1985. Susceptibility of Populus species and hybrids to disease in the north central United States. Plant Dis 69:755–57
    [Google Scholar]
  75. Patterson A, Flores-Rentería L, Whipple A, Whitham TG, Gehring CA 2019. Common garden experiments disentangle plant genetic and environmental contributions to ectomycorrhizal fungal community structure. New Phytol 221:493–502
    [Google Scholar]
  76. Price GR. 1972. Extension of covariance selection mathematics. Ann. Hum. Genet. 35:485–90
    [Google Scholar]
  77. Queller DC. 2014. Joint phenotypes, evolutionary conflict and the fundamental theorem of natural selection. Philos. Trans. R. Soc. B 369:20130423
    [Google Scholar]
  78. Rausher MD. 1996. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet 12:212–17
    [Google Scholar]
  79. Ricklefs RE. 2008. Disintegration of the ecological community. Am. Nat. 172:741–50
    [Google Scholar]
  80. Robertson A. 1957. Optimum group size in progeny testing and family selection. Biometric 13:442–50
    [Google Scholar]
  81. Roughgarden J, Gilbert SF, Rosenberg E, Zilber-Rosenberg I, Lloyd EA 2017. Holobionts as units of selection and a model of their population dynamics and evolution. Biol. Theor. 13:44–65
    [Google Scholar]
  82. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV et al. 2008. Plant–soil microorganism interactions: a heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–81
    [Google Scholar]
  83. Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Whitham TG, Hart SC 2012. Functional and heritable consequences of plant genotype on community composition and ecosystem processes. Trait-Mediated Indirect Interactions: Ecological and Evolutionary Perspectives T Ohgushi, O Schmitz, RD Holt 371–90 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  84. Shuster SM, Lonsdorf EV, Wimp GM, Bailey JK, Whitham TG 2006. Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60:991–1003
    [Google Scholar]
  85. Simmonds NW. 1996. Yields of cereal grain and protein. Exp. Agric. 32:351–56
    [Google Scholar]
  86. Smith DS, Bailey JK, Shuster SM, Whitham TG 2011. A geographic mosaic of trophic interactions and selection: trees, aphids and birds. J. Evol. Biol. 24:422–29
    [Google Scholar]
  87. Smith DS, Lau MK, Jacobs R, Monroy JA, Shuster SM, Whitham TG 2015. Rapid plant evolution in the presence of an introduced species alters community composition. Oecologia 179:563–72
    [Google Scholar]
  88. Stevens L, Goodnight CJ, Kalisz S 1995. Multilevel selection in natural populations of Impatiens capensis. Am. Nat 145:513–26
    [Google Scholar]
  89. Sthultz CM, Gehring CA, Whitham TG 2009a. Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species. Glob. Change Biol. 15:1949–61
    [Google Scholar]
  90. Sthultz CM, Whitham TG, Kennedy K, Deckert R, Gehring CA 2009b. Genetically-based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species. New Phytol 184:657–67
    [Google Scholar]
  91. Stone AC, Gehring CA, Cobb NS, Whitham TG 2018. Genetic-based susceptibility of a foundation tree to herbivory interacts with climate to influence arthropod community composition, diversity and resilience. Front. Plant Sci. 9:1831
    [Google Scholar]
  92. Strauss SY, Irwin RE. 2004. Ecological and evolutionary consequence of multispecies plant-animal interactions. Annu. Rev. Ecol. Evol. Syst. 21:435–66
    [Google Scholar]
  93. Swenson W, Arendt J, Wilson DS 2000a. Artificial selection of microbial ecosystems for 3‐chloroaniline biodegradation. Environ. Microbiol. 2:564–71
    [Google Scholar]
  94. Swenson W, Wilson DS, Elias R 2000b. Artificial ecosystem selection. PNAS 97:9110–14
    [Google Scholar]
  95. terHorst CP, Zee PC, Heath KD, Miller TE, Pastore AI et al. 2018. Evolution in a community context: trait responses to multiple species interactions. Am. Nat. 191:368–80
    [Google Scholar]
  96. Thompson JN. 1994. The Coevolutionary Process Chicago: Univ. Chicago Press
  97. Turkington R, Harper JL. 1979. The growth, distribution and neighbor relationships of Trifolium repens in a permanent pasture. IV. Fine-scale biotic differentiation. J. Ecol. 76:245–54
    [Google Scholar]
  98. Wade MJ. 1977. An experimental study of group selection. Evolution 31:134–53
    [Google Scholar]
  99. Wade MJ. 1978. A critical review of the models of group selection. Q. Rev. Biol. 53:101–14
    [Google Scholar]
  100. Wade MJ. 1985. Soft selection, hard selection, kin selection, and group selection. Am. Nat. 125:61–73
    [Google Scholar]
  101. Wade MJ. 2007. The co-evolutionary genetics of ecological communities. Nat. Rev. Genet. 8:185–95
    [Google Scholar]
  102. Wade MJ. 2016. Adaptation in Metapopulations: How Interaction Changes Evolution Chicago: Univ. Chicago Press
  103. Wade MJ, Bijma P, Ellen ED, Muir W 2010. Group selection and social evolution in domesticated animals. Evol. Appl. 3:453–65
    [Google Scholar]
  104. Wade MJ, Shuster SM. 2004. Sexual selection: harem size and the variance in male reproductive success. Am. Nat. 164:E83–89
    [Google Scholar]
  105. Ware IM, Fitzpatrick CR, Senthilnathan A, Bayliss SLJ, Beals KK et al. 2019. Feedbacks link ecosystem ecology and evolution across spatial and temporal scales: empirical evidence and future directions. Funct. Ecol. 33:31–42
    [Google Scholar]
  106. Weber MG, Wagner CE, Best RJ, Matthews B 2017. Evolution in a community context: on integrating ecological interactions and macroevolution. Trends Ecol. Evol. 32:291–304
    [Google Scholar]
  107. West-Eberhard MJ. 1989. Phenotypic plasticity and the origin of diversity. Annu. Rev. Ecol. Syst. 20:249–78
    [Google Scholar]
  108. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK et al. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7:510–23
    [Google Scholar]
  109. Whitham TG, Difazio SP, Schweitzer JA, Shuster SM, Allen GJ et al. 2008. Extending genomics to natural communities and ecosystems. Science 320:492–95
    [Google Scholar]
  110. Whitham TG, Gehring CA, Bothwell HM, Cooper HF, Hull JB et al. 2020. Using the Southwest Experimental Garden Array to enhance riparian restoration in response to global change: identifying and deploying genotypes and populations for current and future environments. Riparian Research and Management: Past, Present, Future, Vol. 2 SW Carothers, RR Johnson, DM Finch, KJ Kingsley, RH Hamre 63–79 Gen. Tech. Rep. RMRS-GTR-411 Fort Collins, CO: U.S. Dep. Agric. For. Serv. Rocky Mt. Res. Stn
    [Google Scholar]
  111. Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM et al. 2012. Community specificity: life and afterlife effects of genes. Trends Plant Sci 17:271–81
    [Google Scholar]
  112. Whitham TG, Young WP, Martinsen GD, Gehring CA, Schweitzer JA et al. 2003. Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–73
    [Google Scholar]
  113. Williams AP, Cook ER, Smerdon JE, Cook BI, Abatzoglou JT et al. 2020. Large contribution from anthropogenic warming to an emerging North American megadrought. Science 368:314–18
    [Google Scholar]
  114. Williams GC. 1966. Adaptation and Natural Selection Princeton, NJ: Princeton Univ. Press
  115. Williams HTP, Lenton TM. 2007. Artificial selection of simulated microbial ecosystems. PNAS 104:8918–23
    [Google Scholar]
  116. Wilson DS. 1975. A theory of group selection. PNAS 72:143–46
    [Google Scholar]
  117. Wilson DS. 1983. The group selection controversy: history and current status. Annu. Rev. Ecol. Syst. 14:159–87
    [Google Scholar]
  118. Wilson DS. 1997. Biological communities as functionally organized units. Ecology 78:2018–24
    [Google Scholar]
  119. Wilson DS. 2016. Two meanings of complex adaptive systems. Complexity and Evolution: Toward a New Synthesis for Economics DS Wilson, A Kirman 31–46 Cambridge, MA: MIT Press
    [Google Scholar]
  120. Wimp GM, Young WP, Woolbright SA, Martinsen GD, Keim P, Whitham TG 2004. Conserving plant genetic diversity for dependent animal communities. Ecol. Lett. 7:776–80
    [Google Scholar]
  121. Zilber-Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 2008:32723–35
    [Google Scholar]
  122. Zytynska SE, Fay MF, Penney D, Preziosi RF 2011. Genetic variation in a tropical tree species influences the associated epiphytic plant and invertebrate communities in a complex forest ecosystem. Philos. Trans. R. Soc. B 366:1329–36
    [Google Scholar]
  123. Zytynska SE, Khudr MS, Harris E, Preziosi RF 2012. Genetic effects of tank-forming bromeliads on the associated invertebrate community in a tropic forest system. Oecologia 170:46775
    [Google Scholar]
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