Multiple Colonizations Lead to Cryptic Biodiversity in an Island Ecosystem: Comparative Phylogeography of Anchialine Shrimp Species in the Ryukyu Archipelago, Japan

Abstract

Archipelagos of the Indo-West Pacific are considered to be among the richest in the world in biodiversity, and phylogeographic studies generally support either the center of origin or the center of accumulation hypothesis to explain this pattern. To differentiate between these competing hypotheses for organisms from the Indo-West Pacific anchialine ecosystem, defined as coastal bodies of mixohaline water fluctuating with the tides but having no direct oceanic connections, we investigated the genetic variation, population structure, and evolutionary history of three caridean shrimp species (Antecaridina lauensis, Halocaridinides trigonophthalma, and Metabetaeus minutus) in the Ryukyu Archipelago, Japan. We used two mitochondrial genes—cytochrome c oxidase subunit I (COI) and large ribosomal subunit (16S-rDNA)— complemented with genetic examination of available specimens from the same or closely related species from the Indian and Pacific Oceans. In the Ryukyus, each species encompassed 2–3 divergent (9.52%–19.2% COI p-distance) lineages, each having significant population structure and varying geographic distributions. Phylogenetically, the A. lauensis and M. minutus lineages in the Ryukyus were more closely related to ones from outside the archipelago than to one another. These results, when interpreted in the context of Pacific oceanographic currents and geologic history of the Ryukyus, imply multiple colonizations of the archipelago by the three species, consistent with the center of accumulation hypothesis. While this study contributes toward understanding the biodiversity, ecology, and evolution of organisms in the Ryukyus and the Indo-West Pacific, it also has potential utility in establishing conservation strategies for anchialine fauna of the Pacific Basin in general.