Review
The ecological causes of evolution

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Natural selection is the process that results in adaptive evolution, but it is not the cause of evolution. The cause of natural selection and, therefore, of adaptive evolution, is any environmental factor (agent of selection) that results in differential fitness among phenotypes. Surprisingly little is known about selective agents, how they interact or their relative importance across taxa. Here, I outline three approaches for their investigation: functional analysis, correlational analysis and experimental manipulation. By refocusing attention on the structure and consequences of ecological variation, a better characterisation of selective agents would improve understanding of natural selection and evolution, including adaptive radiation, coevolution, the niche, the evolutionary ecology of the ranges of species and their response to environmental change.

Section snippets

What causes natural selection?

When one contemplates how understanding of evolution has improved over the 150 years since Darwin first published his ideas about natural selection [1], it might come as a surprise to realise how little is understood about the causes of adaptive evolution in natural populations. Recent developments are causing evolutionary ecologists to think more explicitly about the nature of natural selection: how it varies spatiotemporally 2, 3, 4, 5, the ecology that drives it 6, 7, 8, how adaptation,

Functional analysis

The functional analysis of a trait or polymorphism, in which one infers selective agents from trait function, can be useful in the initial investigation of the causes of selection. For example, extravagant traits used in courtship are probably shaped by the aggression or choice of members of the same species. Clarke's study [16] of the alcohol dehydrogenase (Adh) polymorphism in Drosophila melanogaster is archetypal. The two common alleles (‘F’ and ‘S’) differ in their efficiency of catalysing

Observational data

Correlations between spatiotemporal variation in selection and putative environmental variables might help to identify selective agents [17]. Many studies have documented variation in the strength of selection through space and time. It is unfortunate that the ecological correlates of this have seldom been pursued in depth [5], because such studies afford a real opportunity to identify selective agents. Simple plots of selection metrics against single environmental variables can be revealing

Experimental manipulation of environment

The solution to most of the difficulties inherent in an observational approach to identifying agents of selection is to use an experimental one [17]. Although experimental approaches to the study of natural selection are not uncommon, many involve manipulations of traits or trait distributions 31, 32. These experiments tell little about selective agents, unless environmental factors are manipulated simultaneously. Such combination manipulations are powerful for gaining a full understanding of

Natural selection and evolution

An understanding of natural selection cannot be complete without knowing its causes, their relative importance and how they interact to form the eco-evolutionary landscape. There is currently a resurgence of interest in natural selection, and how its strength varies both spatially and temporally 3, 5, 14. Linking this directly to variation in selective agents would result in a more mechanistic understanding of selection. With an accompanying expectation of h2 or G [37], this would also enable

Concluding remarks

Current understanding of the causes of natural selection and, therefore, of evolution, is poor but could easily be improved by the appropriate analysis of existing data, and new experimental studies that explicitly measure the impact of environmental manipulations on the strength of selection. In particular, there is much to be learned from: (i) exploration of eco-evolutionary landscapes, especially using existing data from long-term evolutionary studies; (ii) meta-analysis of existing

Acknowledgements

I would like to thank Russ Lande for making me aware of the Wade and Kalisz paper, and Ryan Calsbeek, Francis Gilbert, Armand Kuris, Tom Reader, Erik Svensson and two anonymous reviewers for comments on earlier versions of the manuscript.

References (100)

  • R. Calsbeek et al.

    Experimentally assessing the relative importance of predation and competition as agents of selection

    Nature

    (2010)
  • P.A. Flight

    Physiological stress and the fitness effects of Mpi genotypes in the acorn barnacle Semibalanus balanoides

    Mar. Ecol. Prog. Ser.

    (2010)
  • J.J. Wiens

    Niche conservatism as an emerging principle in ecology and conservation biology

    Ecol. Lett.

    (2010)
  • J.B. Yoder

    Ecological opportunity and the origin of adaptive radiations

    J. Evol. Biol.

    (2010)
  • J.P. Sexton

    Evolution and ecology of species range limits

    Ann. Rev. Ecol. Evol. Syst.

    (2009)
  • R.K. Colwell et al.

    Hutchinson's duality: the once and future niche

    Proc. Natl. Acad. Sci. U.S.A.

    (2009)
  • L.M. Chevin

    Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory

    PLoS Biol.

    (2010)
  • H.W. Bates

    Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidæ

    Trans. Linn. Soc. Lond.

    (1861)
  • B. Clarke

    Contribution of ecological genetics to evolutionary theory – detecting direct effects of natural selection on particular polymorphic loci

    Genetics

    (1975)
  • M.J. Wade et al.

    The causes of natural selection

    Evolution

    (1990)
  • A. Charmantier

    Adaptive phenotypic plasticity in response to climate change in a wild bird population

    Science

    (2008)
  • S.M. Carlson et al.

    Ten years of varying lake level and selection on size-at-maturity in Sockeye Salmon

    Ecology

    (2007)
  • G.G. Simpson

    The Major Features of Evolution

    (1953)
  • D. Schluter

    The Ecology of Adaptive Radiation

    (2000)
  • D. Garant

    Evolution in a changing environment: a case study with great tit fledging mass

    Am. Nat.

    (2004)
  • J. Clobert

    Survival rate in the great tit Parus major in relation to sex, age, and immigration status

    J. Anim. Ecol.

    (1988)
  • D. Schluter

    Estimating the form of natural selection on a quantitative trait

    Evolution

    (1988)
  • R. Lande et al.

    The measurement of selection on correlated characters

    Evolution

    (1983)
  • K.J. Gaston

    The Structure and Dynamics of Geographic Ranges

    (2003)
  • A.F. Agrawal et al.

    How much do genetic covariances alter the rate of adaptation?

    Proc. R. Soc. Lond. Ser. B: Biol. Sci.

    (2009)
  • M.D. Rausher

    The measurement of selection on quantitative traits – biases due to environmental covariances between traits and fitness

    Evolution

    (1992)
  • R. Stoks

    Phenotypic shifts caused by predation: selection or life-history shifts?

    Evol. Ecol.

    (1999)
  • R.H. Kaplan et al.

    Ecological and developmental context of natural selection: maternal effects and thermally induced plasticity in the frog Bombina orientalis

    Evolution

    (2006)
  • B.R. Anholt

    Measuring selection on a population of damselflies with a manipulated phenotype

    Evolution

    (1991)
  • B. Sinervo

    Allometric engineering–a causal analysis of natural selection on offspring size

    Science

    (1992)
  • E. Svensson et al.

    Experimental excursions on adaptive landscapes: density-dependent selection on egg size

    Evolution

    (2000)
  • L. Fishman et al.

    Pollen limitation and natural selection on floral characters in the yellow monkeyflower, Mimulus guttatus

    New Phytol.

    (2008)
  • S. Sandring et al.

    Pollinator-mediated selection on floral display and flowering time in the perennial herb Arabidopsis lyrata

    Evolution

    (2009)
  • P. Tiffin et al.

    Measuring tolerance to herbivory: accuracy and precision of estimates made using natural versus imposed damage

    Evolution

    (2000)
  • A. Charmantier et al.

    Environmental quality and evolutionary potential: lessons from wild populations

    Proc. R. Soc. Lond. Ser. B: Biol. Sci.

    (2005)
  • M.A. McPeek

    Linking local species interactions to rates of speciation in communities

    Ecology

    (1996)
  • A.P. Hendry

    Ecological speciation! Or the lack thereof?

    Can. J. Fish. Aquat. Sci.

    (2009)
  • P. Nosil et al.

    Ecological niche dimensionality and the evolutionary diversification of stick insects

    PLoS ONE

    (2008)
  • E.B. Taylor

    Species pairs of north temperate freshwater fishes: evolution, taxonomy, and conservation

    Rev. Fish Biol. Fish.

    (1999)
  • R. Knudsen

    Temporal stability of individual feeding specialization may promote speciation

    J. Anim. Ecol.

    (2010)
  • M. Bertrand

    Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics

    J. Fish Biol.

    (2008)
  • A.D.C MacColl

    Parasite burdens differ between sympatric three-spined stickleback species

    Ecography

    (2009)
  • B. Sinervo et al.

    Correlational selection and the evolution of genomic architecture

    Heredity

    (2002)
  • M.C. Whitlock

    Founder effects and peak shifts without genetic drift: adaptive peak shifts occur easily when environments fluctuate slightly

    Evolution

    (1997)
  • J.N. Thompson

    The Geographic Mosaic of Coevolution

    (2005)
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