Evolutionary gain of red blood cells in a commensal bivalve (Galeommatoidea) as an adaptation to a hypoxic shrimp burrow

Abstract

Evolutionary transitions from free-living to symbiotic lifestyles often lead to dramatic changes in morphological, ecological and physiological characteristics. Galeommatoidea represents a highly diverse superfamily of Bivalvia, with > 620 described species in multiple free-living and symbiotic clades and, thereby, provides a unique opportunity to investigate the character evolution associated with lifestyle transitions. Barrimysia cumingii is a commensal galeommatoidean that lives in the deep burrow of the strahlaxiid shrimp Neaxius acanthus. The burrow is a sulphiderich reducing environment owing to poor water circulation and decay of seagrass leaves accumulated by the shrimp. In this study, we found that abundant spherical red blood cells (RBCs; ~10 μm in diameter) with one prominent nucleus occur in the haemocoel of B. cumingii. This is the first report of RBCs for the superfamily. Our phylogenetic reconstruction based on four-gene DNA sequences indicates a relatively recent divergence of B. cumingii from free-living ancestors without RBCs and the origin of RBCs in association with the colonization of the shrimp burrow. Other bivalve lineages with RBCs tend to occur in hypoxic habitats, including mangrove swamps and deep-sea hydrothermal vents and cold seeps, suggesting that B. cumingii has also obtained RBCs as a physiological adaptation to within-host-burrow hypoxia.