Skip to main content
SpringerLink
Log in

A quantitative genetic approach for predicting ecological change in biological communities

  • ORIGINAL PAPER
  • Published:
Theoretical Ecology Aims and scope Submit manuscript

Abstract

Ecological studies of communities have become increasingly focused on the role of genetics. These studies often conclude that genetics and evolution play an important role in community structure and function. For instance, studies have shown that the structure of insect communities associated with a host plant is heritable and therefore can potentially evolve. However, when studying communities of interacting species two problems are faced: (1) the traits that determine the outcomes of these interactions are often unknown, and (2) communities are normally highly multidimensional (n-dimensional for n species). In order to surmount these problems, we adapt a commonly used approach for studying the evolution of multivariate quantitative traits to the study of biological communities. Specifically, we propose utilizing a community-based genetic covariance matrix (G-matrix) and an associated vector of community selection gradients for predicting changes in community composition, where the “traits” under study are the abundances, or other properties, of various interacting species. This approach capitalizes on the relative ease with which data on the abundance of individuals interacting with individuals of a focal species (e.g., abundances of various herbivorous insects on a plant) can be collected and on the utility of the quantitative genetic approach for predicting multidimensional evolution. In order to evaluate the utility and accuracy of the G-matrix approach for predicting the evolution of communities, we develop and analyze numerical simulations of evolving communities. Results of these simulations show that an approach based on community G-matrices and selection gradients provides a rich understanding of how underlying genetics shape community structure and, in many cases, accurately predicts how community structure changes over time.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrawal AA (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol Ecol Res 7:651–667

    Google Scholar 

  • Agrawal AF, Brodie ED, Rieseberg LH (2001) Possible consequences of genes of major effect: transient changes in the G-matrix. Genetica 112:33–43

    Article  PubMed  Google Scholar 

  • Ando D, Mano SI, Koide N, Nakajima M (2008) Estimation of heritability and genetic correlation of number of abdominal and caudal vertebrae in masu salmon. Fish Sci 74:293–298

    Article  CAS  Google Scholar 

  • Arnold SJ, Bürger R, Hohenlohe PA, Ajie BC, Jones AG (2008) Understanding the evolution and stability of the G-matrix. Evolution 62:2451–2461

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Begin M, Roff DA (2001) An analysis of G matrix variation in two closely related cricket species. Gryllus firmus and G. pennsylvanicus. J Evol Biol 14:1–13

    Article  Google Scholar 

  • Brodie ED III, Ridenhour BJ (2003) Reciprocal selection at the phenotypic interface of coevolution. Integr Comp Biol 43:408–418

    Article  PubMed  Google Scholar 

  • Brodie ED, Ridenhour BJ, Brodie ED (2002) The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067–2082

    Article  PubMed  Google Scholar 

  • Chesson P, Huntly N (1989) Short-term instabilities and long-term community dynamics. Trends In Ecology & Evolution

  • De Caceres M, Legendre P, Wiser SK, Brotons L (2012) Using species combinations in indicator value analyses. Methods Ecol Evol 3:973–982

    Article  Google Scholar 

  • Doroszuk A, Wojewodzic MW, Gort G, Kammenga JE (2008) Rapid divergence of genetic variance–covariance matrix within a natural population. Am Nat 171:291–304

    Article  PubMed  Google Scholar 

  • Elias M, Gompert Z, Jiggins C, Willmott K (2008) Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol 6:e300

    Article  PubMed Central  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, Essex

    Google Scholar 

  • Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. Proc Natl Acad Sci U S Am 100:8916–8920

    Article  CAS  Google Scholar 

  • Grant BS, Owen DF, Clarke CA (1996) Parallel rise and fall of melanic peppered moths in America and Britain. J Hered 87:351–357

    Article  Google Scholar 

  • Grant BS, Cook AD, Clarke CA, Owen DF (1998) Geographic and temporal variation in the incidence of melanism in peppered moth populations in America and Britain. J Hered 89:465–471

    Article  Google Scholar 

  • Guo SW, Thompson EA (1994) Monte Carlo estimation of mixed models for large complex pedigrees. Biometrics 50:417–432

    Article  CAS  PubMed  Google Scholar 

  • Hanski I, Gaggiotti OE (2004) Ecology, genetics, and evolution of metapopulations. Elsevier, Burlington

    Google Scholar 

  • Heywood JS (2005) An exact form of the breeder's equation for the evolution of a quantitative trait under natural selection. Evolution 59:2287–2298

    Article  PubMed  Google Scholar 

  • Hine E, Chenoweth SF, Rundle HD, Blows MW (2009) Characterizing the evolution of genetic variance using genetic covariance tensors. Philos Trans Royal Soc B-Biol Sci 364:1567–1578

    Article  Google Scholar 

  • Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 52:1564–1571

    Article  Google Scholar 

  • Johnson MTJ (2008) Bottom-up effects of plant genotype on aphids, ants, and predators. Ecology 89:145–154

    Article  PubMed  Google Scholar 

  • Johnson MTJ, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22:250–257

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Jones AG, Arnold SJ, Bürger R (2003) Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution 57:1747–1760

    Article  PubMed  Google Scholar 

  • Jones AG, Arnold SJ, Bürger R (2004) Evolution and stability of the G-matrix on a landscape with a moving optimum. Evolution 58:1639–1654

    Article  PubMed  Google Scholar 

  • Jones AG, Arnold SJ, Bürger R (2007) The mutation matrix and the evolution of evolvability. Evolution 61:727–745

    Article  PubMed  Google Scholar 

  • Kaczorowski RL, Juenger TE, Holtsford TP (2008) Heritability and correlation structure of nectar and floral morphology traits in Nicotiana alata. Evolution 62:1738–1750

    Article  PubMed  Google Scholar 

  • Kempthorne O (1997) Heritability: uses and abuses. Genetica 99:109–112

    CAS  PubMed  Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    Article  CAS  PubMed  Google Scholar 

  • Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33:402–416

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Leimu R, Koricheva J (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. Am Nat 168:E15–E37

    Article  PubMed  Google Scholar 

  • Locke SA, McLaughlin JD, Marcogliese DJ (2012) Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122:73–83

    Article  Google Scholar 

  • Losos JB, Leal M, Glor RE, de Queiroz K, Hertz PE, Schettino LR, Lara AC, Jackman TR, Larson A (2003) Niche lability in the evolution of a Caribbean lizard community. Nature 424:542–545

    Article  CAS  PubMed  Google Scholar 

  • Lush JL (1937) Animal breeding plans. Collegiate Press, Ames

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • MacArthur R (1955) Fluctuations of animal populations and a measure of community stability. Ecology 36:533–536

    Article  Google Scholar 

  • Maddox GD, Root RB (1990) Structure of the encounter between goldenrod (Solidago altissima) and its diverse insect fauna. Ecology 71:2115–2124

    Article  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • McCann KS (2000) The diversity–stability debate. Nature 405:228–233

    Article  CAS  PubMed  Google Scholar 

  • Peacor SD, Werner EE (1997) Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78:1146–1156

    Article  Google Scholar 

  • Pearson K (1903) I. Mathematical contributions to the theory of evolution. XI. On the influence of natural selection on the variability and correlation of organs. Philos Trans R Soc Lond, A Phys Sci 200:1–66

    Article  Google Scholar 

  • Phillips P, Arnold S (1999) Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution 53:1506–1515

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ridenhour BJ, Nuismer SL (2012) Perspective: trait-mediated indirect interactions and the coevolutionary process. In: Ohgushi T, Schmitz OJ, Holt RD (eds) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, Cambridge

    Google Scholar 

  • Ritland K (1996) A marker-based method for inferences about quantitative inheritance in natural populations. Evolution 50:1062–1073

    Article  Google Scholar 

  • Ritland K, Ritland C (1996) Inferences about quantitative inheritance based on natural population structure in the Yellow Monkeyflower, Mimulus guttatus. Evolution 50:1074–1082

    Article  Google Scholar 

  • Roche BM, Fritz RS (1997) Genetics of resistance of Salix sericea to a diverse community of herbivores. Evolution 51:1490–1498

    Article  Google Scholar 

  • Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York

    Book  Google Scholar 

  • Rudgers JA, Whitney KD (2006) Interactions between insect herbivores and a plant architectural dimorphism. J Ecol 94:1249–1260

    Article  Google Scholar 

  • Schönemann PH (1997) On models and muddles of heritability. Genetica 99:97–108

    PubMed  Google Scholar 

  • Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant–soil–microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781

    Article  PubMed  Google Scholar 

  • Sekloka E, Lançon J, Goze E, Hau B, Lewicki-Dhainaut S, Thomas G (2008) Breeding new cotton varieties to fit the diversity of cropping conditions in Africa: effect of plant architecture, earliness and effective flowering time on late-planted cotton productivity. Exp Agric 44:197–207

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Smith DS, Bailey JK, Shuster SM, Whitham TG (2010) A geographic mosaic of trophic interactions and selection: trees, aphids and birds. J Evol Biol 24:422–429

    Article  PubMed  Google Scholar 

  • Steppan SJ, Phillips PC, Houle D (2002) Comparative quantitative genetics: evolution of the G matrix. Trends Ecol Evol 17:320–327

    Article  Google Scholar 

  • Stinchcombe JR, Rausher MD (2001) Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomoea hederacea. Am Nat 158:376–388

    Article  CAS  PubMed  Google Scholar 

  • Stoltenberg S (1997) Coming to terms with heritability. Genetica 99:89–96

    CAS  PubMed  Google Scholar 

  • Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant–animal interactions. Annu Rev Ecol Evol Syst 35:435–466

    Article  Google Scholar 

  • Sugiura S, Tsuru T, Yamaura Y (2012) Effects of an invasive alien tree on the diversity and temporal dynamics of an insect assemblage on an oceanic island. Biol Invasions 15:157–169

    Article  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Thompson JN, Nuismer SL, Gomulkiewicz R (2002) Coevolution and maladaptation. Integr Comp Biol 42:381–387

    Article  PubMed  Google Scholar 

  • Turelli M, Barton NH (1994) Genetic and statistical analyses of strong selection on polygenic traits—what, me normal? Genetics 138:913–941

    CAS  PubMed Central  PubMed  Google Scholar 

  • Urban MC, Skelly DK (2006) Evolving metacommunities: toward an evolutionary perspective on metacommunities. Ecology 87:1616–1626

    Article  PubMed  Google Scholar 

  • Wade MJ (2007) The co-evolutionary genetics of ecological communities. Nat Rev Genet 8:185–195

    Article  CAS  PubMed  Google Scholar 

  • Weigensberg I, Roff DA (1996) Natural heritabilities: can they be reliably estimated in the laboratory? Evolution 50:2149–2157

    Article  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 

  • Whitlock RAJ, Grime JP, Booth R, Burke T (2007) The role of genotypic diversity in determining grassland community structure under constant environmental conditions. J Ecol 95:895–907

    Article  CAS  Google Scholar 

  • Wijmenga C, Frants RR, Brouwer OF, Moerer P, Padberg GW (1990) Location of facioscapulohumeral muscular dystrophy gene on chromosome 4. Lancet 336:651–653

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Barrie Robison and Luke Harmon for helpful discussions and William Godsoe, Virginie Poullain, and the anonymous reviewers for comments on earlier versions of the manuscript. A special thanks to Henry C. Chaser for another year of help in the field.

Author information

Authors and Affiliations

  1. Department of Biological Science, University of Notre Dame, 100 Galvin Life Sciences, Notre Dame, IN, 46556, USA

    Benjamin J. Ridenhour

  2. Department of Biological Sciences, University of Idaho, Moscow, ID, USA

    Scott L. Nuismer

Authors
  1. Benjamin J. Ridenhour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Scott L. Nuismer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Benjamin J. Ridenhour.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 64 kb)

ESM 2

(PDF 2405 kb)

ESM 3

(PDF 186 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ridenhour, B.J., Nuismer, S.L. A quantitative genetic approach for predicting ecological change in biological communities. Theor Ecol 7, 137–148 (2014). https://doi.org/10.1007/s12080-013-0206-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12080-013-0206-4

Keywords

Search

Navigation