Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus)

A common challenge in reconstructing phylogenies involves a high frequency of short internal branches, which makes basal relationships difficult to resolve. Often it is not clear whether this pattern results from insufficient or inappropriate data, versus from a rapid evolutionary radiation. The snapping shrimp genus Synalpheus, which contains in excess of 100 species and is a prominent component of coral-reef faunas worldwide, provides an example. Its taxonomy has long been problematic due to the subtlety of diagnostic characters and apparently widespread variability within species. Here we use partial mt COI and 16S rRNA sequences and morphological characters to reconstruct relationships among 31 species in the morphologically well-defined gambarelloides species group, a putative clade of obligate sponge associates that is mostly endemic to the Caribbean and contains the only known eusocial marine animals. Analysis of the combined data produced a single tree with good support for many terminal clades and for relationships with outgroups, but poor support for branches near the base of the gambarelloides group. Most basal branches are extremely short and terminal branches are long, suggesting a relatively ancient, but rapid radiation of the gambarelloides group. This hypothesis is supported by significant departure from a null model of temporally random cladogenesis. Calibration of divergence times among gambarelloides-group species using data from three geminate pairs of Synalpheus species separated by the isthmus of Panamá suggests a major radiation between approximately 5 and 7 Mya, a few My before final closure of the Panamanian seaway during a period of spreading carbonate environments in the Caribbean; a second, smaller radiation occurred approximately 4 Mya. This molecular evidence for a rapid radiation among Caribbean marine organisms in the late Miocene/early Pliocene is strikingly similar to patterns documented from fossil data for several other Caribbean reef-associated invertebrate taxa. The similar patterns and timing of cladogenesis evidenced by molecular and fossil data for different Caribbean and East Pacific taxa suggests that the radiation involved a wide range of organisms, and strengthens the case that poor basal resolution in the gambarelloides group of Synalpheus reflects a real evolutionary phenomenon. The rapid radiation also helps explain the historical difficulty of diagnosing species in Synalpheus.