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 Item Type Article Authors Titus, Benjamin M.; Daly, Marymegan; Hamilton, Natalie; Berumen, Michael L.; Baeza, J. Antonio Citation Titus BM, Daly M, Hamilton N, Berumen ML, Baeza JA (2018) 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. Journal of Biogeography. Available: http://dx.doi.org/10.1111/ jbi.13231. Eprint version Post-print DOI 10.1111/jbi.13231 Publisher Wiley Journal Journal of Biogeography Rights Archived with thanks to Journal of Biogeography; This file is an open access version redistributed from: https:// rss.onlinelibrary.wiley.com/doi/am-pdf/10.1111/jbi.13231 Download date 06/10/2021 06:41:04 Link to Item http://hdl.handle.net/10754/627849 1 2 MR BENJAMIN M TITUS (Orcid ID : 0000-0002-0401-1570) 3 PROF. MICHAEL L. BERUMEN (Orcid ID : 0000-0003-2463-2742) 4 5 6 Article type : Research Paper 7 8 9 Article type: Original article 10 11 Thor amboinensis 12 - 13 14 Benjamin M. Titus1, 6, *, Marymegan Daly1, Natalie Hamilton1, Michael L. Berumen2, J. 15 Antonio Baeza3,4,5 16 17 1 Department of Evolution, Ecology, and Organismal Biology, The Ohio State 18 University, Columbus, Ohio, 43212, USA 2 19 Division of Biological and Environmental Science and Engineering, Red Sea Research 20 Center, King Abdullah University of Science and Technology, Thuwal, 23955, Saudi 21 Arabia 22 3 Department of Biological Sciences, 132 Long Hall, Clemson University, Clemson, SC 23 29634, United States of America 24 4 Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, Florida 25 34949, United States of America 26 5 Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica 27 del Norte, Larrondo 1281, Coquimbo, Chile 28 6 Division of Invertebrate Zoology, American Museum of Natural History, Central Park Author Manuscript 29 West at 79th St, New York, NY 10024, USA This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/jbi.13231 This article is protected by copyright. All rights reserved 30 31 * Corresponding author. B.M. Titus, Central Park West at 79th St, New York, NY, 10024, 32 USA. E-mail: [email protected]; [email protected] 33 Running head: Global phylogeography of Thor amboinensis 34 Keywords: crustacean, coral reefs, cryptic species, allopatric speciation, introgression, 35 gene flow 36 37 Word count: 7569 38 39 40 The “sexy shrimp” Thor amboinensis is currently considered a single circumtropical 41 species. However, the tropical oceans are partitioned by hard and soft barriers to 42 dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null 43 hypothesis that T. amboinensis is a single global species, reconstruct its global 44 biogeographic history, and comment on population-level patterns throughout the Tropical 45 Western Atlantic. 46 Location Coral reefs in all tropical oceans 47 Specimens of Thor amboinensis were obtained through field collection and 48 museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) 49 gene fragments for global species delimitation and phylogenetic analyses (n = 83 50 individuals, 30 sample localities), while phylogeographic reconstruction in the TWA was 51 based on COI only (n = 303 individuals, 10 sample localities). 52 We found evidence for at least five cryptic lineages (9-22% COI pairwise 53 sequence divergence): four in the Indo-West Pacific and one in the Tropical Western 54 Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the 55 South Central Pacific are more closely related to the Tropical Western Atlantic lineage 56 than to a co-occurring lineage that is widespread throughout the Indo-West Pacific. 57 Concatenated and species tree phylogenetic analyses differ in the placement of an Author Manuscript 58 endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. 59 Phylogeographic reconstruction throughout the Tropical Western Atlantic reveals little 60 genetic structure over more than 3000 km. This article is protected by copyright. All rights reserved 61 Thor amboinensis is a species complex that has undergone a series of 62 allopatric speciation events and whose members are in secondary contact in the Indo- 63 West Pacific. Nuclear- and mitochondrial- gene phylogenies show evidence of 64 introgression between lineages inferred to have been separated more than 20 million 65 years ago. Phylogenetic discordance between multi-locus analyses suggest that T. 66 amboinensis originated in the Tethys sea and dispersed into the Atlantic and Indo-West 67 Pacific through the Tethys seaway or, alternatively, originated in the Indo-West Pacific 68 and dispersed into the Atlantic around South Africa. Population-level patterns in the 69 Caribbean indicate extensive gene flow across the region. 70 71 I 72 Marine species with circumtropical or cosmopolitan distributions are often large, 73 highly mobile, and migratorial. Many are pelagic (open ocean) and travel thousands of 74 kilometres to forage and reproduce, others maintain exceptionally large effective 75 population sizes through a series of continuously distributed populations (Díaz-Jaimes et 76 al., 2010; Gaither et al., 2016). Coral reef dwelling species exhibiting circumtropical 77 distributions however, are limited to a discontinuous shallow water habitat that represents 78 a fraction of the seafloor, and are spatially restricted after recruitment. These species are 79 reliant on pelagic larval dispersal to maintain global ranges and genetic connections 80 among distant populations. Circumtropically distributed reef-dwelling species thus 81 represent an outstanding opportunity to understand biogeographic patterns of divergence 82 and gene flow at a global scale. Tropical marine habitats are bracketed by cold and 83 temperate waters to the North and South, and partitioned by hard (e.g. continental land 84 masses), soft (e.g. ocean currents; open ocean), and intermittent (e.g. temporal barriers 85 created by sea level rise and fall) barriers to dispersal (reviewed by Cowman & Bellwood 86 2013). Understanding how, or if, these species maintain sufficient gene flow to 87 homogenize distant populations and remain single cosmopolitan species sheds light on 88 population connectivity in the ocean, and the evolutionary and biogeographic processes Author Manuscript 89 driving diversification in tropical marine systems. 90 Major barriers to dispersal that have subdivided the tropical oceans include (i) the 91 closure of the Tethys Sea (Terminal Tethyan Event: TTE) ~12-18 Ma, which separated This article is protected by copyright. All rights reserved 92 the Atlantic from the Indo-Pacific as Africa collided with Eurasia creating the world’s 93 two major ocean basins (reviewed by Cowman & Bellwood); (ii) the formation of the 94 Isthmus of Panama (IOP) ~3.5 Ma (but see O’Dea et al., 2016 for a review on the 95 controversy surrounding this date), that separated the Atlantic from the Eastern Pacific, 96 fundamentally changing major currents in both oceans; and (iii) the Eastern Pacific 97 Barrier (EPB), the largest expanse of open ocean (~5,000 km) on the planet, often 98 considered a “soft barrier,” that has separated the Indo-Pacific from the Eastern Pacific 99 for ~65 Myr (reviewed by Cowman & Bellwood). Less obvious barriers include (iv) the 100 Indo-Pacific Barrier (IPB), centred on the Coral Triangle and considered an intermittent 101 barrier that separates the Indian and Pacific oceans, where divergence between ocean 102 basins originated during the mid-Miocene (15-10 Ma), and has been continually 103 reinforced through the Pleistocene as shallow continental shelves have been periodically 104 exposed and flooded during repeated glacial cycles (~2.5 Ma-11 ka; Cowman & 105 Bellwood, 2013); and (v) the Red Sea Barrier, separating the Red Sea from the Indian 106 Ocean, an intermittent barrier temporally reducing exchange between the two basins by 107 sea level rise and fall during the Pleistocene (DiBattista et al., 2016). Additional open- 108 water soft barriers are responsible for the isolation and creation of smaller endemic 109 biodiversity hotspots within major biogeographic regions, such as Hawaii and Easter 110 Island (Bowen et al., 2016). Thus, most of the major marine biogeographic regions (e.g. 111 Atlantic, Indian Ocean, Central and Eastern Pacific) have a long history of isolation 112 (Cowman & Bellwood, 2013) providing an ideal setting for understanding the role of 113 allopatric speciation as a driver of global biodiversity on coral reefs. 114 The phylogeographic literature suggests that maintaining a global distribution as a 115 single reef-dwelling species is unlikely, and numerous molecular studies have shown that 116 taxa described as globally distributed are typically cryptic species complexes (e.g. 117 Holland et al., 2004; Barroso et al., 2010). To our knowledge, no benthic, reef-dwelling, 118 invertebrate taxa subject to molecular investigation have been confirmed to be a single 119 circumtropical species. Among vertebrates,