Larger bacterial populations evolve heavier fitness trade-offs and undergo greater ecological specialization

Abstract

Evolutionary studies over the last several decades have invoked fitness trade-offs to explain why species prefer some environments to others. However, the effects of population size on trade-offs and ecological specialization remain largely unknown. To complicate matters, trade-offs themselves have been visualized in multiple ways in the literature. Thus, it is not clear how population size can affect the various aspects of trade-offs. To address these issues, we conducted experimental evolution with Escherichia coli populations of two different sizes in two nutritionally limited environments, and studied fitness trade-offs from three different perspectives. We found that larger populations evolved greater fitness trade-offs, regardless of how trade-offs are conceptualized. Moreover, although larger populations adapted more to their selection conditions, they also became more maladapted to other environments, ultimately paying heavier costs of adaptation. To enhance the generalizability of our results, we further investigated the evolution of ecological specialization across six different environmental pairs, and found that larger populations specialized more frequently and evolved consistently steeper reaction norms of fitness. This is the first study to demonstrate a relationship between population size and fitness trade-offs, and the results are important in understanding the population genetics of ecological specialization and vulnerability to environmental changes.

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Fig. 1: Schematic representation of ecological specialization across two environments.
Fig. 2: Correlation between relative fitness values in galactose and thymidine minimal media after evolution in these environments at two different population sizes.
Fig. 3: Loss of fitness below the ancestral levels in the away environments.
Fig. 4: Reaction norms of fitness across the six home-away environmental pairs used in our study.
Fig. 5: Slopes of reaction norms of the fitness of our experimental populations across six environmental pairs.

Data availability

All the data relevant to this study can be found at https://doi.org/10.5061/dryad.bnzs7h46z.

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Acknowledgements

We thank Milind Watve and MS Madhusudhan for their valuable inputs. YC was supported by a Senior Research Fellowship initially sponsored by IISER Pune and then by Council for Scientific and Industrial Research (CSIR), Govt. of India. SM was supported by an INSPIRE undergraduate fellowship, sponsored by the Department of Science and Technology (DST), Govt. of India. This project was supported by an external grant (BT/PR22328/BRB/10/1569/2016) from the Department of Biotechnology, Govt. of India, and internal funding from IISER Pune.

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YC and SD designed the study. YC and SM conducted the experiments. YC analyzed the data. YC and SD wrote the paper with inputs from SM.

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Correspondence to Sutirth Dey.

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Chavhan, Y., Malusare, S. & Dey, S. Larger bacterial populations evolve heavier fitness trade-offs and undergo greater ecological specialization. Heredity 124, 726–736 (2020). https://doi.org/10.1038/s41437-020-0308-x

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