Phylogeography of Long-spined Sea Urchin Diadema setosum Across the Indo-Malay Archipelago.

Abstract

Widely distributed, broadcast-spawning Diadema sea urchins have been used as model invertebrate species for studying the zoogeography of the tropical Indo-Pacific. So far, the Indo-Malay archipelago, a wide and geographically complex maritime region extending from the eastern Indian Ocean to the western Pacific Ocean, has been under-sampled. This study aims to fill this sampling gap and uncover the phylogeographic structure of the long-spined sea-urchin D. setosum in the central Indo-West pacific region. D. setosum samples (total N = 718) were collected in 13 sites throughout the Indo-Malay archipelago. We sequenced over 1157 bp of COI gene. The Phylogeographic structure was derived from pairwise Ф_ST estimates using multidimensional scaling and hierarchical clustering analysis; biogeographic hypotheses were tested by AMOVA; genetic relationships between haplotypes were summarised in the form of a minimum-spanning network; and pairwise mismatch distributions were compared to the expectations from demographic and spatial expansion models. All samples from the Indo-West Pacific were of the previously uncovered D. setosum-a lineage. Phylogeographic structure was evident: the Andaman Sea population and the northern New Guinea population were genetically distinct. Subtler but significant haplotype-frequency differences distinguished two populations within the Indonesian seas, distributed in a parapatric-like fashion. The phylogeographic partition observed was insufficiently explained by previous biogeographic hypotheses. The haplotype network showed a series of closely related star-shaped haplogroups with a high proportion of singletons. Nucleotide-pairwise mismatch patterns in the two populations from the Indonesian seas were consistent with both demographic and spatial expansion models. While geographic barriers to gene flow were inferred at the western and eastern extremities of the Indo-Malay archipelago, the subtler parapatric pattern observed within the Indonesian seas indicated restriction in gene flow, in a fashion that can hardly be explained by geographic isolation given the dynamic current systems that cross this region. Our results thus raise the hypothesis of subtle reproductive isolation between ecologically incompatible populations. While the coalescence pattern of the Andaman-Sea population suggested demographic stability over evolutionary timescales, that of the two populations from the Indonesian seas indicated recent population expansion, possibly linked to the rapid changes in available D. setosum habitat caused by sea-level oscillations in the late Pleistocene. The phylogeographic patterns observed in this study point to likely allopatric differentiation in the central Indo-West Pacific region. Genetic differences between populations were likely reinforced during interglacials by some form of reproductive isolation.