A latent capacity for evolutionary innovation through exaptation in metabolic systems

Journal name:
Nature
Volume:
500,
Pages:
203–206
Date published:
DOI:
doi:10.1038/nature12301
Received
Accepted
Published online

Some evolutionary innovations may originate non-adaptively as exaptations, or pre-adaptations, which are by-products of other adaptive traits1, 2, 3, 4, 5. Examples include feathers, which originated before they were used in flight2, and lens crystallins, which are light-refracting proteins that originated as enzymes6. The question of how often adaptive traits have non-adaptive origins has profound implications for evolutionary biology, but is difficult to address systematically. Here we consider this issue in metabolism, one of the most ancient biological systems that is central to all life. We analyse a metabolic trait of great adaptive importance: the ability of a metabolic reaction network to synthesize all biomass from a single source of carbon and energy. We use novel computational methods to sample randomly many metabolic networks that can sustain life on any given carbon source but contain an otherwise random set of known biochemical reactions. We show that when we require such networks to be viable on one particular carbon source, they are typically also viable on multiple other carbon sources that were not targets of selection. For example, viability on glucose may entail viability on up to 44 other sole carbon sources. Any one adaptation in these metabolic systems typically entails multiple potential exaptations. Metabolic systems thus contain a latent potential for evolutionary innovations with non-adaptive origins. Our observations suggest that many more metabolic traits may have non-adaptive origins than is appreciated at present. They also challenge our ability to distinguish adaptive from non-adaptive traits.

At a glance

Figures

  1. Viability on glucose entails viability on multiple other carbon sources.
    Figure 1: Viability on glucose entails viability on multiple other carbon sources.

    a, The binary innovation vector of a hypothetical metabolic network that is viable on glucose. The vector shows that the random network is viable (labelled by 1) on glucose, sorbitol and fructose, but not viable (labelled by 0) on pyruvate and acetate. The innovation index of this network (IGlucose = 2) is the number of additional carbon sources on which the network is viable. b, The distribution of innovation indices for 500 random networks viable on glucose. Only 4% of networks have IGlucose = 0, meaning that they are viable only on glucose.

  2. Innovation varies with respect to the carbon source, C, and the mean metabolic distance between C and Cnew.
    Figure 2: Innovation varies with respect to the carbon source, C, and the mean metabolic distance between C and Cnew.

    a, For each of 50 carbon sources (horizontal axis), the figure indicates the mean innovation index (bar) and its coefficient of variation (vertical line) for 500 random networks required to be viable on that carbon source. Note the broad distribution of the index. Some carbon sources, such as acetate, allow viability on more than nine additional carbon sources, on average, whereas others, such as deoxyadenosine, support viability on fewer than one additional carbon source. The innovation index of glucose (red) is typical compared with other carbon sources. b, A hypothetical carbon source, Cnew, which can be synthesized from another carbon source, C, in one reaction (arrow), and which leads, through multiple further reactions, to the synthesis of biomass. Some metabolic networks may have an alternative metabolic pathway that bypasses Cnew altogether (right-hand sequence of arrows). c, Like b, but with Cnew and C separated by multiple reactions. The fewer reactions separate C and Cnew, the more likely it is that Cnew is not bypassed by some alternative metabolic pathway, and that viability on C therefore implies viability on Cnew. d, Testing the hypothesis in c. The horizontal axis shows the mean number of reactions that separate C and Cnew in networks that are viable on both C and Cnew, binned into integer intervals according to the floor of this number (that is, the greatest smaller integer). The vertical axis shows the fraction of random metabolic networks required to be viable on carbon source C that are additionally viable on Cnew. We note that the potential for innovation decreases with increasing distance. Box edges, 25th and 75th percentiles; central horizontal line in each box, median; whiskers, ±2.7s.d.; open circles, outliers. Data are based on samples of 500 random viable networks for each of 50 carbon sources C (n = 25,000).

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Affiliations

  1. Institute of Evolutionary Biology and Environmental Sciences, Building Y27, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland

    • Aditya Barve &
    • Andreas Wagner
  2. The Swiss Institute of Bioinformatics, Bioinformatics, Quartier Sorge, Bâtiment Genopode, 1015 Lausanne, Switzerland

    • Aditya Barve &
    • Andreas Wagner
  3. The Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, New Mexico 87501, USA

    • Andreas Wagner

Contributions

A.B. and A.W. designed the research; A.B. performed the research; A.B. contributed new reagents and analytic tools; A.B. and A.W. analysed the data; and A.B. and A.W. wrote the paper.

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The authors declare no competing financial interests.

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