Ecological factors rather than barriers to dispersal shape genetic structure of algal 1 symbionts in horizontally - transmitting corals 2 3

24 Many reef-building corals acquire their algal symbionts (Symbiodinium sp.) from the 25 local environment upon recruitment. This horizontal transmission strategy where hosts 26 pair with locally available symbionts could serve to increase coral fitness across diverse 27 environments, as long as the host maintains high promiscuity and symbionts adapt 28 locally. Here, we tested this hypothesis in two coral host species by comparing host and 29 symbiont genetic structures across different spatial scales in Micronesia. Each host 30 species associated with two genetically distinct Symbiodinium lineages, confirming high 31 promiscuity in broadly dispersing hosts. However, contrary to our initial expectation, 32 symbiont genetic structure was independent of physical barriers to dispersal between 33 islands, unlike genetic structure of their hosts that was nearly perfectly explained by 34 oceanic currents. Instead, Symbiodinium consistently demonstrated genetic divergence 35 among local reefs and between the two host species at each island, although not 36 necessarily between distant islands. These observations indicate that Symbiodinium 37 disperse much more broadly than previously thought and continuously adapt to specific 38 hosts and reef environments across their range, following the classical Baas Becking’s 39 hypothesis: “Everything is everywhere, but the environment selects”. Overall, our 40 findings confirm horizontal transmission could be a mechanism for broadly dispersing 41 coral species to enhance their local fitness by associating with locally adapted symbionts. 42 Dramatic differences in factors driving the genetic structures of horizontally-transmitting 43 corals and their Symbiodinium imply that viewing their combined genomes as a single 44 evolving entity (‘hologenome’) would be misleading. 45 46 . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/037994 doi: bioRxiv preprint first posted online Feb. 23, 2016;