Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Evolutionary and ecological functional genomics

Nature Reviews Genetics volume 4, pages 649–655 (2003)Cite this article

Abstract

A unique combination of disciplines is emerging — evolutionary and ecological functional genomics — which focuses on the genes that affect ecological success and evolutionary fitness in natural environments and populations. Already this approach has provided new insights that were not available from its disciplinary components in isolation. However, future advances will necessitate the re-engineering of scientific attitudes, training and institutions, to achieve extensive multidisciplinarity.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Criteria for model species in evolutionary and ecological functional genomics.
Figure 2: Model organisms for evolutionary and ecological functional genomics.
Figure 3: Variation in mouse coat colour.

References

  1. Bartholomew, G. A. in New Directions in Ecological Physiology (eds. Feder, M. E., Bennett, A. F., Burggren, W. W. & Huey, R. B.) 11–35 (Cambridge Univ. Press, Cambridge, 1987).

    Google Scholar 

  2. Feder, M. E. in New Directions in Comparative Developmental Physiology (eds. Burggren, W. W. & Warburton, S.) (in the press).

  3. Mitchell-Olds, T. Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol. Evol. 16, 693–700 (2001).

    Article  Google Scholar 

  4. Oleksiak, M., Churchill, G. & Crawford, D. Variation in gene expression within and among natural populations. Nature Genet. 32, 261–266 (2002).

    Article  CAS  Google Scholar 

  5. Rifkin, S. A., Kim, J. & White, K. P. Evolution of gene expression in the Drosophila melanogaster subgroup. Nature Genet. 33, 138–144 (2003).

    Article  CAS  Google Scholar 

  6. Glazier, A. M., Nadeau, J. H. & Aitman, T. J. Finding genes that underlie complex traits. Science 298, 2345–2349 (2002).

    Article  CAS  Google Scholar 

  7. Ford, M. J. Application of selective neutrality tests to molecular ecology. Mol. Ecol. 11, 1245–1262 (2002).

    Article  CAS  Google Scholar 

  8. Meagher, T. R. & Futuyma, D. Evolution, science, and society. Am. Nat. 158, 1–46 (2001).

    Article  Google Scholar 

  9. Ben-Shahar, Y., Robichon, A., Sokolowski, M. B. & Robinson, G. E. Influence of gene action across different time scales on behavior. Science 296, 741–744 (2002).

    Article  CAS  Google Scholar 

  10. Baldwin, I. T. An ecologically motivated analysis of plant–herbivore interactions in native tobacco. Plant Physiol. 127, 1449–1458 (2001).

    Article  CAS  Google Scholar 

  11. Weinig, C. et al. Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162, 1875–1884 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Pigliucci, M., Pollard, H. & Cruzan, M. Comparative studies of evolutionary responses to light environments in Arabidopsis. Am. Nat. 161, 68–82 (2003).

    Article  Google Scholar 

  13. Tian, D. C., Traw, M. B., Chen, J. Q., Kreitman, M. & Bergelson, J. Pleiotropic cost of R-gene mediated resistance in Arabidopsis thaliana. Nature 423, 74–77 (2003).

    Article  CAS  Google Scholar 

  14. Cavalieri, D., Townsend, J. P. & Hartl, D. L. Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis. Proc. Natl Acad. Sci. USA 97, 12369–12374 (2000).

    Article  CAS  Google Scholar 

  15. Feder, M. E. Engineering candidate genes in studies of adaptation: the heat-shock protein Hsp70 in Drosophila melanogaster. Am. Nat. 154, 55–66 (1999).

    Google Scholar 

  16. de Bono, M. & Bargmann, C. I. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94, 679–89 (1998).

    Article  CAS  Google Scholar 

  17. Parichy, D. M. & Johnson, S. L. Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev. Genes Evol. 211, 319–328 (2001).

    Article  CAS  Google Scholar 

  18. Kopp, A., Duncan, I. & Carroll, S. B. Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408, 553–559 (2000).

    Article  CAS  Google Scholar 

  19. Gibson, G. Microarrays in ecology and evolution: a preview. Mol. Ecol. 11, 17–24 (2002).

    Article  CAS  Google Scholar 

  20. Daborn, P. J. et al. A single P450 allele associated with insecticide resistance in Drosophila. Science 297, 2253–2256 (2002).

    Article  CAS  Google Scholar 

  21. Fowler, S. & Thomashow, M. F. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14, 1675–1690 (2002).

    Article  CAS  Google Scholar 

  22. Churchill, G. A. Fundamentals of experimental design for cDNA microarrays. Nature Genet. 32, 490–495 (2002).

    Article  CAS  Google Scholar 

  23. Slonim, D. K. From patterns to pathways: gene expression data analysis comes of age. Nature Genet. 32, 502–508 (2002).

    Article  CAS  Google Scholar 

  24. Chuaqui, R. F. et al. Post-analysis follow-up and validation of microarray experiments. Nature Genet. 32, 509–514 (2002).

    Article  CAS  Google Scholar 

  25. Toma, D. P., White, K. P., Hirsch, J. & Greenspan, R. J. Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nature Genet. 31, 349–353 (2002).

    Article  CAS  Google Scholar 

  26. Beja, O. et al. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415, 630–633 (2002).

    Article  CAS  Google Scholar 

  27. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002).

    Article  CAS  Google Scholar 

  28. Jackson, R. B. et al. Linking molecular insight and ecological research. Trends Ecol. Evol. 17, 409–414 (2002).

    Article  Google Scholar 

  29. Jackson, R. B., Moore, L. A., Hoffmann, W. A., Pockman, W. T. & Linder, C. R. Ecosystem rooting depth determined with caves and DNA. Proc. Natl Acad. Sci. USA 96, 11387–11392 (1999).

    Article  CAS  Google Scholar 

  30. Roberts, S. P. & Feder, M. E. Changing fitness consequences of hsp70 copy number in transgenic Drosophila larvae undergoing natural thermal stress. Funct. Ecol. 353–357 (2000).

  31. Maloof, J. N. et al. Natural variation in light sensitivity of Arabidopsis. Nature Genet. 29, 441–446 (2001).

    Article  CAS  Google Scholar 

  32. Nachman, M. W., Hoekstra, H. E. & D'Agostino, S. L. The genetic basis of adaptive melanism in pocket mice. Proc. Natl Acad. Sci. USA 100, 5268–5273 (2003).

    Article  CAS  Google Scholar 

  33. Meagher, S., Penn, D. J. & Potts, W. K. Male–male competition magnifies inbreeding depression in wild house mice. Proc. Natl Acad. Sci. USA 97, 3324–3329 (2000).

    Article  CAS  Google Scholar 

  34. Lexer, C., Welch, M. E., Durphy, J. L. & Rieseberg, L. H. Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Mol. Ecol. 12, 1225–1235 (2003).

    Article  CAS  Google Scholar 

  35. Peichel, C. et al. The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905 (2001).

    Article  CAS  Google Scholar 

  36. Aparicio, S. et al. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297, 1301–1310 (2002).

    Article  CAS  Google Scholar 

  37. Beldade, P., Brakefield, P. M. & Long, A. D. Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415, 315–318 (2002).

    Article  CAS  Google Scholar 

  38. Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).

    Article  CAS  Google Scholar 

  39. El-Assal, S. E. -D., Alonso-Blanco, C., Peeters, A. J. M., Raz, V. & Koornneef, M. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nature Genet. 29, 435–440 (2001).

    Article  CAS  Google Scholar 

  40. Dilda, C. L. & Mackay, T. F. C. The genetic architecture of Drosophila sensory bristle number. Genetics 162, 1655–1674 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Robin, C., Lyman, R. F., Long, A. D., Langley, C. H. & Mackay, T. F. C. hairy: a quantitative trait locus for Drosophila sensory bristle number. Genetics 162, 155–164 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang, X. S. & Hill, W. G. Joint effects of pleiotropic selection and stabilizing selection on the maintenance of quantitative genetic variation at mutation-selection balance. Genetics 162, 459–471 (2002).

    PubMed  PubMed Central  Google Scholar 

  43. Holub, E. B. The arms race is ancient history in Arabidopsis, the wildflower. Nature Rev. Genet. 2, 516–527 (2001).

    Article  CAS  Google Scholar 

  44. Jakob, K. et al. Pseudomonas viridiflava and P. syringae — natural pathogens of Arabidopsis thaliana. Mol. Plant Microbe Interact. 15, 1195–1203 (2002).

    Article  CAS  Google Scholar 

  45. Grant, M. R. et al. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc. Natl Acad. Sci. USA 95, 15843–15848 (1998).

    Article  CAS  Google Scholar 

  46. Brakefield, P. M. & Liebert, T. G. Evolutionary dynamics of declining melanism in the peppered moth in the Netherlands. Proc. Royal Soc. Lond. B 267, 1953–1957 (2000).

    Article  CAS  Google Scholar 

  47. Clegg, M. T. & Durbin, M. L. Tracing floral adaptations from ecology to molecules. Nature Rev. Genet. 4, 206–215 (2003).

    Article  CAS  Google Scholar 

  48. Watt, W. B. Avoiding paradigm-based limits to knowledge of evolution. Evol. Biol. 32, 73–96 (2000).

    Article  Google Scholar 

  49. Feder, M. E. & Watt, W. B. in Genes in Ecology (eds. Berry, R. J., Crawford, T. J. & Hewitt, G. M.) 365–391 (Blackwell Scientific, Oxford, 1993).

    Google Scholar 

  50. Fay, J. C., Wyckoff, G. J. & Wu, C. I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415, 1024–1026 (2002).

    Article  CAS  Google Scholar 

  51. Swanson, W. J., Zhang, Z. H., Wolfner, M. F. & Aquadro, C. F. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98, 2509–2514 (2001).

    Article  CAS  Google Scholar 

  52. Riley, R., Jin, W. & Gibson, G. Contrasting selection pressures on components of Ras-mediated signal transduction in Drosophila. Mol. Ecol. 12, 1315–1323 (2003).

    Article  CAS  Google Scholar 

  53. Schulte, P. M. Environmental adaptations as windows on molecular evolution. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 128, 597–611 (2001).

    Article  CAS  Google Scholar 

  54. Watt, W. B. & Dean, A. M. Molecular-functional studies of adaptive genetic variation in prokaryotes and eukaryotes. Ann. Rev. Genet. 34, 593–622 (2000).

    Article  CAS  Google Scholar 

  55. Fields, P. A., Kim, Y. S., Carpenter, J. F. & Somero, G. N. Temperature adaptation in Gillichthys (Teleost: Gobiidae) A(4)-lactate dehydrogenases: identical primary structures produce subtly different conformations. J. Exp. Biol. 205, 1293–1303 (2002).

    CAS  PubMed  Google Scholar 

  56. Farrell, B. D. et al. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55, 2011–2027 (2001).

    Article  CAS  Google Scholar 

  57. Oleksiak, M. F., Kolell, K. J. & Crawford, D. L. Utility of natural populations for microarray analyses: isolation of genes necessary for functional genomic studies. Marine Biotechnol. 3, 203–211 (2001).

    Article  Google Scholar 

  58. Boffelli, D. et al. Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299, 1391–1394 (2003).

    Article  CAS  Google Scholar 

  59. Zdobnov, E. et al. Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298, 149–159 (2002).

    Article  CAS  Google Scholar 

  60. Charlesworth, D., Charlesworth, B. & McVean, G. A. T. Genome sequences and evolutionary biology, a two-way interaction. Trends Ecol. Evol. 16, 235–242 (2001).

    Article  CAS  Google Scholar 

  61. Ureta-Vidal, A., Ettwiller, L. & Birney, E. Comparative genomics: genome-wide analysis in metazoan eukaryotes. Nature Rev. Genet. 4, 251–262 (2003).

    Article  CAS  Google Scholar 

  62. Cooper, T. F., Rozen, D. E. & Lenski, R. E. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl Acad. Sci. USA 100, 1072–1077 (2003).

    Article  CAS  Google Scholar 

  63. Elena, S. F. & Lenski, R. E. Microbial genetics: evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Rev. Genet. 4, 457–469 (2003).

    Article  CAS  Google Scholar 

  64. Ideker, T., Galitski, T. & Hood, L. A new approach to decoding life. Annu. Rev. Genom. Human. Genet. 2, 343–372 (2001).

    Article  CAS  Google Scholar 

  65. Wittbrodt, J., Shima, A. & Schartl, M. Medaka — a model organism from the far East. Nature Rev. Genet. 3, 353–364 (2002).

    Article  Google Scholar 

  66. Kocher, T. D., Lee, W. -J., Sobolewska, H., Penman, D. & McAndrew, B. A Genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148, 1225–1232 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Pennisi, E. Recharged field's rallying cry: gene chips for all organisms. Science 297, 1985–1987 (2002).

    Article  CAS  Google Scholar 

  68. Whitfield, C. W. et al. Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res. 12, 555–566 (2002).

    Article  Google Scholar 

  69. Davidson, E. H., McClay, D. R. & Hood, L. Regulatory gene networks and the properties of the developmental process. Proc. Natl Acad. Sci. 100, 1475–1480 (2003).

    Article  CAS  Google Scholar 

  70. Bradshaw, H. D., Ceulemans, R., Davis, J. & Stettler, R. F. Emerging model systems: poplar (Populus) as a model forest tree. J. Plant Growth Reg. 19, 306–313 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank G. Bartholomew, J. Bergelson, B. Hill, C. Langley, M. Lynch, T. MacKay, M. Nachman, M. Turelli, W. Watt and three anonymous referees for helpful discussion and comments. We are grateful to J. Bergelson, J. Colbourne, M. Lynch, M. Nachman and C. Weinig for access to unpublished manuscripts and proposals. T.M.-O was supported by the European Union (contract number QLRT-2000-01097), the Bundesminesterium für Bildung und Forschung, the United States National Science Foundation and the Max-Planck Gesellschaft. M.E.F. was supported by National Science Foundation grants, which also supported the establishment of the evolutionary and ecological functional genomics (EEFG) community. In lieu of a trans-Atlantic coin flip, the order of authorship was determined by random fluctuation in the Euro/Dollar exchange rate.

Author information

Author notes

  1. Martin E. Feder and Thomas Mitchell-Olds: Both authors contributed equally to this article.

Authors and Affiliations

  1. the Committee on Evolutionary Biology, Committee on Genetics,

    Martin E. Feder

  2. Department of Organismal Biology and Anatomy, University of Chicago, 1027 East 57th Street, Chicago, 60637, Illinois, USA

    Martin E. Feder

  3. Department of Genetics and Evolution, Max-Planck Institute of Chemical Ecology, Jena, 07745, Germany

    Thomas Mitchell-Olds

Authors
  1. Martin E. Feder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Mitchell-Olds
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Mitchell-Olds.

Related links

Related links

DATABASES

TAIR

RPM1

Further Information

Daphnia Genomics Consortium

EEFG

EEFG Conference

Genome News Network

Genomes Online Database

Martin E. Feder's web site

Max Planck Institute of Chemical Ecology Department of Genetics and Evolution

NemATOL

Organism-Specific Genome Databases

TIGR Gene Indices

Wild Relatives of Arabidopsis

Glossary

BALANCING SELECTION

Natural selection that maintains higher levels of genetic variation than are expected under neutrality.

BIOPROSPECTING

The sampling of diverse organisms for genes, gene products and other compounds that are of value to humans.

DARWINIAN FITNESS

The expected reproductive contribution to future generations.

EPISTASIS

The influence of the interaction of multiple loci on variation in a single trait.

GEOTAXIS

Movement up or down, which requires the perception of and response to gravity.

GUILDS

Groups of species that use a common resource in similar ways.

LINKAGE DISEQUILIBRIUM

When genotype frequencies at several loci are correlated or non-independent.

MUTATION–SELECTION BALANCE MODEL

A population genetics model that assumes that a combination of mutation and balancing selection can explain present levels of genetic variation.

NATURAL EXPERIMENTS

The comparison of naturally arising variants of individual organisms, populations, species or higher taxa, which is similar to the way in which control and manipulated subjects are compared in anthropogenic experimentation.

PHYLOGENETIC FOOTPRINTING AND SHADOWING

Both approaches seek to identify conserved regulatory elements by comparing genomic sequences between related species. Phylogenetic footprinting uses one or a few relatively distant evolutionary comparisons, whereas phylogenetic shadowing examines a set of closely related species.

PLEIOTROPY

When a single gene or polymorphism influences two or more separate traits.

POST-GENOMIC

The era following the availability of complete genome sequences.

STABILIZING SELECTION

Natural selection that favours intermediate values of a quantitative trait.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Feder, M., Mitchell-Olds, T. Evolutionary and ecological functional genomics. Nat Rev Genet 4, 649–655 (2003). https://doi.org/10.1038/nrg1128

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg1128

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing