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Caridea: Alpheidae: Synalpheus) Supports Morphology-Based Species Concepts

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Caridea: Alpheidae: Synalpheus) Supports Morphology-Based Species Concepts W&M ScholarWorks VIMS Articles 2011 Multi-Locus Phylogeny Of Sponge-Dwelling Snapping Shrimp (Caridea: Alpheidae: Synalpheus) Supports Morphology-Based Species Concepts KM Hultgren JE Duffy Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Marine Biology Commons Recommended Citation Hultgren, KM and Duffy, JE, "Multi-Locus Phylogeny Of Sponge-Dwelling Snapping Shrimp (Caridea: Alpheidae: Synalpheus) Supports Morphology-Based Species Concepts" (2011). VIMS Articles. 1657. https://scholarworks.wm.edu/vimsarticles/1657 This Article is brought to you for free and open access by W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. JOURNAL OF CRUSTACEAN BIOLOGY, 31(2): 352-360, 2011 Downloaded from https://academic.oup.com/jcb/article-abstract/31/2/352/2419375 by VIRGINIA INSTITUTE OF Marine Science user on 08 August 2019 MULTI-LOCUS PHYLOGENY OF SPONGE-DWELLING SNAPPING SHRIMP (CARIDEA: ALPHEIDAE: SYNALPHEUS) SUPPORTS MORPHOLOGY-BASED SPECIES CONCEPTS Kristin M. Hultgren and J. Emmett Duffy (KMH, [email protected]) National Museum of Natural History, Smithsonian Institution, MRC 163, PO Box 37012, Washington, DC 20013-7012; (JED, [email protected]) Virginia Institute of Marine Science, P.O. Box 1346, Gloucester Pt., Virginia 23062-1346, U.S.A. ABSTRACT Alpheid snapping shrimp are one of the most diverse groups of coral-reef fauna, and sponge-dwelling shrimp in the genus Synalpheus (gambarelloides species group) have in particular become a model system for studying the evolution of social biology and host use in marine invertebrates. Despite recent advances in understanding the evolution and systematics of Synalpheus, the taxonomy and phylogenetic relationships within this group remain challenging. More than 20 new species in the S. gambarelloides species group have been described over the past two decades, primarily within several cryptic species complexes, which has doubled the known diversity of this group in the West Atlantic. Here we construct a new phylogenetic tree describing relationships between 40 different species from the S. gambarelloides-group (119 individuals from across the Caribbean), using a combined dataset consisting of two mitochondrial loci (16S and COI), one nuclear protein-coding gene (elongation-factor 2), and 33 morphological characters. Putative conspecific specimens of Synalpheus from multiple locations across the Caribbean were always monophyletic (with one exception), providing strong support for the validity of species concepts based on morphology. Our study also provides further evidence for the monophyly of the S. gambarelloides-group in the Caribbean, resolves the molecular relationships within many recently described species complexes, and provides a new phylogenetic framework for future evolutionary studies of this group. KEY WORDS: Alpheidae, Caridea, phylogeny, snapping shrimp, Synalpheus gambarelloides DOI: 10.1651/10-3382.1 INTRODUCTION become a model system for studying not only the The snapping shrimp genus Synalpheus is one of the most evolutionary ecology of host use (Duffy, 1992, 1996b; taxonomically and ecologically diverse group of coral-reef Macdonald et al., 2006; Hultgren and Duffy, 2010), but also fauna, with over 150 species worldwide, and many species the ecology and evolution of social biology (Duffy et al., are symbionts with a diverse range of larger host taxa 2000, 2002; Duffy, 2007; Duffy and Macdonald, 2010). (Coutie`re, 1909; Banner and Banner, 1975; Bruce, 1976; Our understanding of the evolutionary ecology of host Rios and Duffy, 2007). Species in the Synalpheus use and social systems in these shrimp has been gambarelloides-group (Nardo, 1847) are by far the most transformed by prior work on the phylogenetics of this well-studied group of these snapping shrimp. The S. group from the West Atlantic (Duffy et al., 2000; Morrison gambarelloides-group is largely limited to the western et al., 2004). Previous phylogenetic work has demonstrated North Atlantic (with some exceptions), is thought to be that eusociality evolved independently at least three times monophyletic based on prior molecular phylogenies in the West Atlantic Synalpheus (Duffy et al., 2000) and (Morrison et al., 2004), and its members share a few key that the high diversity of the S. gambarelloides-group may morphological synapomorphies, most notably a brush of have originated from a rapid species radiation , 5-7 MYA setae on the dactyl of the minor chela (Coutie`re, 1909; Rios (Morrison et al., 2004), concurrent with radiations of and Duffy, 2007). Members of this species group also live several other Caribbean reef-associated species. This period exclusively in the canals of marine sponges (Dardeau, 1984; of ancient rapid cladogenesis is evident in branching Duffy, 1992; Macdonald et al., 2006; Rios and Duffy, 2007). patterns in phylogenies of Synalpheus, which are charac- Although accounts of sponge-dwelling have been noted in terized by short basal branches and poorly supported nodes several other synalpheid and alpheid species (Banner and at the base of the tree, and much better support for more Banner, 1975, 1982), this symbiotic habit is most well terminal species-level nodes (Morrison et al., 2004). documented in members of the S. gambarelloides-group Alternately, this pattern could have resulted from the genes (Duffy, 1996c; Macdonald et al., 2006). Most notably, used to reconstruct relationships; both previously published several species within this group are eusocial—living in phylogenies of Synalpheus relied only on mitochondrial large, reproductively skewed colonies consisting of tens to molecular loci (16s rRNA and cytochrome oxidase I), hundreds of individuals with one or a very few breeding which tend to evolve rapidly and may be less useful in females (Duffy, 1996a, 2007). As such, this group has reconstructing more basal relationships. Nuclear loci 352 HULTGREN AND DUFFY: NEW PHYLOGENY OF SYNALPHEUS 353 typically evolve more slowly than mitochondrial loci distinct populations for 19 of the 40 species of Synalpheus (Palumbi et al., 2001; Sanderson and Shaffer, 2002), and used in this study. Our study resolves molecular relation- serve as independent molecular loci from the nuclear ships in four cryptic species complexes, and provides an genome. As such, nuclear loci have been useful in updated phylogenetic framework for this diverse shrimp reconstructing older (family-level) crustacean relationships group. (Porter et al., 2005; Ahyong et al., 2007; Tsang et al., 2008; Downloaded from https://academic.oup.com/jcb/article-abstract/31/2/352/2419375 by VIRGINIA INSTITUTE OF Marine Science user on 08 August 2019 Bracken et al., 2009), and may be useful in reconstructing the more basal relationships of the S. gambarelloides- MATERIALS AND METHODS group. Taxon Sampling Synalpheus, like many other groups of snapping shrimp For this study, we focused on representatives of the S. gambarelloides- in Alpheidae, are characterized by high levels of cryptic group in the West Atlantic, in which most members of the group are speciation (Morrison et al., 2004; Rios and Duffy, 2007; endemic. We sampled 70 new individual specimens of Synalpheus from the S. gambarelloides-group and 3 species of Synalpheus from outside of Anker and De Grave, 2008; Macdonald et al., 2009; the S. gambarelloides-group from the West Atlantic, and also included Mathews and Anker, 2009), similar to many other coral sequences from 45+ specimens of Synalpheus from a previous study reef-associated organisms (Knowlton, 1993; Duda and (Morrison et al., 2004). Although our sample overlaps broadly with those Kohn, 2005; Puebla et al., 2008). In the West Atlantic 32 species sampled in Morrison et al. (2004), we include 9 additional alone, systematic surveys of sponge-dwelling Synalpheus species of Synalpheus that have recently been described (Rios and Duffy, 2007; Anker and Toth, 2008; Macdonald et al., 2009; Hultgren et al., 2010) have doubled the number of described species in the last or are in the process of being described (Macdonald, Hultgren, Duffy, 14 years from 20 to 43 (Duffy, 1996d, 1998; Rios and unpublished data) [DOI: 10.1651/10-3382.1 on-line Appendix 1]. New Duffy, 1999, 2007; Macdonald and Duffy, 2006; Anker and shrimp vouchers used in this study were collected between 2005 and 2009 Toth, 2008; Macdonald et al., 2009; Hultgren et al., 2010). from Belize (Carrie Bow Cay; 16u489N, 88u059W), Caribbean Panama (Bocas del Toro; 9u209N, 82u159W), Jamaica (Discovery Bay; 18u289N, Twenty of these species (46% of West Atlantic diversity) 77u279W), Curac¸ao (12u129N, 69u49W), and Barbados (13u139N, were formally described subsequent to the most recent 59u389W). In general, shrimp were collected from their host sponges phylogeny of Synalpheus (Morrison et al., 2004). Many of and identified while alive; whole specimens were preserved in 95% these new species belong to closely related species ethanol (pre-2009 collections); for 2009 collections, a sample (legs or eggs) of each specimen was preserved in RNAlater (Applied Biosystems), complexes – groups in which one or two nominal and the rest of the specimen was preserved in 95% ethanol for morphological species were recently split into multiple morphological identification. species, often based on subtle morphological differences. These species complexes and the morphological characters Morphological Characters that define
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