The role of multilevel selection in host microbiome evolution

Area of Science:

• Evolutionary biology
• Microbiome research
• Multilevel selection theory

Background:

• Host-associated microbiomes significantly influence animal reproductive success.
• The hologenome concept proposes hosts and microbiomes as integrated evolutionary units (holobionts).
• A quantitative framework is needed to assess holobiont-level selection, given ongoing debate.

Purpose of the Study:

• To develop a quantitative framework for understanding holobiont-level selection.
• To identify conditions under which selection can act on the integrated host-microbiome entity.
• To explore the coevolutionary dynamics between hosts and their microbiomes.

Main Methods:

• Application of multilevel selection theory.
• Mathematical modeling of host-microbiome interactions.
• Analysis of factors influencing microbiome heritability and host generation time.

Main Results:

• Holobiont-level selection can favor traits beneficial to the host, even if costly to microbes.
• Stringent conditions are required, including slow microbiome evolution and strong vertical transmission.
• Host generation time must be short relative to microbial evolutionary timescales.

Conclusions:

• Multilevel selection theory provides a quantitative basis for the hologenome concept.
• Holobiont-level selection is possible but constrained by transmission modes and generation times.
• The framework predicts specific host-microbiome systems where holobiont selection may operate.