Abstract
All organisms depend on symbiotic associations with bacteria for their success, yet how these interspecific interactions influence the population structure, ecology, and evolution of microbial symbionts is not well understood. Additionally, patterns of genetic variation in interacting species can reveal ecological traits that are important to gene flow and co-evolution. In this study, we define patterns of spatial and temporal genetic variation of a coral reef fish, Siphamia tubifer, and its luminous bacterial symbiont, Photobacterium mandapamensis in the Okinawa Islands, Japan. Using restriction site-associated sequencing (RAD-Seq) methods, we show that populations of the facultative light organ symbiont of S. tubifer exhibit genetic structure at fine spatial scales of tens of kilometers despite the absence of physical barriers to dispersal and in contrast to populations of the host fish. These results suggest that the host’s behavioral ecology and environmental interactions between host and symbiont help to structure symbiont populations in the region, consequently fostering the specificity of the association between host generations. Our approach also revealed several symbiont genes that were divergent between host populations, including hfq and a homolog of varS, both of which play a role in host association in Vibrio cholerae. Overall, this study highlights the important role that a host animal can play in structuring the distribution of its bacterial symbiont, particularly in highly connected marine environments, thereby promoting specificity of the symbiosis between host generations.
Highlights
In open marine environments, where there are few physical barriers to dispersal, microbes are expected to exist as well-mixed populations, supporting the classic panmictic view in microbial biogeography that “everything is everywhere, but the environment selects” (Baas-Becking, 1934)
We carried out an analysis of the restriction siteassociated sequencing (RAD-Seq) data for a total of 8,637 loci in 282 S. tubifer specimens sampled from eleven locations that were separated by two to tens of kilometers around Okinawa Island and up to 140 km between Okinawa Island and Kume Island
We obtained data for discrete, live populations of bacterial symbionts by extracting and sequencing genomic DNA directly from whole light organs of S. tubifer, a symbiotically luminous fish commonly found on coral reefs in the Okinawa Islands
Summary
In open marine environments, where there are few physical barriers to dispersal, microbes are expected to exist as well-mixed populations, supporting the classic panmictic view in microbial biogeography that “everything is everywhere, but the environment selects” (Baas-Becking, 1934). This view has been challenged in recent years, providing evidence of geographic structure in certain marine microbes (Martiny et al, 2006; Ivars-Martínez et al, 2008), often over broad geographic scales and with coarse taxonomic resolution (Pommier et al, 2005, 2007; Brown et al, 2012; Sul et al, 2013). Many such associations are highly specific (Cavanaugh, 1994; Nyholm and McFall-Ngai, 2004), indicating that mechanisms such as environmental filtering and the ecology or physiology of the host ensure that a certain symbiont is acquired from the environment by each new host generation
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