Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae)

https://doi.org/10.1016/j.ympev.2014.03.008Get rights and content

Highlights

  • We present the first worldwide molecular phylogeny of the shrimp genus Synalpheus.

  • We establish a sequence divergence threshold for Synalpheus using the COI gene.

  • Three out of six traditionally recognized species groups are monophyletic.

  • Our data indicate the presence of multiple potential cryptic species in Synalpheus.

Abstract

The snapping shrimp genus Synalpheus (Alpheidae) is one of the most speciose decapod genera, with over 160 described species worldwide. Most species live in symbiotic relationships with other marine organisms, such as sponges, corals and crinoids, and some sponge-dwelling species have a highly organized, social structure. The present study is the first worldwide molecular phylogenetic analysis of Synalpheus, based on >2200 bp of sequence data from two mitochondrial (COI and 16S) and two nuclear (PEPCK and 18S) loci. Our molecular data show strong support for monophyly of three out of six traditionally recognized morphology-based species groups: the S. brevicarpus, S. comatularum and S. gambarelloides groups. The remaining three species groups (S. paulsoni, S. neomeris and S. coutierei groups) are non-monophyletic in their current composition and will need to be either abandoned or taxonomically redefined. We also identified potential cryptic species of Synalpheus in our dataset, using intraspecific and interspecific sequence variation in COI from the taxonomically well-studied S. gambarelloides group to establish a genetic divergence threshold. We then used both genetic divergence and tree-based criteria (reciprocal monophyly) to identify potential cryptic species in the remaining taxa of the genus. Our results suggest the presence of multiple cryptic lineages in Synalpheus, underlining the need for more integrative taxonomic studies—including morphological, ecological, molecular, and color pattern data—in this biologically interesting genus.

Introduction

Species-rich marine groups present a particular challenge for both taxonomy and systematics, as they often contain cryptic taxa that are difficult to identify using traditional, morphology-based criteria (Knowlton, 1986, Knowlton, 1993, Knowlton, 2000, Hebert et al., 2003, Witt et al., 2006, Barber and Boyce, 2006, Mathews, 2006). Diagnosing and defining species in these groups, and examining their phylogenetic relationships, is critical for our understanding of evolution and diversity of tropical marine invertebrate communities.

Shrimps of the family Alpheidae represent one of the most diverse groups of marine decapod crustaceans, with 45 genera and over 600 described species worldwide (Chace, 1972, Chace, 1988, Anker et al., 2006, De Grave and Fransen, 2011). Alpheid shrimps are among the most abundant decapods in tropical and subtropical, shallow-water habitats, in particular on coral reefs (Pearse, 1932, Ruetzler, 1976, Felder and Chaney, 1979). Many alpheids live in permanent association with a variety of other marine invertebrates and gobiid fishes (Banner and Banner, 1975, Bruce, 1976, Anker et al., 2005, Ríos and Duffy, 2007, Karplus and Thompson, 2011). The genus Synalpheus Spence Bate, 1888 is the second-largest genus in the family, with over 160 described species worldwide (Banner and Banner, 1975, Chace, 1988, De Grave and Fransen, 2011). The ecological diversity of Synalpheus, which includes multiple instances of symbioses with sponges, echinoderms and cnidarians (Fig. 1), and several modes of social organization, has made this genus an attractive model system for studies of speciation, host specialization and evolution of sociality (Duffy, 1992, Duffy, 1996, VandenSpiegel et al., 1998, Duffy and Macdonald, 2010, Hultgren and Duffy, 2012). However, most of the research in the genus Synalpheus has focused on a single clade of 45 described Caribbean sponge-dwelling species in the Synalpheus gambarelloides species group, and examining the evolution of specialized host use across the entire genus requires a robust phylogeny that spans the worldwide diversity of this group.

Due in part to the spectacular diversity of Synalpheus in tropical marine habitats, the taxonomy of many described species remains in an unsatisfying state. This is especially true for numerous Indo-West Pacific and East Pacific taxa, some with problematic synonyms, subspecies and varieties (De Man, 1888, Coutière, 1905, Coutière, 1908, Coutière, 1909, De Man, 1911, Coutière, 1921). Furthermore, almost nothing is known about the phylogenetic structure within this genus worldwide (Banner and Banner, 1975, Anker and De Grave, 2008, Hermoso-Salazar et al., 2008). Coutière, 1908, Coutière, 1909 subdivided the genus into six informal species groups: S. brevicarpus, S. biunguiculatus (later changed to S. coutierei), S. comatularum, S. laevimanus (later changed to S. gambarelloides), S. neomeris, and S. paulsoni groups. Subsequent taxonomic treatments (Banner and Banner, 1975) concluded that only three of these species groups (S. brevicarpus, S. comatularum, and S. gambarelloides groups) had enough morphological support to be taxonomically useful (see also Hermoso-Salazar et al., 2008).

The S. brevicarpus group contains approximately a dozen species (both sponge-symbionts and non-symbiotic, Fig. 1C), some currently under description (Anker, unpublished data), distributed exclusively in the eastern Pacific and western Atlantic. The S. comatularum group includes at least 10 described species, all found in the tropical parts of the Indo-West Pacific; most (if not all) of its members are associates of crinoids (Fig. 1B). The very large S. gambarelloides species group (>70 described species) is distributed worldwide, although the vast majority of species occur in the tropical western Atlantic. It is by far the best-studied group of Synalpheus, in terms of ecology and phylogenetics. All members of the S. gambarelloides group are ecologically quite homogeneous, dwelling exclusively in the interior canals of sponges (Banner and Banner, 1975, Dardeau, 1984, Chace, 1988, Ríos and Duffy, 2007). Molecular studies have consistently indicated strong support for the monophyly of this group, although prior phylogenies sampled only a few taxa outside of the S. gambarelloides group (Duffy et al., 2000, Morrison et al., 2004, Hultgren and Duffy, 2011). Based on these data, Ríos and Duffy (2007) erected a new genus, Zuzalpheus, for the S. gambarelloides group. However, Anker and De Grave (2008) pointed out that Zuzalpheus was separated from Synalpheus based on minor and ambiguous morphological differences, and this rendered the rest of the genus Synalpheus paraphyletic, based on the phylogeny proposed by Morrison et al. (2004). The resolution of relationships within Synalpheus, and possible establishment of morphologically defined subgenera (including Zuzalpheus), requires a much more extensive and worldwide sampling of taxa from all six of Coutière’s species groups worldwide.

Identifying and describing cryptic species complexes is a major challenge for assessing worldwide species diversity in Synalpheus. For example, since Dardeau’s (1984) work on the western Atlantic species of the S. gambarelloides group, many cryptic species complexes have been identified and split into several species; as a result, the total number of described species in the S. gambarelloides group has more than doubled over the last two decades, from 19 to currently 44 (summarized in Hultgren and Duffy, 2011). In several cases, it may be difficult to use morphological characters alone to accurately delimit species; in this group, molecular sequencing has assisted in discriminating between morphologically similar species (Hultgren et al., 2010), and has strongly supported the morphology-based species concepts (Morrison et al., 2004, Hultgren and Duffy, 2011). Overall, a more integrative approach is needed, which includes molecular data (e.g., COI barcoding gene), as well as color patterns, ecology (e.g., hosts for symbiotic species), and traditional morphological characters.

In many animal groups, molecular data are increasingly being used to identify potential cryptic species (Hebert et al., 2004, Witt et al., 2006, Barber and Boyce, 2006, Oliver et al., 2009), with the 650 bp 5′ region of the mitochondrial cytochrome oxidase I (COI) gene the generally accepted DNA barcode marker (Hebert et al., 2003, Goldstein and Desalle, 2010). Some workers have utilized a delimitation threshold of ten times greater than intraspecific distance (Hebert et al., 2004, Witt et al., 2006), and more recently the “gap” between intraspecific and congeneric heterospecific genetic distance in COI has been utilized as a threshold for species delimitation (Lefebure et al., 2006, Costa et al., 2007, Radulovici et al., 2009, Del-Prado et al., 2010, Goldstein and Desalle, 2010, Puillandre et al., 2012). Other workers advocate a tree-based approach, specifically using reciprocal monophyly as a criterion for species delimitation (reviewed in Goldstein and Desalle, 2010), and many studies use some combination of tree-based and genetic barcoding approaches to identify potential cryptic species (Barber and Boyce, 2006, Xavier et al., 2010, Murray et al., 2012). Ultimately, these potential cryptic species can be confirmed by future studies through traditional taxonomic and coalescent-based species tree inference methods.

The main goal of the present study is to propose the first worldwide phylogeny of the genus Synalpheus, including representatives from all six informal species groups (Coutière, 1909, Banner and Banner, 1975) and from all four oceanic provinces (East Atlantic, West Atlantic, East Pacific, and Indo-West Pacific). We constructed phylogenetic trees using molecular sequence data from four loci: two nuclear loci and two mitochondrial loci, including the 5′ region of the mitochondrial COI gene used for genetic barcoding, to assess monophyly of each of the six species groups, and the relationships among these groups. Within the taxonomically well-studied S. gambarelloides group, we calculated intraspecific and interspecific divergence in COI, used these data to establish a genetic distance threshold, and used a combination of tree-based and genetic distance criteria to identify potential cryptic species in the remaining taxa of Synalpheus. This study provides the foundation for further taxonomic work exploring diversity and clarifying phylogenetic relationships within the genus Synalpheus.

Section snippets

Taxon sampling and species identification

Sequence data were generated from specimens of Synalpheus and Alpheus (latter used as outgroup) collected primarily over the last decade (2001–2010), including numerous specimens collected and processed by two of the authors (AA and KH, see Supplementary data 1). We also used 16S sequence data from prior studies (Morrison et al., 2004, Hultgren and Duffy, 2011) and sequence data (COI, 16S, and 18S) generated by the Smithsonian Institution for the Barcode of Life project (archived by the Barcode

Alignment and sequence data

We obtained mitochondrial COI sequence data from 196 individuals representing 93 different species (here including both described and potential cryptic species), which is about 60% of the current described species diversity of Synalpheus. For PEPCK, we obtained sequence data from 91 individuals (67 species); for 16S, we obtained sequence data from 176 individuals (87 species); for 18S we obtained sequence data from 105 individuals (60 species). The complete-data tree (Fig. 2) consisted of 63

Discussion

The first worldwide phylogenetic study of the diverse snapping shrimp genus Synalpheus demonstrates strong support for the monophyly of three out of six species groups originally established by Coutière (1909): the S. gambarelloides, S. brevicarpus, and S. comatularum groups. However, the phylogenetic relationships among these groups, and the other two major clades recovered in the combined-data trees, were generally less resolved.

Acknowledgments

Funding for this study, including support of KH and CH, was provided by Wolcott funds at the Smithsonian Institution. This study could not have been done without the support of Nancy Knowlton (National Museum of Natural History, Smithsonian Institution). This study also benefited greatly from the taxonomic expertise and collections of J. Emmett Duffy (Virginia Institute of Marine Studies). Dr. Amy Driskell (Smithsonian Laboratory of Analytical Biology) provided assistance with barcoding and

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      Since some of these species belonged to putative cryptic species complexes (Table 1, Appendix A), we also sequenced most specimens for gene regions used in previous studies of cryptic species in Alpheus, including the COI 5′ barcoding region (Anker et al., 2008a, 2008b, 2008c; Hurt et al., 2009, 2013), and/or the16S rRNA and COI 3′ region (Williams et al., 2001; Mathews and Anker, 2009; Bracken-Grissom et al., 2014). We used universal COI barcoding primers for the 5′ region (Geller et al., 2013), and otherwise used standard primers and PCR conditions described in previous papers on alpheid shrimps (Mathews and Anker, 2009; Bracken-Grissom et al., 2014; Hultgren et al., 2014). For some small museum specimens, there was not enough tissue for separate barcoding reactions thereforebarcodes are not provided.

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    1

    Current address: Department of Biology, Tennessee Tech University, Cookeville Tennessee, 38505, USA.

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