Higher rates of sex evolve in spatially heterogeneous environments

Journal name:
Nature
Volume:
468,
Pages:
89–92
Date published:
DOI:
doi:10.1038/nature09449
Received
Accepted
Published online

The evolution and maintenance of sexual reproduction has puzzled biologists for decades1, 2. Although this field is rich in hypotheses3, 4, 5, experimental evidence is scarce. Some important experiments have demonstrated differences in evolutionary rates between sexual and asexual populations6, 7, 8; other experiments have documented evolutionary changes in phenomena related to genetic mixing, such as recombination9, 10 and selfing11. However, direct experiments of the evolution of sex within populations are extremely rare (but see ref. 12). Here we use the rotifer, Brachionus calyciflorus, which is capable of both sexual and asexual reproduction, to test recent theory13, 14, 15 predicting that there is more opportunity for sex to evolve in spatially heterogeneous environments. Replicated experimental populations of rotifers were maintained in homogeneous environments, composed of either high- or low-quality food habitats, or in heterogeneous environments that consisted of a mix of the two habitats. For populations maintained in either type of homogeneous environment, the rate of sex evolves rapidly towards zero. In contrast, higher rates of sex evolve in populations experiencing spatially heterogeneous environments. The data indicate that the higher level of sex observed under heterogeneity is not due to sex being less costly or selection against sex being less efficient; rather sex is sufficiently advantageous in heterogeneous environments to overwhelm its inherent costs2. Counter to some alternative theories16, 17 for the evolution of sex, there is no evidence that genetic drift plays any part in the evolution of sex in these populations.

At a glance

Figures

  1. Fitness in alternative environments.
    Figure 1: Fitness in alternative environments.

    Lifetime reproduction (fitness) of amictic (asexual) Brachionus calyciflorus females was measured on individuals from populations that had evolved for 15 weeks under conditions of either high or low food quality (see text and Methods). The fitness of the same genotype of ten individual clones (third generation after isolation) was measured under high-quality food conditions (left) and low-food-quality conditions (right); n = 18 populations; eight populations with a migration rate of m10% and ten populations with m1% per generation. The graph shows the means ± one standard error; GLMM ***P<0.001 for the high-quality food environment; the difference is not significant in the low-quality food environment. See Methods for fitness assay description.

  2. Evolution of the propensity for sex in Brachionus calyciflorus populations from spatially heterogeneous and spatially homogeneous environments measured in a common environment.
    Figure 2: Evolution of the propensity for sex in Brachionus calyciflorus populations from spatially heterogeneous and spatially homogeneous environments measured in a common environment.

    The propensity for sex was measured as the percentage of females induced into mixis (sexual reproduction) when exposed to a standardized stimulus. Vertical lines at week 14 mark the start of the second part of the experiment, when all populations were mixed and reassigned to treatments. Each data point represents the mean of 7–10 populations per treatment ± one standard error. Migration rates are shown of m10% per generation (a) and m1% per generation (b). For both migration rates, the rate of sex is significantly greater in the heterogeneous treatment than in either homogeneous treatment in comparisons at weeks 6, 12 and 20 (***P<0.001 for all comparisons). Between week 14 and 20, the rate of sex significantly increases in the heterogeneous treatment (***P<0.001 for m10%; **P = 0.01 for m1%). In contrast, sex declines in the homogeneous treatments (***P<0.001). Open triangles (only for m1% in b) represent heterogeneous populations evolving at ten times the standard size of N10,000.

  3. In situ measure of the rate of sex in Brachionus calyciflorus populations from spatially heterogeneous and spatially homogeneous environments measured as the fraction of sexually derived offspring (resting eggs) of total offspring.
    Figure 3: In situ measure of the rate of sex in Brachionus calyciflorus populations from spatially heterogeneous and spatially homogeneous environments measured as the fraction of sexually derived offspring (resting eggs) of total offspring.

    Mean percentages of resting eggs out of all eggs in Brachionus calyciflorus populations (a) and mean female densities (b) are plotted over time. Error bars represent ± one standard error. The populations appear to reach demographic equilibrium after about 75days. After this point (days 75–109), female densities are very similar across treatments, thereby permitting a reasonable comparison for rates of sex. During this period, the percentage of sexually produced offspring was significantly higher in the heterogeneous treatment than in the homogeneous treatments (GLMM: for the heterogeneous versus homogeneous high-quality food condition, χ2 = 31.458, d.f. = 1, P<0.001; for the heterogeneous versus homogeneous low-quality food condition, χ2 = 24.947, d.f. = 1, P<0.001). Vertical lines mark the time points at which the propensity for sex was measured in a common environment (Fig. 2) and horizontal lines mark the data used for the comparison of resting egg fraction between treatments.

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Author information

Affiliations

  1. Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, Ontario M5S 3B2, Canada

    • Lutz Becks &
    • Aneil F. Agrawal
  2. Department of General Ecology, Zoological Institute, Center for Biological Sciences, University of Cologne, D-50931 Köln, Germany

    • Lutz Becks

Contributions

L.B. and A.F.A. conceived and designed the study, L.B. performed experiments, L.B. and A.F.A. discussed and analysed the results, and shared the writing of the paper.

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The authors declare no competing financial interests.

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Comments

  1. Report this comment #15494

    Paul Adams said:

    The evolution sex scandal – the failure to reach a convincing scientific consensus about the single most prominent evolutionary innovation since the advent of DNA/protein-based life – has thankfully not yet reached the notice of creationists. This important, clear and cautious paper gives reason to hope that the scandal might soon be eliminated – just in the nick of time. A resolution of this issue might also help clear logjams in other fields.

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