Cophylogeny and convergence shape holobiont evolution in sponge-microbe symbioses

Area of Science:

• Marine Biology
• Ecology
• Evolutionary Biology

Background:

• Sponges host diverse microbial communities crucial for reef ecosystems.
• Sponges are categorized by symbiont abundance: low microbial abundance (LMA) and high microbial abundance (HMA).
• The evolutionary history of these symbiotic states is not well understood.

Purpose of the Study:

• To investigate the evolutionary dynamics of LMA and HMA symbiotic states in sponges.
• To determine the ancestral symbiotic state in sponges.
• To understand the factors driving the evolution of HMA symbioses.

Main Methods:

• Exhaustive sampling of Caribbean sponge biodiversity.
• Phylogenetic analysis to infer evolutionary relationships.
• Comparative analysis of microbial communities in LMA and HMA sponges.

Main Results:

• The low microbial abundance (LMA) state is predicted to be the ancestral condition for sponges.
• High microbial abundance (HMA) symbioses have evolved independently multiple times, often recruiting similar microbial assemblages.
• HMA symbioses exhibit stronger signals of phylosymbiosis and cophylogeny, indicating more intense co-evolutionary interactions.
• HMA holobionts are associated with increased endemism, metabolic dependence, and chemical defenses.

Conclusions:

• Sponges likely originated with LMA symbioses, with HMA states evolving later.
• The evolution of HMA symbioses may be linked to increased dissolved organic matter or predator diversification.
• HMA symbioses represent a significant evolutionary innovation in sponge holobionts, enhancing their ecological roles and defenses.