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Genetic Variation and Geographic Differentiation in the Marine Triclad

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Genetic Variation and Geographic Differentiation in the Marine Triclad Genetic variation and geographic differentiation in the marine triclad Bdelloura candida (Platyhelminthes, Tricladida, Maricola), ectocommensal on the American horseshoe crab Limulus polyphemus The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citation Riesgo, Ana, Emily A. Burke, Christopher Laumer, and Gonzalo Giribet. 2017. “Genetic variation and geographic differentiation in the marine triclad Bdelloura candida (Platyhelminthes, Tricladida, Maricola), ectocommensal on the American horseshoe crab Limulus polyphemus.” Marine Biology 164 (5): 111. doi:10.1007/ s00227-017-3132-y. http://dx.doi.org/10.1007/s00227-017-3132-y. Published Version doi:10.1007/s00227-017-3132-y Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:33029986 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA Mar Biol (2017) 164:111 DOI 10.1007/s00227-017-3132-y ORIGINAL PAPER Genetic variation and geographic differentiation in the marine triclad Bdelloura candida (Platyhelminthes, Tricladida, Maricola), ectocommensal on the American horseshoe crab Limulus polyphemus Ana Riesgo1 · Emily A. Burke2 · Christopher Laumer3,4 · Gonzalo Giribet2 Received: 17 September 2016 / Accepted: 30 March 2017 / Published online: 20 April 2017 © The Author(s) 2017. This article is an open access publication Abstract Bdelloura candida (Platyhelminthes, Tricladida, fow. Even though previous studies have suggested that Maricola) is an ectocommensal symbiont on the American the populations of the host may be in decline, those of B. horseshoe crab Limulus polyphemus, living on the book candida remain stable, and some even shows signatures of gills and appendages, where it spends its entire life. Given expansion. Our results indicate that the phylogeography of its limited dispersal capabilities and its inability to live out- these marine ectocommensal triclads closely mirrors that of side of the host, we hypothesized a genetic structure that its Limulus host, and highlight the challenges to both host parallels that of its host. We obtained 84 planarian individu- and symbiont to genetically connect populations across als from 19 horseshoe crabs collected from 10 sites from their distribution. Massachusetts to Florida. We amplifed the mitochondrial 16S rRNA and the nuclear internal transcribed spacer 2 and conducted phylogeographic and population genetic analy- Introduction ses, which show a clear and strong genetic break between the populations in the Atlantic and the Gulf coasts. Among The study of symbiosis is a growing feld in biology, the Atlantic populations, two additional, weaker barriers requiring integration of multiple disciplines (McFall-Ngai located along Cape Hatteras and Cape Cod restrict gene 2008). Symbiotic relationships among different phyla are often “loose”, especially among ectocommensal animals, which are commonly non-specifc. However, many such Responsible Editor: T. Reusch. ectocommensal relationships are known to be strictly spe- Reviewed by A. Waeschenbach and an undisclosed expert. cifc, such as those of cycliophorans with their nephropid (clawed) lobsters (Funch and Kristensen 1995; Obst et al. Electronic supplementary material The online version of this 2006), where a faithful one-to-one species–host relation- article (doi:10.1007/s00227-017-3132-y) contains supplementary ship exists, even in places where two host species coexist material, which is available to authorized users. (Baker et al. 2007; Baker and Giribet 2007). In this case * Ana Riesgo it is easy to appeal to the phenomenon of co-speciation, [email protected] as each lobster host has a different ectocommensal spe- cies of Symbion, and these have never been found in non- 1 Department of Life Sciences (Invertebrate Division), nephropid hosts (it is thought that the American lobster can The Natural History Museum of London, Cromwell Road, London SW7 5BD, UK have up to three cryptic species of Symbion in the S. ameri- canus complex, but these are not shared with any other host 2 Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, species). In general, symbiont and host share gene fow and 26 Oxford Street, Cambridge, MA 02138, USA their genetic structure is linked, the symbiont mirroring 3 EMBL‑European Bioinformatics Institute, Wellcome Trust the genetic structure of the host (Blasco-Costa and Poulin Genome Campus, Hinxton, Cambridgeshire CB10 1SD, UK 2013), although the global level of population genetic dif- 4 Wellcome Trust Sanger Institute, Wellcome Trust Genome ferentiation is usually lower in symbionts and parasites than Campus, Hinxton, Cambridgeshire CB10 1SA, UK in hosts (Mazé-Guilmo et al. 2016). However, species traits 1 3 111 Page 2 of 14 Mar Biol (2017) 164:111 (e.g., size and life cycle) other than host genetic structure Ropes 1987; Shuster 2003). However, many of these pop- can have an effect in shaping symbiont structure, as shown ulations have suffered recent decline due to a diversity of in two recent meta-analyses of host-symbiont genetic struc- anthropogenic factors (Faurby et al. 2010). Genetically, a ture (Blasco-Costa and Poulin 2013; Mazé-Guilmo et al. marked structure exists among specimens north and south 2016). of northeastern Florida in mitochondrial DNA (Saunders A potentially similar case is that of the members of et al. 1986a), allozymes (Selander et al. 1970), micros- Bdellouridae, a family of marine planarians (Platyhel- atellite nuclear markers (King et al. 2015), and morphol- minthes, Tricladida, Maricola) and its host, the American ogy (Riska 1981), in what constitutes a well-documented horseshoe crab, Limulus polyphemus (Linnaeus, 1758). The marine biogeographic break (e.g., Avise 1992; Lee and members of the genus Bdelloura are characterized by the Foighil 2004). This genetic structure most probably results absence of eye lenses, a posterior adhesive caudal disk set from the territoriality of adults and the low dispersal capac- off from the rest of the body, and numerous testes distrib- ity of the trilobite larva, which has been mainly studied in uted throughout the body (Leidy 1851). The genus includes the Delaware estuary (Botton and Loveland 1987). Their three described species, Bdelloura candida (Girard, 1850), transport as passive particles by the alongshore currents B. propinqua Wheeler, 1894, and B. wheeleri Wilhelmi, was estimated between 144 and 432 m per h, although they 1909, of which B. candida is the most widespread and eas- tend to remain in the close vicinity of the shoreline (Bot- ily identifed (Sluys 1989). ton and Loveland 2003). Recapture data from L. polyphe- Bdelloura candida was described from Chelsea Beach, mus tag-and-release experiments provide a mean recovery Massachusetts (Girard 1850). Their whitish-coloured, distance of approximately 3–4 miles (Baptiste et al. 1957; oval-shaped bodies are about 15 4 mm (sometimes up Sokoloff 1978). Furthermore, many adults were shown to × to 2 cm in length) while moving, according to Wilhelmi remain tightly associated with their particular estuary or (1908). In his monograph, Sluys (1989) described B. can- local shoreline. This philopatry regarding reproductive and dida’s characteristic undulated sides, large central pharynx, behavioural habits is also suggestive of a pattern of genetic and broad caudal disk that changes shape depending on structure. the state of contraction. Bdelloura candida lives ectocom- Several authors have already postulated that genetic mensally on the walking appendages, carapace, and book structure from some symbionts/parasites can mirror and gills of the Atlantic horseshoe crab. Despite relying heav- even complement genetic data from their hosts (Nieberd- ily on their hosts for indirect nutrition, the feeding mecha- ing and Olivieri 2007). Since genetic data are not available nisms and digestive structures of the commensal species for B. candida to test whether its genetic structure mirrors of Bdellouridae do not differ signifcantly from those of that of L. polyphemus, we examined specimens from hosts their free-living relatives (Jennings 1977). Bdelloura can- at ten sites along the Atlantic and Gulf coasts of the USA, dida can be found concomitantly with its host throughout as we wanted to ascertain whether the commensal showed its distribution range along the Gulf and Atlantic coasts of the signature of the host’s phylogeographic structure. North America (Sekiguchi and Shuster 2009). As a direct developer (Sluys 1989), B. candida hatches from cocoons attached to the book gills of L. polyphemus, and it has, Materials and methods therefore, little capacity for dispersal. The adults cannot survive independently, living exclusively on its L. polyphe- Sample collection mus host; thus, they must recolonize the same host or a nearby individual after Limulus moults, a process that prob- A total of 84 specimens of B. candida were collected from ably relies on chemical signalling (Chevalier and Steinbach 18 L. polyphemus individuals at ten sampling sites along 1969). This strict association to horseshoe crabs makes B. the Atlantic and Gulf coasts (Table 1). Specimens were candida an excellent model for phylogeographic research fxed in 96% ethanol and stored at 80 °C for long-term − of symbiotic organisms. preservation. All host and
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