Global species delimitation and phylogeography of the circumtropical ‘sexy shrimp’ Thor amboinensis reveals a cryptic species complex and secondary contact in the Indo-West Pacific

Benjamin M. Titus, Marymegan Daly, Natalie Hamilton, Michael L. Berumen, J. Antonio Baeza

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

Aim The “sexy shrimp” Thor amboinensis is currently considered a single circumtropical species. However, the tropical oceans are partitioned by hard and soft barriers to dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null hypothesis that T. amboinensis is a single global species, reconstruct its global biogeographical history, and comment on population-level patterns throughout the Tropical Western Atlantic. Location Coral reefs in all tropical oceans. Methods Specimens of Thor amboinensis were obtained through field collection and museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) gene fragments for global species delimitation and phylogenetic analyses (n = 83 individuals, 30 sample localities), while phylogeographical reconstruction in the TWA was based on COI only (n = 303 individuals, 10 sample localities). Results We found evidence for at least five cryptic lineages (9%–22% COI pairwise sequence divergence): four in the Indo-West Pacific and one in the Tropical Western Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the South Central Pacific are more closely related to the Tropical Western Atlantic lineage than to a co-occurring lineage that is widespread throughout the Indo-West Pacific. Concatenated and species tree phylogenetic analyses differ in the placement of an endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. Phylogeographical reconstruction throughout the Tropical Western Atlantic reveals little genetic structure over more than 3,000 km. Main conclusions Thor amboinensis is a species complex that has undergone a series of allopatric speciation events and whose members are in secondary contact in the Indo-West Pacific. Nuclear- and mitochondrial- gene phylogenies show evidence of introgression between lineages inferred to have been separated more than 20 Ma. Phylogenetic discordance between multi-locus analyses suggest that T. amboinensis originated in the Tethys sea and dispersed into the Atlantic and Indo-West Pacific through the Tethys seaway or, alternatively, originated in the Indo-West Pacific and dispersed into the Atlantic around South Africa. Population-level patterns in the Caribbean indicate extensive gene flow across the region.
Original languageEnglish (US)
Pages (from-to)1275-1287
Number of pages13
JournalJournal of Biogeography
Volume45
Issue number6
DOIs
StatePublished - Apr 27 2018

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledged KAUST grant number(s): CRG-1-2012-BER-002
Acknowledgements: We thank the Florida Museum of Natural History and the California Academy of Science for specimens used in this study. We are grateful to Dan Exton, Anna Klompen, Jason Macrander, Todd Melman, Spencer Palombit, Gustav Paulay, Estefanía Rodríguez, Nuno Simoes, Tane Sinclair-Taylor, Jill Titus, Eric Witt, Clay Vondriska, and the Operation Wallacea dive staff for assistance in obtaining specimens and sequence data. Specimens were collected from throughout the Tropical Western Atlantic under permits: SE/A-88-15, PPF/DGOPA-127/14, CZ01/9/9, FKNMS-2012-155, SAL-12-1432A-SR, STT037-14, 140408, MAR/FIS/17, and 19985. This research was supported by funding from a National Science Foundation-Doctoral Dissertation Improvement Grant DEB-1601645, the Florida Fish and Wildlife Conservation Commission, Operation Wallacea, American Philosophical Society, International Society for Reef Studies Graduate Fellowship, PADI Foundation Grant, and American Museum of Natural History Lerner Gray Funds awarded to BMT, and National Geographic Explorers grant awarded to JAB. Additional funding was provided through the Undergraduate Research Office at The Ohio State University to NH, the King Abdullah University of Science and Technology (award CRG-1-2012-BER-002 and baseline research funds to MLB), and by the Trautman Fund, The Ohio State University. Comments from two anonymous reviewers greatly improved this manuscript.

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