Skip to main content
SpringerLink
Log in

Neighbours matter: natural selection on plant size depends on the identity and diversity of the surrounding community

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Plant diversity can affect ecological processes such as competition and herbivory, and these ecological processes can act as drivers of evolutionary change. However, surprisingly little is known about how ecological variation in plant diversity can alter selective regimes on members of the community. Here, we examine how plant diversity at two different scales (genotypic and species diversity) impacts natural selection on a focal plant species, the common evening primrose (Oenothera biennis). Because competition is frequently relaxed in both genotypically and species rich plant communities, we hypothesized that increasing diversity would weaken selection on competitive ability. Changes in plant diversity can also affect associated arthropod communities. Therefore, we hypothesized that diversity would alter selection on plant traits mediating these interactions, such as herbivory related traits. We grew 24 focal O. biennis genotypes within four different neighbourhoods: genotypic monocultures or polycultures of O. biennis, and species monocultures or polycultures of old-field species that commonly co-occur with O. biennis. We then measured genotypic selection on nine plant traits known to be ecologically important for competition and herbivory. Focal O. biennis plants were smaller, flowered for shorter periods of time, had lower fitness, and experienced greater attack from specialist predispersal seed predators when grown with conspecifics versus heterospecifics. While neither conspecific nor heterospecific diversity altered trait means, both types of diversity altered the strength of selection on focal O. biennis plants. Specifically, selection on plant biomass was stronger in conspecific monocultures versus polycultures, but weaker in heterospecific monocultures versus polycultures. We found no evidence of selection on plant traits that mediate insect interactions, despite differences in arthropod communities on plants surrounded by conspecifics versus heterospecifics. Our data demonstrate that plant genotypic and species diversity can act as agents of natural selection, potentially driving evolutionary changes in plant communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432

    Article  Google Scholar 

  • Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen J-P (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116

    Article  PubMed  CAS  Google Scholar 

  • Agrawal AA, Johnson MTJ, Hastings AP, Maron JL (2013) A field experiment demonstrating plant life-history evolution and its eco-evolutionary feedback to seed predator populations. Am Nat 181:S35–S45

    Article  PubMed  Google Scholar 

  • Ashman TL, Morgan MT (2004) Explaining phenotypic selection on plant attractive characters: male function, gender balance or ecological context? Proc R Soc Lond Ser B Biol Sci 271:553–559

    Article  Google Scholar 

  • Becks L, Ellner SP, Jones LE, Hairston NG (2010) Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics. Ecol Lett 13:989–997

    PubMed  Google Scholar 

  • Benkman CW (2013) Biotic interaction strength and the intensity of selection. Ecol Lett 16:1054–1060

    Article  PubMed  Google Scholar 

  • Bennett AB, Gratton C (2013) Floral diversity increases beneficial arthropod richness and decreases variability in arthropod community composition. Ecol Appl 23:86–95

    Article  PubMed  Google Scholar 

  • Brodie ED III, Moore AJ, Janzen FJ (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 10:313–318

    Article  PubMed  Google Scholar 

  • Callaway RM, Brooker R, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848

    Article  PubMed  CAS  Google Scholar 

  • Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci USA 104:18123–18128

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592

    Article  PubMed  Google Scholar 

  • Caruso CM (2000) Competition for pollination influences selection on floral traits of Ipomopsis aggregata. Evolution 54:1546–1557

    Article  PubMed  CAS  Google Scholar 

  • Caruso CM (2001) Differential selection on floral traits of Ipomopsis aggregata growing in contrasting environments. Oikos 94:295–302

    Article  Google Scholar 

  • Clark JS (2010) Individuals and the variation needed for high species diversity in forest trees. Science 327:1129–1132

    Article  PubMed  CAS  Google Scholar 

  • Cleland RE (1972) Oenothera: cytogenetics and evolution. Academic Press, New York

    Google Scholar 

  • Conner J, Hartl D (2004) A primer of ecological genetics. Sinauer Associates, Sunderland

    Google Scholar 

  • Cook-Patton SC, McArt SH, Parachnowitsch AL, Thaler JS, Agrawal AA (2011) A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92:915–923

    Article  PubMed  Google Scholar 

  • Crawford KM, Rudgers JA (2012a) Genetic diversity within a dominant plant outweighs plant species diversity in structuring an arthropod community. Ecology 94:1025–1035

  • Crawford KM, Rudgers JA (2012b) Plant species diversity and genetic diversity within a dominant species interactively affect plant community biomass. J Ecol 100:1512–1521

  • Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968

    Article  PubMed  CAS  Google Scholar 

  • Crutsinger GM, Cadotte MW, Sanders NJ (2009) Plant genetics shapes inquiline community structure across spatial scales. Ecol Lett 12:285–292

    Article  PubMed  Google Scholar 

  • De Mazancourt C, Johnson E, Barraclough TG (2008) Biodiversity inhibits species’ evolutionary responses to changing environments. Ecol Lett 11:380–388

    Article  PubMed  Google Scholar 

  • Donohue K, Messiqua D, Pyle EH, Heschel MS, Schmitt J (2000) Evidence of adaptive divergence in plasticity: density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution 54:1956–1968

    Article  PubMed  CAS  Google Scholar 

  • Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465

    Article  Google Scholar 

  • Fridley JD, Grime JP (2010) Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity. Ecology 91:2272–2283

    Article  PubMed  Google Scholar 

  • Genung MA, Lessard JP, Brown CB, Bunn WA, Cregger MA, Reynolds WN, Felker-Quinn E, Stevenson ML, Hartley AS, Crutsinger GM, Schweitzer JA, Bailey JK (2010) Non-additive effects of genotypic diversity increase floral abundance and abundance of floral visitors. PLoS One 5:e8711

    Article  PubMed  PubMed Central  Google Scholar 

  • Genung MA, Bailey JK, Schweitzer JA (2012) Welcome to the neighbourhood: interspecific genotype by genotype interactions in Solidago influence above- and belowground biomass and associated communities. Ecol Lett 15:65–73

    Article  PubMed  Google Scholar 

  • Goldberg DE, Barton AM (1992) Patterns and consequences of interspecific competition in natural communities: a review of field experiments with plants. Am Nat 139:771–801

    Article  Google Scholar 

  • Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A meta-analysis of competition in field experiments. Am Nat 140(4):539–72

  • Haddad NM, Tilman D, Haarstad J, Ritchie M, Knops JMH (2001) Contrasting effects of plant richness and composition on insect communities: a field experiment. Am Nat 158:17–35

    Article  PubMed  CAS  Google Scholar 

  • Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039

    Article  PubMed  Google Scholar 

  • Hersch-Green EI, Turley NE, Johnson MTJ (2011) Community genetics: what have we accomplished and where should we be going? Phil Tran R Soc B Biol Sci 366:1453–1460

    Article  Google Scholar 

  • Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35

    Article  Google Scholar 

  • Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623

    Article  PubMed  Google Scholar 

  • Johnson MTJ (2007) Genotype-by-environment interactions lead to variable selection on life-history strategy in common evening primrose (Oenothera biennis). J Evol Biol 20:190–200

    Article  PubMed  CAS  Google Scholar 

  • Johnson MTJ (2011) The contribution of evening primrose (Oenothera biennis) to a modern synthesis of evolutionary ecology. Popul Ecol 53:9–21

    Article  Google Scholar 

  • Johnson MTJ, Agrawal AA (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–885

    Article  Google Scholar 

  • Johnson MTJ, Lajeunesse MJ, Agrawal AA (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol Lett 9:24–34

    PubMed  Google Scholar 

  • Johnson MTJ, Agrawal AA, Maron JL, Salminen JP (2009a) Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. J Evol Biol 22:1295–1307

    Article  PubMed  CAS  Google Scholar 

  • Johnson MTJ, Vellend M, Stinchcombe JR (2009b) Evolution in plant populations as a driver of ecological changes in arthropod communities. Phil Tran R Soc B Biol Sci 364:1593–1605

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Lankau RA, Strauss SY (2007) Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317:1561–1563

    Article  PubMed  CAS  Google Scholar 

  • Larson E, Bogdanowicz S, Agrawal A, Johnson M, Harrison R (2008) Permanent genetic resources: isolation and characterization of polymorphic microsatellite loci in common evening primrose (Oenothera biennis). Mol Ecol Res 8:434–436

    Article  CAS  Google Scholar 

  • Lau JA (2008) Beyond the ecological: biological invasions alter natural selection on a native plant species. Ecology 89:1023–1031

    Article  PubMed  Google Scholar 

  • MacColl ADC (2011) The ecological causes of evolution. Trends Ecol Evol 26:514–522

    Article  PubMed  Google Scholar 

  • McArt SH, JS Thaler (2013) Plant genotypic diversity reduces the rate of consumer resource utilization. Proc R Soc Ser B: Biol Sci 280:20130639

  • McArt SH, Cook-Patton SC, Thaler JS (2012) Relationships between arthropod richness, evenness, and diversity are altered by complementarity among plant genotypes. Oecologia 168:1013–1021

    Article  PubMed  Google Scholar 

  • McArt SH, Halitschke R, Salminen J-P, Thaler JS (2013) Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology 94:966–975

    Article  Google Scholar 

  • Meziane D, Shipley B (2001) Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply. Ann Bot 88:915–927

    Article  Google Scholar 

  • Morgan DC, Smith H (1981) Non-photosynthetic responses to light quality. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological Plant Ecology I. Springer, Berlin, pp 109–134

    Chapter  Google Scholar 

  • Mulder CPH, Koricheva J, Huss-Dannell K, Högberg P, Joshi J (1999) Insects affect relationships between plant species richness and ecosystem processes. Ecol Lett 2:237–46

  • Parachnowitsch AL, Caruso CM (2008) Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89:1802–1810

    Article  PubMed  Google Scholar 

  • Parachnowitsch AL, Kessler A (2010) Pollinators exert natural selection on flower size and floral display in Penstemon digitalis. New Phytol 188:393–402

    Article  PubMed  Google Scholar 

  • Parker JD, Salminen J-P, Agrawal AA (2010) Herbivory enhances positive effects of plant genotypic diversity. Ecol Lett 13:553–563

    Article  PubMed  Google Scholar 

  • Rausher MD (1992) The measurement of selection on quantitative traits—biases due to environmental covariances between traits and fitness. Evolution 46:616–626

    Article  Google Scholar 

  • Ridenhour BJ (2005) Identification of selective sources: partitioning selection based on interactions. Am Nat 166:12–25

    Article  PubMed  Google Scholar 

  • Smith RA, Rausher MD (2008) Experimental evidence that selection favors character displacement in the ivyleaf morning glory. Am Nat 171:1–9

    Article  PubMed  Google Scholar 

  • Strauss SY, Lau JA, Schoener TW, Tiffin P (2008) Evolution in ecological field experiments: implications for effect size. Ecol Lett 11:199–207

    Article  PubMed  Google Scholar 

  • Tack AJM, Johnson MTJ, Roslin T (2012) Sizing up community genetics: it’s a matter of scale. Oikos 121:481–488

    Article  Google Scholar 

  • Tiffin P (2002) Competition and time of damage affect the pattern of selection action on plant defense against herbivores. Ecology 83:1981–1990

    Article  Google Scholar 

  • Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. (MPB-26). Princeton University Press, Princeton

  • Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720

    Article  CAS  Google Scholar 

  • Turcotte MM, Corrin MSC, Johnson MTJ (2012) Adaptive evolution in ecological communities. PLoS Biol 10(5):e1001332

  • Vellend M (2006) The consequences of genetic diversity in competitive communities. Ecology 87:304–311

    Article  PubMed  Google Scholar 

  • Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781

    Article  Google Scholar 

  • Wade MJ, Kalisz S (1990) The causes of natural selection. Evolution 44:1947–1955

    Article  Google Scholar 

  • Weinig C (2000) Differing selection in alternative competitive environments: shade-avoidance responses and germination timing. Evolution 54:124–136

    Article  PubMed  CAS  Google Scholar 

  • Whitham TG, Young WP, Martinsen GD, Gehring CA, Schweitzer JA, Shuster SM, Wimp GM, Fischer DG, Bailey JK, Lindroth RL, Woolbright S, Kuske CR (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573

    Article  Google Scholar 

Download references

Acknowledgments

An NSF IGERT grant in Biogeochemistry and Environmental Biocomplexity supported this research, and C. Becker, S. Campbell, A. Erwin, M. Kersch- Becker, P. Llambias, G. Petchenka, M. Stastny, and numerous Cornell undergraduates provided field assistance. Thanks to M. Johnson, S. Karrenberg and N. Sletvold for feedback on analyses, and A. Agrawal and J. Thaler for support and encouragement on this multifaceted experiment. Three anonymous reviewers, as well as the plant–insect interaction groups at Uppsala and Cornell provided useful comments that greatly improved the manuscript.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, 75236, Uppsala, Sweden

    Amy L. Parachnowitsch

  2. Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA

    Susan C. Cook-Patton

  3. Department of Biology, University of Massachusetts-Amherst, Amherst, MA, 01003, USA

    Scott H. McArt

Authors
  1. Amy L. Parachnowitsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan C. Cook-Patton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Scott H. McArt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amy L. Parachnowitsch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 52 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parachnowitsch, A.L., Cook-Patton, S.C. & McArt, S.H. Neighbours matter: natural selection on plant size depends on the identity and diversity of the surrounding community. Evol Ecol 28, 1139–1153 (2014). https://doi.org/10.1007/s10682-014-9727-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-014-9727-6

Keywords

Search

Navigation