Phylogeny and evolution of Indo-Pacific shrimp-associated gobies (Gobiiformes: Gobiidae).

Despite the ubiquity of obligate mutualisms on coral reef ecosystems, little is known about the evolution of many participating species. The shrimp gobies, known primarily from the coral reef habitats of the Indo-Pacific, are small benthic fishes that participate in a remarkable mutualism with alpheid shrimp. In this mutualism, the shrimp build and maintain a burrow that is guarded by the goby, and the shrimp and goby engage in an intricate tactile communication system. The mutualism is obligate for most shrimp gobies as participating species are highly vulnerable to predation when separated from a shrimp partner. We use phylogenetic analysis of nuclear and mitochondrial DNA sequence data to infer evolutionary relationships among shrimp gobies, and between shrimp gobies and their non-mutualistic gobiid relatives. We show that the mutualist shrimp association has arisen twice among gobies, once in a clade composed of Amblyeleotris, Ctenogobiops, and Vanderhorstia, and a second time in a clade including Cryptocentrus, Mahidolia, Tomiamichthys and Stonogobiops. We then compare the evolution of traits within each shrimp goby clade and consider their intrarelationships. We document cryptic diversity among shrimp gobies, with three distinct clades delineated among Mahidolia mysticina specimens captured at the same locality, paired with the same shrimp species. Mahidolia is placed as sister to the Cryptocentrus species Cryptocentrus cinctus; both exhibit pronounced dichromatism, occurring in both brown and yellow (xanthic) forms. We additionally clarify species identities within Amblyeleotris, confirming that widespread similar species Amblyeleotris fasciata, Amblyeleotris steinitzi and Amblyeleotris wheeleri are all distinct. We hypothesize that the flexibility of gobiid gobies and alpheid shrimp to interact with mutualist partners, as well as the apparently highly beneficial nature of mutualism between them, has contributed to the dual evolution of shrimp-association among Indo-Pacific gobies.