Molecular systematics of caridean shrimps based on five nuclear genes: Implications for superfamily...

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Zoologischer Anzeiger 250 (2011) 270–279

olecular systematics of caridean shrimps based on five nuclear genes:mplications for superfamily classification

hi Pang Lia, Sammy De Graveb, Tin-Yam Chanc,d, Ho Chee Leia, Ka Hou Chua,∗

Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, N. T., Hong KongOxford University Museum of Natural History, Parks Road, Oxford OX1 3PW, United KingdomInstitute of Marine Biology, National Taiwan Ocean University, 2 Pei-Ning Road, Keelung 20224, TaiwanCenter of Excellence for Marine Bioenviroment and Biotechnology, National Taiwan Ocean University,

Pei-Ning Road, Keelung 20224, Taiwan

eceived 26 September 2010; received in revised form 22 February 2011; accepted 12 April 2011orresponding editor: S. De Grave.

bstract

Caridean shrimps are the second most diverse group of Decapoda. Over the years, several different systematic classifications,xclusively based on morphology, have been proposed, but the classification of the infraorder Caridea remains unresolved. In thistudy, five nuclear genes, 18S rRNA, enolase, histone 3, phosphoenolpyruvate carboxykinase and sodium–potassium ATPase-subunit, were used to examine the systematic status of caridean families and superfamilies. We constructed gene trees basedn a combined dataset of 3819 bp, containing 35 caridean species from 19 families in 11 superfamilies. At the family level, andased on our restricted representation, our molecular data support monophyly of the families Glyphocrangonidae, Crangonidae,andalidae, Alpheidae, Rhynchocinetidae, Nematocarcinidae, Pasiphaeidae, Atyidae and Stylodactylidae. In contrast, both theippolytidae and Palaemonidae are polyphyletic in our analysis. Two major clades are revealed. The Alpheidae, Hippolytidae,rangonidae, Glyphocrangonidae, Barbouriidae, Pandalidae, Hymenoceridae, Gnathophyllidae and Palaemonidae make up

he first clade, while the second clade comprises the Rhynchocinetidae, Oplophoridae, Nematocarcinidae, Alvinocarididae,ampylonotidae, Pasiphaeidae and Eugonatonotidae. Two families, Bathypalaemonellidae and Stylodactylidae, are shown toe basal groups in our tree. At the superfamily level, our results do not support the currently accepted superfamily classification,lthough there is support for a superfamily Palaemonoidea, though only three out of its eight families are included. The results
uggest that the currently accepted superfamily classification of the Caridea does not reflect their evolutionary relationships.
major revision of the higher systematics of Caridea appears thus to be vital, ideally incorporating both molecular andorphological evidence.

2011 Elsevier GmbH. All rights reserved.

es; Sup
eywords: Decapoda; Caridea; Phylogenetics; Protein-coding gen
∗Corresponding author. Tel.: +852 2609 6772.E-mail addresses: [email protected] (C.P. Li),

[email protected] (S. De Grave), [email protected]. Chan), [email protected] (H.C. Lei),[email protected] (K.H. Chu).

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044-5231/$ – see front matter © 2011 Elsevier GmbH. All rights reserved.oi:10.1016/j.jcz.2011.04.003

erfamily

. Introduction

Caridean shrimps are the second most diverse group ofecapoda, encountered from tropical to polar regions, in botharine and freshwater habitats. Caridean shrimps can on the
hole be characterized by the following features: (1) carry-
ng their eggs until hatching; (2) the absence of chelae onhe third pereopods; and (3) pleura of second pleomere over-

dx.doi.org/10.1016/j.jcz.2011.04.003

mailto:[email protected]





dx.doi.org/10.1016/j.jcz.2011.04.003


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apping those of first and third. Over the last century or so,everal classification schemes of Caridea were proposed (seeeview in Holthuis, 1993), but the phylogenetic relationshipsithin the Caridea, and the systematic status of the caridean

uperfamilies and families remain relatively unresolved. Theurrently accepted scheme is outlined in De Grave et al.2009), which is based on the evolutionary schemes of Chace1992) and Holthuis (1993), which in turn build extensivelyn older schemes (Ortmann, 1890; Alcock, 1901; Borradaile,907; Calman, 1909; Bouvier, 1917; Holthuis, 1955; Balss,957). Chace (1992), and followed in this by Holthuis (1993)argely utilized the structure of the three anterior pairs of pere-pods, the six pairs of mouthparts and the gill and exopodomplement, to divide the Caridea into 28 families placed in5 superfamilies. Minor changes at family and superfamilyevels and additions were made by Bruce (1993), Vereshchaka1997), Martin and Davis (2001), De Grave and Moosa (2004)nd others. De Grave et al. (2009) recognize 36 familiesithin the Caridea placed in 16 superfamilies. More recent

hanges are the clarification of the status of Galatheacarisbyssalis Vereshchaka (1997) as the megalopal stage of Eug-natonotus chacei Chan and Yu, 1991 by De Grave et al.2010) and the removal of the superfamily Procaridoidea to aeparate infraorder by Bracken et al. (2010). Thus, currently4 families remain in Caridea, placed in 13 superfamilies.Two alternative schemes have been proposed over the

ears. Thompson (1967), utilizing a somewhat rudimen-ary phylogeny, divided the then known Caridea into tenuperfamilies and 23 families, making minor changes to theolthuis (1955) classification by moving a few families tother superfamilies and erecting a new superfamily. Far moreadical was the work by Christoffersen (1987, 1988, 1989a,b,990), who using manual cladistic analysis suggested arofound departure from the Holthuis (1955) scheme, cul-inating in a new classification in which 36 families are

ecognized, placed in eight superfamilies (Christoffersen,990). As discussed in Martin and Davis (2001), his propos-ls have not yet met with wide acceptance, with most workersreferring instead to follow the non-phylogenetic Chace-olthuis scheme, more in deference to their vast knowledgef carideans than anything else. Nevertheless, some sugges-ions put forward by Christoffersen have been accepted byecent workers, for instance the recognition of the Alvinocari-idae Christoffersen, 1986 and Barbouriidae Christoffersen,987 and it is becoming clear that more of his insights willecome mainstream as phylogenetic studies unfold further.

As both the non-phylogenetic classification of Chace-olthuis and the cladistic classification of Christoffersen

re based solely on morphological characters, the classi-cation of the infraorder at both superfamily and family

evels remains unstable. The main limitations of exclusivelyelying on morphological characters to classify carideans
re that systematicists have emphasized different morpho-ogical characters in their respective schemes, and that theurrent morphological characters emphasized, such as thetructure of the first two pereopods, carapace ornamenta-
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ion and mouthpart structure are limited to external featuresn adult morphology and are further of unproven homologysee discussion in Fransen and De Grave, 2009). A moreigid approach should be more integrative and incorporatearval characters, internal characters such as foregut ossiclesnd more recently emphasized structures, such as the carpo-ropodal brush (De Grave and Goulding, this volume). Butore importantly, should draw on the considerable advan-

ages of molecular systematics, a still poorly explored avenuef study in Caridea (Fransen and De Grave, 2009).

The first molecular systematic study at family level was byracken et al. (2009), who based on mitochondrial (16S) anduclear (18S) ribosomal DNA data from 104 species from0 families in 14 superfamilies, questioned the arrangementf the currently accepted caridean superfamily classifica-ion, as well as the monophyly of several families, suchs the Hippolytidae, Palaemonidae and Pasiphaeidae. How-ver, due to the weak resolving power of both 16S and 18SRNA genes at higher taxonomic levels, the relationshipsithin the Caridea remained relatively poorly resolved. In

he present study, aside from 18S rRNA, four protein-codinguclear genes, enolase, histone (H3), phosphoenolpyruvatearboxykinase (PEPCK) and sodium–potassium ATPase �-ubunit (NaK), were used to examine the systematic status ofhe currently accepted caridean superfamilies and families.uclear protein-coding genes have been used to infer rela-

ionships among higher taxonomic level groups in insectsor many years (Friedlander et al., 1996; Leys et al., 2002)nd Tsang et al. (2008) showed promising results in infer-ing phylogenetic relationships among decapod infraordersith two nuclear protein-coding gene markers, NaK andEPCK. These have subsequently been applied to resolve

he phylogeny of the Palinuridae (Tsang et al., 2009) andenaeoidea (Ma et al., 2009). Most recently, Tsang et al. (inress) furnished some important insights in the phylogenyf the Anomura based on five nuclear protein-coding genes,ncluding arginine kinase (AK), enolase, glyceraldehyde 3-hosphate dehydrogenase (GAPDH), NaK and PEPCK. Its thus clear that nuclear protein-coding genes are capablef resolving phylogenetic relationships among taxa at higheraxonomic levels within the Decapoda. By constructing theene trees of 35 caridean species from 19 families and 11uperfamilies, we thus attempt to provide new insights intohe classification of the infraorder Caridea at the superfamilyevel.

. Materials and methods

.1. Sample collection

A total of 35 species from 19 caridean families in 11
uperfamilies plus one outgroup species, Stenopus hispidusOlivier, 1811), were used in this study (Table 1), outf 34 families and 13 superfamilies (De Grave et al.,009). Eleven of the 19 families, the Pasiphaeidae, Nema-

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Table 1. Details of specimens and sequences used in this study (specimens from Hong Kong and Japan were purchased from aquarium shops with origins unknown). Classification followsDe Grave et al. (2009). *MSLKHC, Marine Science Laboratory, The Chinese University of Hong Kong; NMV, Museum Victoria, Australia; NSMT-Cr, National Science Museum, Tokyo;NTOU, National Taiwan Ocean University in Keelung, Taiwan; OUMNH-ZC, Oxford University Museum of Natural History, Zoological Collection, UK.

Superfamily Family Species Samplinglocality

Voucher ID* GenBank accession number

18S Enolase H3 NaK PEPCK

Pasiphaeoidea Pasiphaeidae Pasiphaea japonica Taiwan NTOU M00999 JF346260 JF346295 JF346331 JF346367 JF346403Pasiphaea levicarinata Taiwan NTOU M01000 JF346261 JF346296 JF346332 JF346368 JF346404

Oplophoroidea Oplophoridae Systellapsis pellucida Taiwan NTOU M01001 JF346250 JF346283 JF346319 JF346355 JF346391Atyoidea Atyidae Caridina japonica Taiwan NTOU M01002 JF346236 JF346267 JF346303 JF346339 JF346375

Atyopsis moluccensis Hong Kong NTOU M00728 JF346252 JF346286 JF346322 JF346358 JF346394Bresilioidea Alvinocarididae Alvinocaris longirostris Okinawa NTOU M01014 JF346247 JF346279 JF346315 JF346351 JF346387Nematocarcinoidea Eugonatonotidae Eugonatonotus chacei Taiwan NTOU M00876 DQ642858 JF346274 JF346310 JF346346 JF346382

Nematocarcinidae Nematocarcinus aff. combensis Taiwan NTOU M00724 JF346238 JF346269 JF346305 JF346341 JF346377Nematocarcinus gracilis Taiwan NTOU M00725 JF346240 JF346271 JF346307 JF346343 JF346379Nematocarcinus tenuipes Taiwan NTOU M01003 JF346248 JF346280 JF346316 JF346352 JF346388

Rhynchocinetidae Cinetorhynchus erythrostictus Taiwan NTOU M00690 JF346242 JF346273 JF346309 JF346345 JF346381Rhynchocinetes conspiciocellus Taiwan NTOU M00904 JF346243 JF346275 JF346311 JF346347 JF346383Rhynchocinetes uritai Taiwan NTOU M00679 JF346245 JF346277 JF346313 JF346349 JF346385Rhynchocinetes durbanensis Hong Kong MSLKHC-Rhdur JF346251 JF346285 JF346321 JF346357 JF346393

Stylodactyloidea Stylodactylidae Stylodactylus major Taiwan NTOU M01004 JF346237 JF346268 JF346304 JF346340 JF346376Stylodactylus multidentatus Taiwan NTOU M01005 JF346256 JF346290 JF346326 JF346362 JF346398Parastylodactylus bimaxillaris Taiwan NTOU M01006 JF346259 JF346294 JF346330 JF346366 JF346402

Campylonotoidea Bathypalaemonellidae Bathypalaemonetes brevirostris Taiwan NTOU M01007 JF346239 JF346270 JF346306 JF346342 JF346378Campylonotidae Campylonotus rathbunae Australia NMV J54342 JF346246 JF346278 JF346314 JF346350 JF346386

Palaemonoidea Gnathophyllidae Gnathophyllum americanum Philippines NTOU M01008 DQ642848 JF346281 JF346317 JF346353 JF346389Hymenoceridae Hymenocera picta Japan NSMT-Cr DQ642855 JF346292 JF346328 JF346364 JF346400Palaemonidae Macrobrachium rosenbergii Hong Kong MSLKHC-Maros DQ642856 JF346284 JF346320 JF346356 JF346392

Periclimenes brevicarpalis Hong Kong MSLKHC-CA22Pebre JF346254 JF346288 JF346324 JF346360 JF346396Alpheoidea Alpheidae Alpheus gracilipes Moorea OUMNH-ZC.2011.5.021 DQ642859 JF346299 JF346335 JF346371 JF346407

Metalpheus rostratipes Moorea OUMNH-ZC 2011.5.028 JF346264 JF346300 JF346336 JF346372 JF346408Betaeus longidactylus California MSLKHC-CA24Belon JF346263 JF346298 JF346334 JF346370 JF346406

Hippolytidae Saron marmoratus Taiwan NTOU M01009 JF346244 JF346276 JF346312 JF346348 JF346384Lysmata amboinensis Hong Kong MSLKHC-CA23Lyamb JF346249 JF346282 JF346318 JF346354 JF346390

Barbouriidae Janicea antiguensis Cape Verde OUMNH-ZC 2044.15.002 JF346262 JF346297 JF346333 JF346369 JF346405Pandaloidea Pandalidae Heterocarpus abulbus Taiwan NTOU M00707 JF346257 JF346291 JF346327 JF346363 JF346399

Plesionika grandis Taiwan NTOU M01010 JF346258 JF346293 JF346329 JF346365 JF346401Crangonoidea Crangonidae Neocrangon sagamiensis Taiwan NTOU M01011 JF346234 JF346265 JF346301 JF346337 JF346373

Parapontocaris aspera Taiwan NTOU M01012 JF346235 JF346266 JF346302 JF346338 JF346374Glyphocrangonidae Glyphocrangon stenolepis Taiwan NTOU M01013 JF346241 JF346272 JF346308 JF346344 JF346380

Glyphocrangon perplexa Taiwan NTOU M00706 JF346255 JF346289 JF346325 JF346361 JF346397Outgroup Stenopodidae Stenopus hispidus Hong Kong MSLKHC-Sthis JF346253 JF346287 JF346323 JF346359 JF346395


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ocarcinidae, Oplophoridae, Glyphocrangonidae, Campy-onotidae, Alvinocarididae, Eugonatonotidae, Gnathophyll-dae, Hymenoceridae, Barbouriidae and Bathypalaemonel-idae, had only one genus included in the present study,lthough it should be noted that three of them are actuallyonogeneric families (Glyphocrangonidae, Campylonoti-

ae, Eugonatonotidae). At the superfamily level, only oneamily from each of the superfamilies Bresilioidea andandaloidea was included in the present study. Similar to

he monogeneric families, four included superfamilies areurrently comprised of a single family (Oplophoroidea, Aty-idea, Stylodactyloidea, Pasiphaeoidea), but see below for

discussion on Oplophoroidea. Thus the taxon coveragef this study allowed us to examine the systematic sta-us of five superfamilies containing more than one family,he Nematocarcinoidea, Campylonotoidea, Palaemonoidea,lpheoidea and Crangonoidea, as well as the interrelation-

hip between the 11 included superfamilies and 19 families.ll specimens were identified to species level by the second or

hird author.

.2. Molecular analysis

The whole specimen, pleopods or eggs of the shrimp spec-mens (about 15 mg) was used for DNA extraction using aIAamp DNA Mini Kit, DNA was then eluted in 200 �l ofilli-Q H2O, and stored in −20 ◦C freezer. Partial segments

rom five nuclear genes, enolase (∼370 bp), H3 (∼350 bp),aK (∼670 bp), PEPCK (ranging from 550 to 800 bp) and8S rRNA (∼1800 bp), were amplified by polymerase chaineaction (PCR) (Saiki et al., 1988). Reactions were performedn a 50 �l reaction that contained 5–10 �l of DNA template,.4 �M of each primer, 0.2 �M of dNTP, 2.5 units of Taqolymerase (Takara, Dalian, China), and 1× reaction bufferith 1.5 mM of MgCl2.For the enolase and H3 segments, PCR products were

mplified using primers EA2/ES2 (Tsang et al., in press) andF/AR (Colgan et al., 1998), respectively, and the thermal

ycle was as follows: initial denaturation for 3 min at 94 ◦C,ollowed by 33 cycles of 30 s at 94 ◦C, 30 s at 53 ◦C, and 50 st 72 ◦C, with a final extension at 72 ◦C for 3 min. For themplification of the NaK segment, the primers FB/NR (Tsangt al., 2008) were used, and the thermal cycle used was similaro that above except the annealing temperature was increasedo 56 ◦C. Two primer sets were used to amplify the PEPCKegment. The 5′ primers were PD or PA3 while the 3′ primersere PR or PR3 (Tsang et al., 2008). The thermal cycling was

nitial denaturation for 3 min at 94 ◦C, followed by 33 cyclesf 30 s at 94 ◦C, 30 seconds from 52 to 56 ◦C (with differ-nt primer combinations), and 1 min at 72 ◦C, with a finalxtension at 72 ◦C for 3 min. The 18S rRNA segment was
mplified with primers 18SA/18SB (Medlin et al., 1988), andhe thermal cycling used was similar to that for amplifyinghe enolase and H3 segments, except the extension time wasncreased from 50 s to 2 min. Prior to sequencing, PCR prod-
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iger 250 (2011) 270–279 273

cts were purified by either the QIAquick PCR purificationit or the QIAquick gel purification kit.The enolase, H3, NaK and PEPCK gene segments were

equenced using the same forward and reverse primers forCR amplification. To sequence the 18S rRNA gene region,our internal primers, 18S L, 18S C, 18S Y and 18S OApakupakul et al., 1999) were used to amplify three overlap-ing fragments each of ∼600 bp. The purified PCR productsforward and reverse) were loaded onto an ABI 3730xlenetic Analyzer for analysis. The sequencing data fromoth strands were checked and confirmed by eye using ABIeqEditor before data analysis. All sequences used in thistudy were first aligned with MAFFT (Katoh, 2008), andhen checked by eye. The best-fit models of DNA substitutionor each dataset and the combined dataset were determinedsing Modeltest version 3.7 (Posada and Crandall, 1998)nd used for maximum likelihood (ML) (Felsenstein, 1981)nd Bayesian Inference (BI) analyses. In order to improvehe resolving power of the phylogenetic trees, five nuclearenes were combined for analyses in this study since thispproach could help to increase resolving power in differ-nt taxonomic levels (Ahyong and O’Meally, 2004; Portert al., 2005). Phylogenetic trees were reconstructed usingaximum parsimony (MP) (Camin and Sokal, 1965), ML

nd BI approaches. For the MP analysis, the phylogeneticree construction was performed using PAUP* (version 4.0eta version 10; Swofford, 2002). Gaps were treated as thefth character and the analyses were done with random-equence addition. Heuristic search was undertaken using0 random addition sequence starting trees. The ML phylo-enetic tree reconstruction was conducted using PhyML 3.0Guindon and Gascuel, 2003) with computations performedn the ATGC bioinformatics platform. The confidence levelt each branch was evaluated by performing bootstrappingFelsenstein, 1985) with 1000 pseudoreplicates in both MPnd ML analyses.

The BI analysis was conducted in BEAST v1.5.3Drummond and Rambaut, 2003). The combined datasetas partitioned and analyzed using parameters selected byodeltest from individual dataset. A total of 10,000,000

enerations were performed for the combined dataset, withampling every 100 generations, and the first 25% treesi.e., 25,000 trees for combined dataset) were discarded asburn-in”. To ensure that stationarity had been reached, allhylogenetic parameters were checked with Tracer v 1.5Rambaut and Drummond, 2007).

. Results

The combined dataset of the five genes consists of 3819 bprom 35 caridean species plus S. hispidus as the outgroup. The
est-fit model of the combined dataset suggested by Model-est 3.7 was General Time Reversible incorporating invariableites and rate variation among sites (GTR + I + G). The best-t models selected by Modeltest for the individual datasets


274 C.P. Li et al. / Zoologischer Anzeiger 250 (2011) 270–279

Fig. 1. Phylogenetic tree resolved by Bayesian Inference analysis of DNA sequences based on the combined dataset of five nuclear genes.Bayesian posterior probabilities (in bold) and bootstrap values (based on 1000 pseudoreplicates) from maximum parsimony and maximumlikelihood (in bold italics) analyses are indicated on each branch. Only values higher than 50% are shown. Caridean families according toDe Grave et al. (2009) are listed after each species. Superfamily abbreviations follow each species, in both the Chace-Holthuis scheme (DeG n (199

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rave et al., 2009) and the alternative classification of Christofferse

as GTR + I + G for enolase, NaK, PEPCK and H3, whileamura-Nei (TrN) + G + I was selected for 18S rRNA dataset.mong the 11 families for which more than one taxon was

xamined, nine of them, viz. the Atyidae, Rhynchocinetidae,ematocarcinidae, Pasiphaeidae, Pandalidae, Crangonidae,lyphocrangonidae, Alpheidae and Stylodactylidae formedonophyletic groups with strong supports in all three anal-

ses (BP ≥99% in both MP and ML, PP = 1 in BI) (Fig. 1).owever, the included members of Palaemonidae and Hip-olytidae did not form monophyletic groups, respectively.he two species from the family Palaemonidae, Macro-rachium rosenbergii (De Man, 1879) and Periclimenesrevicarpalis (Schenkel, 1902), did not form a clade. Instead,he latter species was closely related to the included speciesrom the Hymenoceridae and Gnathophyllidae with strongupport in all analyses (BP = 96% in MP, 98% in ML and
P = 1 in BI). Lysmata amboinensis (De Man, 1888) (cur-ently in Hippolytidae) clustered with Janicea antiguensisChace, 1972) (Barbouriidae) in all analyses with strong sup-ort (BP ≥98% in both MP and ML, and PP = 1 in BI).
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0).

n contrast however, Saron marmoratus (Olivier, 1811) waslways sister to the Alpheidae clade in both ML and BInalyses (BP = 55% and PP = 1), while in the MP analysis,t clustered with members of the Alpheidae, Palaemonidae,nathophyllidae and Hymenoceridae, but with very weak

upport (BP = 52%).In the present study, two major family clades are recovered.

he first clade, with high support in all analyses (BP = 72%n ML, 93% in MP and PP = 1), included nine caridean fami-ies, viz. Hymenoceridae, Gnathophyllidae, Palaemonidae,lyphocrangonidae, Hippolytidae, Barbouriidae, Crango-idae, Pandalidae and Alpheidae. The relationships amonghe nine families could not be firmly resolved in both

P and ML analyses, but support for all of the internalodes among the nine families was moderate to high (PProm 0.73 to 1.0) in the BI tree (Fig. 1). The Hymeno-
eridae + Palaemonidae + Gnathophyllidae clade (the super-amily Palaemonoidea) was basal to the rest of the sixamilies (PP = 0.97). The second major clade included sevenaridean families (Fig. 1), the Rhynchocinetidae, Oplophori-


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ae, Nematocarcinidae, Alvinocarididae, Campylonotidae,asiphaeidae and Eugonatonotidae, and was only recoveredy the BI analysis, but with strong support (PP = 1). The inter-al node supports within this clade were not strong enough tourther resolve the relationships among constituent families,ut the basal position of the Rhynchocinetidae was stronglyupported (PP = 0.89). The Stylodactylidae and Bathypalae-onellidae (with only one species each) were also basally

laced in the tree in all analyses.

. Discussion

.1. Superfamilies

The high support of deeper nodes compared to previ-us studies on the molecular phylogeny of carideans (e.g.itsuhashi et al., 2007; Bracken et al., 2009, 2010), provides

urther support to the utility of the nuclear protein-codingenes in resolving the higher systematics of decapods, aslready discussed by Tsang et al. (2008, in press). The presentesults allow us to examine the systematic status of somef the superfamilies in the non-phylogenetic Chace-Holthuischeme (De Grave et al., 2009) as well as the alterna-ive arrangements proposed by Christoffersen (1990), evenhough our dataset is perhaps too limited in scope to drawnal conclusions.Our molecular analysis supports the monophyly of the

uperfamily Palaemonoidea as defined by De Grave et al.2009), but clearly rejects the definition of the Palaemonoidearoposed by Christoffersen (1990). Christoffersen (1990)ncluded two families in his concept of Palaemonoidea, thealaemonidae and Rhynchocinetidae, with the superfamilyharacterized by the presence of a distolateral tooth on theasal segment of the first antennae. The discrepancy betweenhe number of included families in De Grave et al. (2009) andhristoffersen (1990), stems from the fact that Christoffersen

1990) likely followed Holthuis (1955) in recognizing fourubfamilies within the Palaemonidae: Pontoniinae (includ-ng the genus Anchistioides Paul’son, 1875), Palaemoninae,uryrhynchinae, Typhlocaridinae, with some of these subse-uently elevated to family level by Chace (1992) and Bruce1993). Curiously though Christoffersen (1990) does notention Gnathophyllidae, already recognized as a family

y Holthuis (1955). Our results unambiguously reject thealaemonoidea concept of Christoffersen (1990), as the fourhynchocinetids included in the study do not form a clade withhe palaemonoids. According to De Grave et al. (2009), theuperfamily Palaemonoidea contains eight families, Anchis-ioididae, Desmocarididae, Euryrhynchidae, Kakaducaridi-ae, Typhlocarididae, Gnathophyllidae, Hymenoceridae andalaemonidae. Page et al. (2008) provided genetic evi-
ence that the Australian members of the Kakaducarididaegenera Kakaducaris, Leptopalaemon) are close to Macro-rachium, and it thus seems likely that this family will soone synonymized, leaving only seven families. Only three of
st1n

iger 250 (2011) 270–279 275

hese families were included in the present study, and theonophyletic status of the Palaemonoidea and the generic

omposition of its constituent families will only be fullyesolved once all families are examined. Nevertheless in theresent study members from the Gnathophyllidae, Hymeno-eridae and Palaemonidae are always grouped together, withhe former two families more closely related. The affinity ofnathophyllidae and Hymenoceridae is also evident in therevious molecular analyses of Mitsuhashi et al. (2007) andracken et al. (2009), being consistent with the traditionalorphological viewpoint. These two families were treated as

single family Gnathophyllidae before Chace (1992), whoharacterized the Gnathophyllidae as having the antepenulti-ate segment of the third maxilliped at least partially fusedith and not much wider than the next proximal segment,hile in the Hymenoceridae this segment is clearly articu-

ated with and much wider than the next proximal segment.In contrast to the apparent monophyly of the Palae-onoidea, the current analyses reject all of the other

uperfamily groupings in the Chace-Holthuis classificationDe Grave et al., 2009) and the alternative scheme ofhristoffersen (1990), at least those that could be examinediven current taxon coverage. This comprises the superfami-ies Nematocarcinoidea (considered to consist of 4 families,

included in the present analysis), Alpheoidea (4 families, included), Campylonotoidea (2 families, both included)nd Crangonoidea (2 families, both included). The com-osition of two superfamilies could not be investigated, asnly one family of each was included in the present anal-sis, Pandaloidea (2 families) and Bresilioidea (5 families).he remaining superfamilies (Oplophoroidea, Atyoidea, Sty-

odactyloidea, Pasiphaeoidea) only comprise one family, allf which were included.Two major caridean clades are recovered in the current

nalysis. The first clade consisting of Alpheidae, Hip-olytidae, Crangonidae, Glyphocrangonidae, Barbouriidae,andalidae, Hymenoceridae, Gnathophyllidae and Palae-onidae is strongly supported. According to De Grave et al.

2009), these nine families belong to four superfamilies, thelpheoidea (Alpheidae, Hippolytidae, Barbouriidae), Cran-onoidea (Crangonidae, Glyphocrangonidae), PandaloideaPandalidae) and Palaemonoidea (Hymenoceridae, Gnatho-hyllidae, Palaemonidae). Our tree does not supportuperfamily status of the Alpheoidea sensu De Grave et al.2009), in which the first pair of pereopods is distinctlyhelate (Chace, 1992). In agreement with Bracken et al.2009), the Hippolytidae is a polyphyletic group in the cur-ent analysis. The genus Saron Thallwitz, 1891 shows a closeelationship with members from the Alpheidae as perhapsxpected (the Alpheoidea), but the genus Lysmata Risso,816 clusters with the barbouriids, crangonids and pandalids.he Crangonidae and Glyphocrangonidae belong to the
uperfamily Crangonoidea (De Grave et al., 2009), in whichhe first pair of pereopods is subchelate or prehensile (Chace,992). In the analysis of Bracken et al. (2009), the Crango-idae and Glyphocrangonidae (superfamily Crangonoidea)


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orm a clade with the Processidae (superfamily Proces-oidea) and Thalassocarididae (superfamily Pandaloidea)ith weak to moderate nodal support. In the present study,

he Processidae and Thalassocarididae were not included,ut Glyphocrangonidae is sister to a clade containing Cran-onidae, Pandalidae, Barbouriidae and a hippolytid, L.mboinensis. As a result, the monophyly of the superfamilyrangonoidea (sensu De Grave et al., 2009) is not sup-orted by the present study. In the scheme of Christoffersen1987, 1990), the genus Lysmata is placed in the familyysmatidae, in turn in the superfamily Crangonoidea togetherith the Barbouriidae, Glyphocrangonidae, Crangonidae,erguiidae and Processidae. Although the Lysmatidae, Bar-

ouriidae and Crangonidae are grouped together in our tree,he Glyphocrangonidae is not included in this clade, so thathe monophyly of the Crangonoidea (sensu Christoffersen,987, 1990) is equally not supported. However, the closevolutionary relationship (characterized by the multiarticu-ated carpus, merus and ischium on the second pereopod inhe post-larval stage) among the Alpheoidea, Crangonoideand Pandaloidea suggested by Christoffersen (1987, 1990) isupported by the present molecular analysis.

The second major clade supported only by BI analysis,et with very strong support, includes the families Rhyn-hocinetidae, Oplophoridae, Nematocarcinidae, Alvinocari-idae, Campylonotidae, Pasiphaeidae and Eugonatonotidae.ccording to Bracken et al. (2009), these six families

Campylonotidae is not included in their study) do notorm a clade, and they are scattered throughout their tree.n the synoptic classification of De Grave et al. (2009),he above seven families are listed in five superfamilies,plophoroidea (Oplophoridae), Bresilioidea (Alvinocari-idae), Pasiphaeoidea (Pasiphaeidae), NematocarcinoideaNematocarcinidae) and Campylonotoidea (Campylonoti-ae, Eugonatonotidae). The superfamily Nematocarcinoideas characterized by having strap-like epipods (mastigob-anchs) on at least three anterior pairs of pereopods and theubtruncated molar process of the mandibles with a trans-ersely ridged grinding surface (Chace, 1992). According toe Grave et al. (2009), the superfamily Nematocarcinoideaould include the Nematocarcinidae, Rhynchocinetidae andugonatonotidae. However, neither Bracken et al. (2009)or the present study supports the monophyly of this super-amily. Instead, in our tree, the Rhynchocinetidae is athe basal position to the group making up the remainingix families in this clade. In the scheme of Christoffersen1990), the Nematocarcinidae and Eugonatonotidae eachave their own superfamily, Nematocarcinoidea and Eug-natonotoidea, respectively, and the Rhynchocinetidae islaced in the Palaemonoidea. As already discussed the cur-ent results do not support the inclusion of Rhynchocinetidaen Palaemonoidea. Perhaps surprisingly, the superfamily
ampylonotoidea (Bathypalaemonellidae and Campylonoti-ae) (De Grave et al., 2009) is not supported in the currentnalysis as the Bathypalaemonellidae is placed at a basalosition in our tree. Chace (1992) erected the Bathypalae-
iCpt

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onellidae as a new family (although the name is nowormally attributed to de Saint Laurent, 1985), which heelieved to be closely related to the Campylonotidae. How-ver, our molecular data do not support this relationship. Inontrast to De Grave et al. (2009), Christoffersen (1990)laced the Stylodactylidae (including Bathypalaemonetesleva, 2001) and Campylonotidae in the superfamily Stylo-actyloidea. This alternative superfamily grouping is equallyot supported by the current molecular data.

All in all, the present study rejects most of the superfamil-al groupings as currently accepted in the Chace-Holthuischeme (De Grave et al., 2009) or the alternative classi-cation of Christoffersen (1990), but we do recognize the

imited scope of our dataset. Further evidence that the cur-ently accepted superfamily level classification in Carideaeeds further scrutiny is presented by Chan et al. (2010) inheir study of Oplophoridae based on 16S and 18S rRNAata. Their results not only clearly demonstrate that theplophoridae are polyphyletic and that Acanthephyridaeate, 1888 had to be resurrected to include several generareviously placed in the Oplophoridae, but that the resultingwo families are not closely related and thus the superfamilyplophoroidea should be abandoned. This could not be cor-

oborated in the present study, as only one representative ofplophoridae was included.On the basis of the available evidence presented here, as

ell as the results from Bracken et al. (2009) and Chan et al.2010), it is increasingly clear that the current superfamilylassification of Caridea is not a natural one. Equally thelternative proposal by Christoffersen (1990) is not fully sup-orted, although some elements of that scheme do appear toe better supported than previously assumed. While it maye premature to call for abandoning the current superfamilycheme until more evidence has accumulated, it is clear thatny discussion at higher taxonomic levels should, as a mini-um, include family-level terminal taxa (although caution is

dvised for those which appear to be poly- or paraphyletic).Besides further molecular systematic studies with wider

axon coverage, new sets of morphological characters needo be constructed at both the superfamily and family lev-ls. As outlined by Fransen and De Grave (2009), surveys oforphological characters across all (and within) the caridean

amilies are urgently needed. Prime examples of such char-cters are foregut ossicles and larval development. Foregutssicles have been previously used to classify the BrachyuraDevi et al., 1987; Babu et al., 1989), with work now extendedo the Anomura. Within Caridea very little is known aboutoregut ossicles, which are generally treated as absent, evenhough Felgenhauer and Abele (1983) demonstrate their exis-ence in several families. Equally, larval characters have alsoeen used in the classification of Brachyura for decades (Rice,980, 1988), and numerous examples abound of their utility
n classification. However, the study of larval development inaridea has not sufficiently progressed since Gurney (1942)rovided an overview, but their usefulness is underscored byhe continued recognition of Anchistioidae, primarily based


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n larval evidence. The molecular phylogenetic study ofitsuhashi et al. (2007) confirmed that larval characters are

seful in revealing the relationships among Anchistiodidae,nathophyllidae, Hymenoceridae, Palaemoninae and Pon-

oniinae. It should also be noted that the current analysisupports the grouping of Alpheoidea, Crangonoidea and Pan-aloidea, in agreement with Christoffersen (1987, 1990) whonited the three superfamilies based only on a larval character,.e. multiarticulated carpus, merus and ischium on the sec-nd pereopod in the post-larval stage. Recently, based on themmense diversity in larval morphological characters foundn the Hippolytidae, Terossi et al. (2010) suggested that thisamily is polyphyletic, further highlighting the potential ofncluding larval characters in phylogenetic studies.

.2. Families

Although our molecular data fail to support most of theuperfamilial groupings based on morphological features,ost of the families examined in the present study are shown

o be monophyletic, at least based on our limited taxon cover-ge. In contrast, Hippolytidae and Palaemonidae are shown toe polyphyletic, as S. marmoratus and L. amboinensis (Hip-olytidae) do not form a clade, while the two palaemonids M.osenbergii and P. brevicarpalis also do not cluster together.he monophyly of the families Hippolytidae and Palae-onidae was equally not supported by Bracken et al. (2009).hristoffersen (1987, 1990) already drew attention to the sus-ected non-monophyly of Hippolytidae and erected severalew families, one of which is currently accepted (Barbouri-dae). Further studies focusing on the systematic relationshipsithin the Hippolytidae sensu lato are clearly desirable.The non-monophyletic status of the Palaemonidae as

hown by Bracken et al. (2010) and the present analysisargely centers around the family status of Gnathophylli-ae and Hymenoceridae. Mitsuhashi et al. (2007) providedmple genetic evidence of a close relationship between thosewo families and Pontoniinae. Should the systematic rela-ionship between these three taxa be satisfactorily resolved,t appears likely that all constituent genera will be united intone (sub)family. In such an event, the apparent paraphyly ofhe Palaemonidae in the current analysis will resolve itselfaturally.

.3. Basal groups

Based on their primitive foregut structures, the Atyidae,tylodactylidae, Nematocarcinidae and Rhynchocinetidaell have been considered as basal lineages within the CarideaFelgenhauer and Abele, 1983, 1985, 1989), even thoughhe evidence appears limited due to poor taxon coverage.
hompson (1967) also considers the Pasiphaeidae andtylodactylidae to be basal lineages, although he equallymphasizes some of their derived features. Chace (1992)onsidered the Pasiphaeidae and Oplophoridae as basal
iGCC

iger 250 (2011) 270–279 277

arideans because of their well developed exopods and prim-tive mandible (incisor and molar joined, well developedalp), although some included genera may show charactereversal, as for instance Pasiphaea Savigny, 1816 does notave a mandibular palp. Christoffersen (1990) considersis redefined superfamily Atyoidea as a basal group, whichomprises morphologically and ecologically very diverseamilies, such as Oplophoridae, Atyidae, Agostocarididae,lvinocarididae and others.Interestingly, two recent molecular studies (Bracken et al.,

009; Chan et al., 2010) as well as the present study rejecthe basal status of the Pasiphaeidae and Oplophoridae as bothere found to be nested within a large caridean clade. In

ontrast, Bracken et al. (2009) consider the families Sty-odactylidae, Rhynchocinetidae and Disciadidae as basalineages. While the Disciadidae is not included in the presentnalysis, the current results suggest that the Stylodactylidaend Bathypalaemonellidae are basal or near-basal carideans,ut not the Rhynchocinetidae. Thus of all the families thatave been identified as potentially basal lineages, the Stylo-actylidae has been repeatedly suggested by both molecularnd morphological data. Morphological features supporting

putative basal status of Stylodactylidae are a well devel-ped rostrum, fused incisor and molar on the mandible, aear complete branchial formula and long, slender unspe-ialized chelipeds, although no mastigobranchs are presentmastigobranchs are considered as a primitive character byhace, 1992). The other two families which have been impli-ated as basal lineages, Disciadidae (see Bracken et al.,009) and Bathypalaemonellidae (present study), in molec-lar phylogenies have not been suggested previously basedn morphology. In the absence of a thorough morphologicalnalysis it is impossible to further comment on the putativeasal status of these families. Clearly, such an analysis needso be conducted with some urgency to refute or corroboratehe putative basal status of these families, including a studyf the foregut ossicles (Bracken et al., 2009).

In view of the limited dataset herein presented, it woulde imprudent to draw any firm conclusion and proposebandoning the currently accepted superfamily classifica-ion of Caridea. Although our results clearly demonstratehe artificial nature of the current classification, furtherntegrated studies are needed before such a radical departurean be advocated.

cknowledgements

We sincerely thank Dr. J. Antonio Baeza (Smithsonianarine Station at Fort Pierce) for providing Betaeus longi-

actylus, and Dr. Gary C. Poore (Museum Victoria, Australia)or providing Campylonotus rathbunae. The work described
n this paper was supported by grants from the Researchrants Council of the Hong Kong SAR, China (project no.UHK4419/04M) to KHC, and from the National Scienceouncil, Taiwan, R.O.C. and Academia Sinica to TYC.


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