The genetic architecture underlying prey-dependent performance in a microbial predator

Nature Communications, vol. 13, pp. 319

Abstract

Natural selection should favour generalist predators that outperform specialists across all prey types. Two genetic solutions could explain why intraspecific variation in predatory performance is, nonetheless, widespread: mutations beneficial on one prey type are costly on another (antagonistic pleiotropy), or mutational effects are prey-specific, which weakens selection, allowing variation to persist (relaxed selection). To understand the relative importance of these alternatives, we characterised natural variation in predatory performance in the microbial predator Dictyostelium discoideum. We found widespread nontransitive differences among strains in predatory success across different bacterial prey, which can facilitate stain coexistence in multi-prey environments. To understand the genetic basis, we developed methods for high throughput experimental evolution on different prey (REMI-seq). Most mutations (~77%) had prey-specific effects, with very few (~4%) showing antagonistic pleiotropy. This highlights the potential for prey-specific effects to dilute selection, which would inhibit the purging of variation and prevent the emergence of an optimal generalist predator.

Authors 8

1. Balint Stewart

   University College London

   Affiliation as printed

   Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK

2. Nicole Gruenheit

   University College London

   Affiliation as printed

   Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK

3. Amy J. Baldwin

   Cardiff University

   Affiliation as printed

   Cardiff School of Biosciences, Neuroscience and Mental Health Research Institute (NMHRI), Cardiff University, Hadyn Ellis Building, Maindy Road, Cardiff, CF24 4HQ, UK

4. Rex L. Chisholm

   Northwestern University

   Affiliation as printed

   Feinberg School of Medicine, Northwestern University, Chicago, IL, 60611, USA

5. Daniel E. Rozen Aachen Institute of Biology, Leiden University Sylvius Laboratory

   Leiden University

   Affiliation as printed

   Institute of Biology, Leiden University, Sylvius Laboratory, Sylviusweg 72, PO Box 9505, 2300 RA, Leiden, The Netherlands

   Institute of Biology, Leiden University, Sylvius Laboratory, Sylviusweg 72, PO Box 9505, 2300 RA, Leiden, The Netherlands

6. Adrian J. Harwood

   Cardiff University

   Affiliation as printed

   Cardiff School of Biosciences, Neuroscience and Mental Health Research Institute (NMHRI), Cardiff University, Hadyn Ellis Building, Maindy Road, Cardiff, CF24 4HQ, UK

7. Jason B. Wolf corresponding

   University of Bath

   Affiliation as printed

   Milner Centre for Evolution and Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath, BA2 7AY, UK. j.b.wolf@bath.ac.uk

   Milner Centre for Evolution and Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath, BA2 7AY, UK

8. Christopher R. L. Thompson corresponding

   University College London

   Affiliation as printed

   Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK. christopher.thompson@ucl.ac.uk

   Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK