Two-speed selection in a holobiont: Alternating host–microbiome evolution under thermal stress

Lipowska et al. (2024) showed host genetic selection can stabilize beneficial microbiomes, supporting hologenomic assumptions. Thermal evolution experiments reveal complex plasticity–adaptation interactions, such as warm-adapted male beetles performing best after cool developmental acclimation (Sales et al., 2024) and cold-selected Drosophila evolving canalized fecundity with reduced plasticity (Roy et al., 2025). This project proposes an experimental holobiont system (e.g., gnotobiotic Drosophila or Tribolium) where selection alternates between host performance (thermal fertility/fecundity) and microbiome function (in vitro community evolution under heat pulses). The method cycles gnotobiotic hosts through heatwaves; between host generations, the harvested microbiome is evolved in defined media under matched heatwave dynamics using evolve-and-resequence (E&R). The microbiome is then reconstituted into naive or selected hosts via cross-fostering. Factorial treatments manipulate host genetic background, microbiome evolutionary history, and acclimation regime to dissect contributions and interactions. This approach is novel because experimental evolution typically treats host or microbiome as static, whereas alternating selection tests whether adaptation flows to the partner best positioned to solve stress and whether this leads to canalized or plastic fitness responses. It builds on holobiont selection evidence and integrates thermal E&R desiderata, testing counterintuitive acclimation–adaptation interactions and canalization outcomes. The impact clarifies division of labor in holobiont adaptation under climate stress and informs microbiome-assisted breeding and conservation strategies targeting thermal resilience and reproductive robustness.

References:

1. Experimental Evolution of a Mammalian Holobiont? Genetic and Maternal Effects on the Cecal Microbiome in Bank Voles Selectively Bred for Herbivorous Capability.. Małgorzata M. Lipowska, Edyta T. Sadowska, Kevin D. Kohl, P. Koteja (2024). Ecological and evolutionary physiology.
2. Experimental evolution reveals that males evolving within warmer thermal regimes improve reproductive performance under heatwave conditions in a model insect.. K. Sales, M. J. Gage, R. Vasudeva (2024). Journal of Evolutionary Biology.
3. Reduction in thermal plasticity of life history traits in response to cold selection: an experimental evolution study using Drosophila melanogaster. Rishav Roy, Aradhya Chattopadhyay, Sreebes Deb Sharma, Aharna Mondal, Payel Biswas, Shampa M. Ghosh (2025). Frontiers in Ecology and Evolution.