The Evolutionary Ecology of a Bioluminescent Vertebrate-Microbe Symbiosis.

Abstract

The evolution of a symbiosis requires the maintenance of an intimate host-symbiont association over ecological time. My dissertation research investigates the ecological mechanisms that facilitate the maintenance of specificity of a vertebrate-microbe symbiosis involving the coral reef cardinalfish, Siphamia tubifer, and the luminous bacterium, Photobacterium mandapamensis, over host generations. Integrating field studies to define aspects of the life history and behavioral ecology of the host fish in Okinawa, Japan, with newly developed genomic methods, I tested the hypothesis that the host’s behavioral ecology genetically structures natural populations of the symbiont, consequently promoting specificity of the symbiosis. I first described the life history of S. tubifer and determine that the host’s pelagic larval duration is approximately one month, during which symbiont acquisition occurs, and once settled, the fish grows quickly, reproduces early, and survives much less than a year. I then applied mark-recapture methods to define the fish’s site fidelity and homing ability and its preference for relevant olfactory cues. Results revealed that S. tubifer exhibits daily fidelity to a reef site and significant homing abilities from up to two kilometers, which results in the local enrichment of a home reef with luminous symbionts released daily by the resident S. tubifer population. Additionally, S. tubifer preferred the chemical cues of its home site water and luminous bacterial symbiont, and juvenile fish also preferred the olfactory cues of conspecifics to unconditioned seawater. Lastly, I applied double-digest, restriction site associated sequencing (ddRAD-Seq) to define the fine-scale population genomic structure of S. tubifer and P. mandapamensis in the Okinawa Islands, Japan. Analysis of nearly 300 individuals from 11 locations and over three years revealed no evidence of genetic structure of the host fish at spatial scales ranging from a few to over 100 kilometers. However, light organ symbiont populations were genetically differentiated between the same reefs approximately 100 kilometers apart, indicating that symbiont acquisition by larval fish occurs near the locally enriched symbiont pool at a settlement site. Therefore, the behavioral ecology of S. tubifer promotes the specificity of the symbiosis between host generations, providing evidence of host-mediated diversification of a marine bacterium.