Turning ecology and evolution against cancer

Journal name:
Nature Reviews Cancer
Volume:
14,
Pages:
371–380
Year published:
DOI:
doi:10.1038/nrc3712
Published online

Abstract

The fight against cancer has drawn researchers from a wide variety of disciplines, ranging from molecular biology to physics, but the perspective of an ecological theorist has been mostly overlooked. By thinking about the cells that make up a tumour as an endangered species, cancer vulnerabilities become more apparent. Studies in conservation biology and microbial experiments indicate that extinction is a complex phenomenon, which is often driven by the interaction of ecological and evolutionary processes. Recent advances in cancer research have shown that tumours, like species striving for survival, harbour intricate population dynamics, which suggests the possibility to exploit the ecology of tumours for treatment.

At a glance

Figures

  1. Competition and cooperation in cancer progression.
    Figure 1: Competition and cooperation in cancer progression.

    a | In the model of cancer as a disease of clonal evolution proposed by Nowell6, an initially benign neoplasm (N) accumulates mutations that confer cancer phenotypes with increasing aggressiveness. Less fit lineages temporarily segregate but are typically lost through competition. b | Clonal lineages with similar fitness may coexist and compete within a tumour — a phenomenon known as clonal interference62, 63. c | Two clones evolve complementary traits. Even though each clone is not self-sufficient, their cooperation results in malignancy37.

  2. Spatial organization in populations.
    Figure 2: Spatial organization in populations.

    a | In colonies of swarming bacteria, 'hyperswarmer' mutants with several flagella have a fitness advantage by being able to travel faster to the edge of the colony, where nutrient concentrations are higher. b | Genetic demixing in a colony of bacteria. A strain of Pseudomonas aeruginosa was labelled using four neutral fluorescent markers (green fluorescent protein (GFP), cyan fluorescent protein (CFP), yellow fluorescent protein (YFP) and DsRed-Express (DSRed-Exp.)), and the four labelled strains were mixed at equal proportions in the founding populations. Genetic demixing occurred as the population expanded over the agar surface on a Petri dish. The figure shows a previously unpublished experiment carried out following the protocol in Ref 116. c | Cane toads are an invasive species in Australia, where they were introduced on the south-east coast in the 1930s. Since then, they have spread through a large part of the northern coast of Australia, and their invasion speed has markedly increased. This increase is attributed to adaptations (such as longer legs) at the leading edge. Image courtesy of B. Phillips, Department of Zoology, University of Melbourne, Australia. Figure part a is reprinted from Cell Reports, 4, Van Ditmarsch, D. et al., Convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria, 697–708 © (2003), with permission from Elsevier111.

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Affiliations

  1. Bioinformatics Program, Boston University, 44 Cummington Mall, Boston, Massachusetts 02215, USA.

    • Kirill S. Korolev
  2. Memorial Sloan-Kettering Cancer Center, Computational Biology Program, New York, New York, USA.

    • Joao B. Xavier
  3. Massachusetts Institute of Technology, 400 Technology Square, NE46-609 Cambridge, Massachusetts, USA.

    • Jeff Gore

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The authors declare no competing interests.

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Author details

  • Kirill S. Korolev

    Kirill S. Korolev is an Assistant Professor of Physics and Bioinformatics at Boston University, Boston, Massachusetts, USA. Trained as a physicist at Harvard University, Cambridge, Massachusetts, USA, and Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA, he looks at evolution through the lens of simple mathematical models that capture only the most essential aspects of the problem. A major theme in his research is the interconnection of ecological and evolutionary processes. For example, he found that population expansions can both inhibit interspecific mutualism and promote intraspecific cooperation. Most recently, he became interested in population genetics models of cancer and the effects of deleterious passenger mutations on cancer progression. Kirill S. Korolev's homepage.

  • Joao B. Xavier

    Joao B. Xavier is an assistant faculty member at the Sloan Kettering Institute in New York, USA, where he leads a multidisciplinary group working on biofilms and cancer. He obtained his Ph.D. in biomathematics at the New University of Lisbon, Portugal, where he studied biocomplexity. During his postdoctoral training at the Delft University of Technology, the Netherlands, and Harvard, Cambridge, Massachusetts, USA, he investigated how microbial biofilms, which are communities of bacteria, develop. While investigating bacterial biofilms, it struck him how many biological problems derive from how cells interact with each other and how they react to environmental changes as a population, as well as how cancer has many parallels to biofilms. Joao B. Xavier's homepage.

  • Jeff Gore

    Jeff Gore is an Assistant Professor of Physics at the Massachusetts Institute of Technology (MIT) in Cambridge, Massachusetts, USA. His laboratory uses experimental microbial populations to explore fundamental ideas in theoretical ecology and evolutionary dynamics. A particular area of focus is to try and understand the consequences of cooperative interactions within a population. Such cooperatively growing populations can suddenly collapse if the population falls below a critical size, and recovery can be very difficult. Moreover, cooperative populations are often susceptible to the emergence and spread of 'cheaters', which are individuals that do not contribute to the public good. Jeff Gore's homepage.

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