Article

The ecological importance of intraspecific variation

  • Nature Ecology & Evolution 25764 (2018)
  • doi:10.1038/s41559-017-0402-5
  • Download Citation
Received:
Accepted:
Published online:

Abstract

Human activity is causing wild populations to experience rapid trait change and local extirpation. The resulting effects on intraspecific variation could have substantial consequences for ecological processes and ecosystem services. Although researchers have long acknowledged that variation among species influences the surrounding environment, only recently has evidence accumulated for the ecological importance of variation within species. We conducted a meta-analysis comparing the ecological effects of variation within a species (intraspecific effects) with the effects of replacement or removal of that species (species effects). We evaluated direct and indirect ecological responses, including changes in abundance (or biomass), rates of ecological processes and changes in community composition. Our results show that intraspecific effects are often comparable to, and sometimes stronger than, species effects. Species effects tend to be larger for direct ecological responses (for example, through consumption), whereas intraspecific effects and species effects tend to be similar for indirect responses (for example, through trophic cascades). Intraspecific effects are especially strong when indirect interactions alter community composition. Our results summarize data from the first generation of studies examining the relative ecological effects of intraspecific variation. Our conclusions can help inform the design of future experiments and the formulation of strategies to quantify and conserve biodiversity.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Brooks, J. & Dodson, S. I. Predation, body size, and composition of plankton. Science 150, 28–35 (1965).

  2. 2.

    Power, M. E. et al. Challenges in the quest for keystones. Bioscience 46, 609–620 (1996).

  3. 3.

    Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108 (2012).

  4. 4.

    Violle, C. et al. The return of the variance: intraspecific variability in community ecology. Trends Ecol. Evol. 27, 245–253 (2012).

  5. 5.

    Bailey, J. K. et al. From genes to ecosystems: an emerging synthesis of eco-evolutionary dynamics. New Phytol. 184, 746–749 (2009).

  6. 6.

    Bolnick, D. I. et al. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011).

  7. 7.

    Stockwell, C. A., Hendry, A. P. & Kinnison, M. T. Contemporary evolution meets conservation biology. Trends Ecol. Evol. 18, 94–101 (2003).

  8. 8.

    Schoener, T. W. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331, 426–429 (2011).

  9. 9.

    Post, D. M. et al. Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Phil. Trans. R. Soc. B 364, 1629–1640 (2009).

  10. 10.

    Hairston, N. G., Ellner, S. P., Geber, M. A., Yoshida, T. & Fox, J. A. Rapid evolution and the convergence of ecological and evolutionary time. Ecol. Lett. 8, 1114–1127 (2005).

  11. 11.

    Albert, C. H. et al. A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits. Funct. Ecol. 24, 1192–1201 (2010).

  12. 12.

    Palkovacs, E. P. & Post, D. M. Experimental evidence that phenotypic divergence in predators drives community divergence in prey. Ecology 90, 300–305 (2009).

  13. 13.

    Harmon, L. J. et al. Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458, 1167–1170 (2009).

  14. 14.

    Crutsinger, G. M., Sanders, N. J. & Classen, A. T. Comparing intra- and inter-specific effects on litter decomposition in an old-field ecosystem. Basic Appl. Ecol. 10, 535–543 (2009).

  15. 15.

    Kinnison, M. T. & Hairston, N. G. J. Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct. Ecol. 21, 444–454 (2007).

  16. 16.

    Govaert, L., Pantel, J. H. & De Meester, L. Eco-evolutionary partitioning metrics: assessing the importance of ecological and evolutionary contributions to population and community change. Ecol. Lett. 19, 839–853 (2016).

  17. 17.

    Schweitzer, J. A. et al. Forest gene diversity is correlated with the composition and function of soil microbial communities. Popul. Ecol. 53, 35–46 (2011).

  18. 18.

    Genung, M. A., Bailey, J. K. & Schweitzer, J. A. Welcome to the neighbourhood: interspecific genotype by genotype interactions in Solidago influence above- and belowground biomass and associated communities. Ecol. Lett. 15, 65–73 (2012).

  19. 19.

    Moritz, C. Defining ‘evolutionarily significant units’ for conservation. Trends Ecol. Evol. 9, 373–375 (1994).

  20. 20.

    Palkovacs, E. P., Kinnison, M. T., Correa, C., Dalton, C. M. & Hendry, A. P. Fates beyond traits: ecological consequences of human-induced trait change. Evol. Appl. 5, 183–191 (2012).

  21. 21.

    Angelini, C. et al. Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61, 782–789 (2011).

  22. 22.

    Hughes, J. B., Daily, G. C. & Ehrlich, P. R. Population diversity: its extent and extinction. Science 278, 689–692 (1997).

  23. 23.

    Miraldo, A. et al. An Anthropocene map of genetic diversity. Science 353, 1532–1535 (2016).

  24. 24.

    Ceballos, G., Ehrlich, P. R. & Dirzo, R. Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc. Natl Acad. Sci. USA 114, E6089–E6096 (2017).

  25. 25.

    Mimura, M. et al. Understanding and monitoring the consequences of human impacts on intraspecific variation. Evol. Appl. 10, 121–139 (2017).

  26. 26.

    Richardson, J. L., Urban, M. C., Bolnick, D. I. & Skelly, D. K. Microgeographic adaptation and the spatial scale of evolution. Trends Ecol. Evol. 29, 165–176 (2014).

  27. 27.

    West-Eberhard, M. J. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249–278 (1989).

  28. 28.

    Hendry, A. P. Eco-evolutionary Dynamics (Princeton Univ. Press, Princeton, 2017).

  29. 29.

    Des Roches, S., Shurin, J. B., Schluter, D. & Harmon, L. J. Ecological and evolutionary effects of stickleback on community structure. PLoS ONE 8, e59644 (2013).

  30. 30.

    Chislock, M. F., Sarnelle, O., Olsen, B. K., Doster, E. & Wilson, A. E. Large effects of consumer offense on ecosystem structure and function. Ecology 94, 2375–2380 (2013).

  31. 31.

    Royauté, R. & Pruitt, J. N. Varying predator personalities generates contrasting prey communities in an agroecosystem. Ecology 96, 2902–2911 (2015).

  32. 32.

    Bowatte, S. et al. Offspring of plants exposed to elevated or ambient CO2 differ in their impacts on soil nitrification in a common garden experiment. Soil Biol. Biochem. 62, 134–136 (2013).

  33. 33.

    Olden, J. D., Poff, N. L., Douglas, M. R., Douglas, M. E. & Fausch, K. D. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol. Evol. 19, 18–24 (2004).

  34. 34.

    Farkas, T. E., Mononen, T., Comeault, A. A., Hanski, I. & Nosil, P. Evolution of camouflage drives rapid ecological change in an insect community. Curr. Biol. 23, 1835–1843 (2013).

  35. 35.

    Urban, M. C. Evolution mediates the effects of apex predation on aquatic food webs. Proc. R. Soc. B 280, 20130859 (2013).

  36. 36.

    Charette, C. & Derry, A. M. Climate alters intraspecific variation in copepod effect traits through pond food webs. Ecology 97, 1239–1250 (2016).

  37. 37.

    Wootton, J. T. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25, 443–466 (1994).

  38. 38.

    Cohen, J. Statistical Power Analysis for the Behavioral Sciences 2nd edn (Lawrence Erlbaum Associates, Mahwah, 1988).

  39. 39.

    Fussmann, G. F., Loreau, M. & Abrams, P. A. Eco-evolutionary dynamics of communities and ecosystems. Funct. Ecol. 21, 465–477 (2007).

  40. 40.

    Weber, M. G., Wagner, C. E., Best, R. J., Harmon, L. J. & Matthews, B. Evolution in a community context: on integrating ecological interactions and macroevolution. Trends Ecol. Evol. 32, 291–304 (2017).

  41. 41.

    Read, Q. D. et al. Accounting for the nested nature of genetic variation across levels of organization improves our understanding of biodiversity and community ecology. Oikos 125, 895–904 (2016).

  42. 42.

    Tessier, A. J. & Woodruff, P. Cryptic trophic cascade along a gradient of lake size. Ecology 83, 1263–1270 (2002).

  43. 43.

    Hazard, C., Kruitbos, L., Davidson, H., Taylor, A. F. S. & Johnson, D. Contrasting effects of intra- and interspecific identity and richness of ectomycorrhizal fungi on host plants, nutrient retention and multifunctionality. New Phytol. 213, 852–863 (2016).

  44. 44.

    Fridley, J. D. & Grime, J. P. Community ecosystem effects of intraspecific genetic diversity in microcosms of grassland varying species diversity. Ecology 91, 2272–2283 (2010).

  45. 45.

    Ohgushi, T. Herbivore-induced effects through trait change in plants. Annu. Rev. Ecol. Evol. Syst. 36, 81–105 (2005).

  46. 46.

    Müller, M. S. et al. Tri-trophic effects of plant defenses: chickadees consume caterpillars based on host leaf chemistry. Oikos 114, 507–517 (2006).

  47. 47.

    Weis, J. J. & Post, D. M. Intraspecific variation in a predator drives cascading variation in primary producer community composition. Oikos 122, 1343–1349 (2013).

  48. 48.

    Crutsinger, G. M. et al. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313, 966–968 (2006).

  49. 49.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

  50. 50.

    Jump, A. S., Marchant, R. & Peñuelas, J. Environmental change and the option value of genetic diversity. Trends Plant Sci. 14, 51–58 (2009).

  51. 51.

    Nosek, B. A. et al. Promoting an open research culture. Science 348, 1422–1425 (2015).

  52. 52.

    Moher, D., Liberati, A., Tetzlaff, J. & Altman, D. G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6, e1000097 (2009).

  53. 53.

    Li, Y., Dicke, M., Harvey, J. A. & Gols, R. Intra-specific variation in wild Brassica oleracea for aphid-induced plant responses and consequences for caterpillar–parasitoid interactions. Oecologia 174, 853–862 (2014).

  54. 54.

    Compson, Z. G. et al. Plant genotype influences aquatic–terrestrial ecosystem linkages through timing and composition of insect emergence. Ecosphere 7, 1–20 (2016).

  55. 55.

    Hargrave, C. W., Hambright, K. D. & Weider, L. J. Variation in resource consumption across a gradient of increasing intra- and interspecific richness. Ecology 92, 1226–1235 (2011).

  56. 56.

    Walsh, M. R., Delong, J. P., Hanley, T. C. & Post, D. M. A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function. Proc. R. Soc. B 279, 3184–3192 (2012).

  57. 57.

    Strauss, S. Y. Indirect effects in community ecology: their definition, study and importance. Trends Ecol. Evol. 6, 206–210 (1991).

  58. 58.

    Balvanera, P. et al. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146–1156 (2006).

  59. 59.

    Palkovacs, E. P., Fryxell, D. C., Turley, N. E. & Post, D. M. in Aquatic Functional Biodiversity (eds Belgrano, A., Woodward, G. & Jacob, U.) 37–51 (Elsevier, London, 2015).

  60. 60.

    Hedges, L. V. Distribution theory for Glass’s estimator of effect size and related estimators. J. Educ. Stat. 6, 107–128 (1981).

  61. 61.

    Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

  62. 62.

    Viechtbauer, W. Accounting for heterogeneity via random-effects models and moderator analyses in meta-analysis. J. Psychol. 215, 104–121 (2007).

  63. 63.

    Konstantopoulos, S. Fixed effects and variance components estimation in three-level meta-analysis. Res. Synth. Methods 2, 61–76 (2011).

  64. 64.

    Calcagno, V. & de Mazancourt, C. glmulti: an R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. 34, 1–29 (2010).

  65. 65.

    Rosenthal, R. The ‘file drawer problem’ and tolerance for null results. Psychol. Bull. 86, 638–641 (1979).

  66. 66.

    Egger, M., Smith, G. D., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 624–629 (1997).

  67. 67.

    Ingram, T. et al. Intraguild predation drives evolutionary niche shift in threespine stickleback. Evolution 66, 1819–1832 (2012).

  68. 68.

    Rudman, S. M. et al. Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem. Proc. R. Soc. B 282, 20151234 (2015).

  69. 69.

    Rudman, S. M. & Schluter, D. Ecological impacts of reverse speciation in threespine stickleback. Curr. Biol. 26, 490–495 (2016).

  70. 70.

    Matthews, B., Aebischer, T., Sullam, K. E., Lundsgaard-Hansen, B. & Seehausen, O. Experimental evidence of an eco-evolutionary feedback during adaptive divergence. Curr. Biol. 26, 483–489 (2016).

  71. 71.

    Post, D. M., Palkovacs, E. P., Schielke, E. G. & Dodson, S. I. Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89, 2019–2032 (2008).

  72. 72.

    Howeth, J. G., Weis, J. J., Brodersen, J., Hatton, E. C. & Post, D. M. Intraspecific phenotypic variation in a fish predator affects multitrophic lake metacommunity structure. Ecol. Evol. 3, 5031–5044 (2013).

  73. 73.

    Katano, O. Effects of individual differences in foraging of pale chub on algal biomass through trophic cascades. Environ. Biol. Fishes 92, 101–112 (2011).

  74. 74.

    Palkovacs, E. P. et al. Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams. Phil. Trans. R. Soc. B 364, 1617–1628 (2009).

  75. 75.

    Bassar, R. D. et al. Local adaptation in Trinidadian guppies alters ecosystem processes. Proc. Natl Acad. Sci. USA 107, 3616–3621 (2010).

  76. 76.

    McArt, S. H., Cook-Patton, S. C. & Thaler, J. S. Relationships between arthropod richness, evenness, and diversity are altered by complementarity among plant genotypes. Oecologia 168, 1013–1021 (2012).

  77. 77.

    Shuster, S. M., Lonsdorf, E. V., Wimp, G. M., Bailey, J. K. & Whitham, T. G. Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60, 991–1003 (2006).

  78. 78.

    Schweitzer, J. A. et al. Plant–soil–microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89, 773–781 (2008).

  79. 79.

    Lojewski, N. R. et al. Genetic basis of aboveground productivity in two native Populus species and their hybrids. Tree Physiol. 29, 1133–1142 (2009).

  80. 80.

    Lojewski, N. R. et al. Genetic components to belowground carbon fluxes in a riparian forest ecosystem: a common garden approach. New Phytol. 195, 631–639 (2012).

Download references

Acknowledgements

We thank the researchers who made their data available for our analysis. We thank K. Kroeker for helpful conversations about the analyses and R. M. Segnitz and members of the Palkovacs Lab for help with preparation of the paper. Funding was provided by the Quebec Centre for Biodiversity Science, bioGENESIS, Future Earth, University of California Institute for the Study of Ecological and Evolutionary Climate Impacts, David and Lucile Packard Foundation and the National Science Foundation (DEB no. 1457333 and DEB no. 1556378).

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, 95060, USA

    • Simone Des Roches
    •  & Eric P. Palkovacs
  2. Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, 06511, USA

    • David M. Post
  3. Department of Biology, University of Central Florida, Orlando, FL, 32816, USA

    • Nash E. Turley
  4. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, 37996, USA

    • Joseph K. Bailey
    •  & Jennifer A. Schweitzer
  5. Redpath Museum and Department of Biology, McGill University, Montreal, QC, H3A 2K6, Canada

    • Andrew P. Hendry
  6. School of Biology and Ecology, University of Maine, Orono, ME, 04469, USA

    • Michael T. Kinnison

Authors

  1. Search for Simone Des Roches in:

  2. Search for David M. Post in:

  3. Search for Nash E. Turley in:

  4. Search for Joseph K. Bailey in:

  5. Search for Andrew P. Hendry in:

  6. Search for Michael T. Kinnison in:

  7. Search for Jennifer A. Schweitzer in:

  8. Search for Eric P. Palkovacs in:

Contributions

All authors developed the study idea and participated in data collection. S.D., D.M.P., N.E.T. and E.P.P. performed the statistical analyses. S.D., D.M.P. and E.P.P. led the writing of the paper. All authors prepared and edited the final drafts.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Simone Des Roches.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Table 1, Supplementary Figure 1

  2. Life Sciences Reporting Summary