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In the Coral Triangle Evidence of host-associated divergence from coral-eating snails (genus Coralliophila) in the Coral Triangle Sara E. Simmonds, Vincent Chou, Samantha H. Cheng, Rita Rachmawati, Hilconida P. Calumpong, G. Ngurah Mahardika & Paul H. Barber Coral Reefs Journal of the International Society for Reef Studies ISSN 0722-4028 Coral Reefs DOI 10.1007/s00338-018-1661-6 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag GmbH Germany, part of Springer Nature. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Coral Reefs https://doi.org/10.1007/s00338-018-1661-6 REPORT Evidence of host-associated divergence from coral-eating snails (genus Coralliophila) in the Coral Triangle 1 1 1 1 Sara E. Simmonds • Vincent Chou • Samantha H. Cheng • Rita Rachmawati • 2 3 1 Hilconida P. Calumpong • G. Ngurah Mahardika • Paul H. Barber Received: 17 March 2017 / Accepted: 29 January 2018 Ó Springer-Verlag GmbH Germany, part of Springer Nature 2018 Abstract We studied how host-associations and geogra- (UCT = 0.427), with divergence among Hawaiian popula- phy shape the genetic structure of sister species of marine tions, the Coral Triangle and the Indian Ocean. Notably, C. snails Coralliophila radula (A. Adams, 1853) and C. vio- violacea showed evidence of ecological divergence; two lacea (Kiener, 1836). These obligate ectoparasites prey lineages were associated with different groups of host coral upon corals and are sympatric throughout much of their species, one widespread found at all sites, and the other ranges in coral reefs of the tropical and subtropical Indo- restricted to the Coral Triangle. Sympatric populations of Pacific. We tested for population genetic structure of snails C. violacea found on different suites of coral species were in relation to geography and their host corals using mtDNA highly divergent (UCT = 0.561, d = 5.13%), suggesting (COI) sequences in minimum spanning trees and AMO- that symbiotic relationships may contribute to lineage VAs. We also examined the evolutionary relationships of diversification in the Coral Triangle. their Porites host coral species using maximum likelihood trees of RAD-seq (restriction site-associated DNA Keywords Marine gastropod Á Parasite Á Sister species Á sequencing) loci mapped to a reference transcriptome. A Porites Á RAD-seq maximum likelihood tree of host corals revealed three distinct clades. Coralliophila radula showed a pronounced genetic break across the Sunda Shelf (UCT = 0.735) but Introduction exhibited no genetic structure with respect to host. C. violacea exhibited significant geographic structure Our understanding of evolution in marine ecosystems is framed by theories developed in terrestrial environments (Miglietta et al. 2011). Historically, researchers have Topic Editor Dr. Line K. Bay invoked geographic-based models of speciation without Electronic supplementary material The online version of this gene flow (i.e. allopatry) to explain the majority of diver- article (https://doi.org/10.1007/s00338-018-1661-6) contains supple- sity in terrestrial systems (Barraclough and Vogler 2000). mentary material, which is available to authorized users. However, such models are not a natural fit for the marine realm (Palumbi 1994; Puebla 2009). Most marine organ- & Sara E. Simmonds [email protected] isms have planktonic larvae that increase the potential for gene flow between geographically separated regions (Rig- 1 Department of Ecology and Evolutionary Biology, University inos and Liggins 2013). Even species with relatively of California Los Angeles, 612 Charles E. Young Dr. East, modest mean dispersal distances can have dispersal kernels Los Angeles, CA 90095, USA 2 with long tails (Kinlan and Gaines 2003), providing suffi- Institute of Environment and Marine Sciences, Silliman cient genetic connectivity to limit population divergence University, 6200 Dumaguete City, Philippines (Slatkin 1987), even across broad geographic scales. 3 Animal Biomedical and Molecular Biology Laboratory, While uncommon, geographic barriers to gene flow in Faculty of Veterinary Medicine, Udayana University Bali, Jl. Raya Sesetan, Gg. Markisa 6, Denpasar, Bali 80223, the ocean do exist, albeit with varying degrees of perme- Indonesia ability. Landmasses are the most obvious, isolating biota in 123 Author's personal copy Coral Reefs different ocean basins (Briggs and Bowen 2013), both sympatrically in coral reefs throughout the tropical and currently (e.g. Isthmus of Panama, see Lessios 2008 for subtropical Indo-Pacific. review) and in the past (e.g. Sunda Shelf, see Ludt and The purpose of this study was to enhance our under- Rocha 2015 for review). However, vast expanses of open- standing of the evolutionary processes generating marine ocean can isolate remote archipelagos like Hawai’i (e.g. biodiversity in the Coral Triangle. Specifically, we tested Polato et al. 2010; Iacchei et al. 2016; Waldrop et al. 2016) the hypothesis that co-distributed populations of C. radula or populations spanning the Eastern Pacific Barrier (e.g. and C. violacea would exhibit concordant patterns of Baums et al. 2012). Additionally, large freshwater outflows phylogeographic structure, patterns that resulted from like the Amazon can form barriers to gene flow for shal- physical processes shaping the phylogeography of other low-water marine species (Rocha 2003). marine organisms in the Coral Triangle. However, because Dispersal barriers are critical to the evolution and dis- parasitic relationships with poritid host corals create the tribution of marine biodiversity, including in the world’s possibility of ecological divergence, we first tested for most diverse marine ecosystem, the Coral Triangle (Barber genetic structure that could result from ecological segre- et al. 2011; Carpenter et al. 2011; Gaither et al. 2011; gation among sympatric populations of snails utilising Gaither and Rocha 2013). Low sea levels during the Plio- different host corals. cene and Pleistocene (Williams and Benzie 1998), and more recent phenomena such as the Halmahera Eddy (Kool et al. 2011), create potent dispersal barriers for various reef Materials and methods organisms (see Barber et al. 2011 and Carpenter et al. 2011 for reviews). Still, allopatric divergence alone may be Field sampling insufficient to explain the Coral Triangle’s exceptional species diversity. Processes such as ecological divergence During 2011–2013, we collected Coralliophila radula and and assortative mating could promote divergence with gene C. violacea from Indo-Pacific locations (N = 14 and N = 17 flow, but remain relatively unexplored in marine systems respectively, Table 1, Fig. 1). These sites span the Sunda (Krug 2011; Miglietta et al. 2011). Shelf Barrier, an area where phylogeographic structure is Ecological divergence is the evolution of reproductive commonly observed (Barber et al. 2011), and also include isolation among populations driven by opposing selection in known areas of isolation (i.e. Hawai’i). At each site, we ecological niches or environments (Schluter and Conte collected 1–15 C. radula and 1–16 C. violacea from 1–6 2009). While widely documented in terrestrial ecosystems, colonies of each host coral species (N = 1–4) (Table 2). In ecological barriers to gene flow in the ocean have only total, we collected 235 C. radula and 328 C. violacea from recently been reported (Krug 2011;Birdetal.2012). In 114 coral colonies (Table 2), representing 12 named Porites terrestrial and freshwater systems, ecological divergence species (Fig. 2). Approximately 50–100% of each snail’s often takes place in sympatry via assortative mating in dif- foot tissue was preserved in 95% ethanol and stored at room ferent microhabitats or on different hosts in species with temperature for DNA analysis. strong symbioses (Hatfield and Schluter 1999;Matsubayashi Porites corals are notoriously difficult to identify in situ et al. 2010). Evidence suggests that ecological factors (Jo- because of their morphological plasticity and small coral- hannesson et al. 2010;Birdetal.2011; Prada and Hellberg lites (Forsman et al. 2015), while genetically similar 2013; Moura et al. 2015) including symbiotic relationships colonies can have vastly different morphologies and vice (Munday et al. 2004;Sotka2005;Fauccietal.2007;Prada versa (Forsman et al. 2009, 2015; Prada et al. 2014a). et al. 2014b; Fritts-Penniman 2016) may similarly drive Therefore, to define coral species both morphologically and ecological divergence in the marine environment. genetically, we collected detailed information about each Marine snails in the genus Coralliophila are symbionts snail’s host; tagged photos of coral colonies in situ; took of anthozoans (Oliverio et al. 2009). The sister species C. macrophotos with a transparent ruler to measure corallites; radula and C. violacea (Oliverio et al. 2009) are ectopar- and sampled tissues for genetic analysis. asites, exhibiting obligate relationships
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