Photosymbiosis Shaped Animal Genome Architecture and Gene Evolution as Revealed in Giant Clams

Abstract

Symbioses are major drivers of organismal diversification and phenotypic innovation. However, how long-term symbioses shape whole genome evolution in metazoans is still underexplored. Here, we used a giant clam (Tridacna maxima) genome to demonstrate how symbiosis has left complex signatures in a genome of an animal. Giant clams thrive in oligotrophic waters by forming a remarkable association with photosymbiotic dinoflagellate algae. Genome-based demographic inferences uncovered a tight correlation between T. maxima global population change and major paleoclimate and habitat shifts, highlighting how abiotic and biotic factors dictate T. maxima microevolution. Comparative analyses revealed unique symbiosis-driven genomic features, including expansion and contraction of immunity-related gene families and a large proportion of lineage-specific genes. Strikingly, about 70% of the genome is composed of repetitive elements, especially transposable elements, most likely resulting from a symbiosis-adapted immune system. This work greatly enhances our understanding of genomic drivers of symbiosis that underlie metazoan evolution and diversification.