Abstract

Introduction

The superfamily Portunoidea Rafinesque, 1815 (455 spp.; De Grave et al., 2009) is a diverse clade of marine crabs that includes commercially important species, significant invasives (Brockerhoff & McLay, 2011) and several ecologically divergent lineages that radiated across tropical, temperate and deep-ocean habitats (e.g., Figs. 1 and ​and2).2). Collectively referred to as “swimming crabs,” members of this clade are known for being aggressive opportunistic omnivores that are agile and well adapted to swimming (Hartnoll, 1971; Hazlett, 1971; Spiridonov, Neretina & Schepetov, 2014; Williams, 1981). Morphologically, portunoid crabs are characterized by having a broad, compressed, laterally streamlined carapace and paddle-shaped posterior “natatory” legs (Hartnoll, 1971). Yet this clade also includes several atypical lineages that are morphologically and ecologically divergent. Among these, members of the tropical Indo-Pacific subfamily Caphyrinae Paulson, 1875 (28 spp.) have evolved symbiotic relationships with algae, anemones, echinoderms, and soft corals (Caulier et al., 2013; Hay et al., 1989; Spiridonov, 1999; Stephenson & Rees, 1968). Relative to most portunoids, members of this group are smaller, less streamlined and exhibit highly modified “natatory” legs adapted for grasping onto or burying beneath their hosts (Figs. 3A–3D, ​,3I3I and ​and4B4B–4F). Additional adaptations to symbiosis found in these crabs include cryptic coloration (Ayotte, 2005), attraction to host chemical defense compounds (Caulier et al., 2013; Hay et al., 1989), consumption of host tissue (Caulier et al., 2014; Hay et al., 1989; Steudler, Schmitz & Ciereszko, 1977), and social monogamy (Caulier et al., 2012; for significance see Baeza & Thiel, 2007). Despite its novelty among portunoid crabs, the nature of symbiosis in Caphyrinae remains poorly studied and underreported (Baeza, 2015; Castro, 2015). Unlike Caphyrinae, most well-studied symbiotic crustaceans fall within clades that are species-rich and dominated by or exclusively composed of symbiotic taxa (Baeza, 2015). This has led some to hypothesize that the emergence of symbiosis in crustaceans promotes large evolutionary radiations (Baeza, 2015). However, this hypothesis remains to be tested, requiring phylogenetic analyses of multiple clades with symbiotic and free-living lineages.

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Figure 1

Representatives of various Portunoidea taxa included in this study.

(A) Brusinia profunda (USNM 277519; New Caledonia; preserved color); (B) Coelocarcinus foliatus (UF 40176; Guam); (C) Carupa tenuipes (UF 39918; Palau); (D) Libystes (UF 23926; Moorea Is.); (E) Lupocyclus cf. philippinensis (UF 41639; Luzon Is.); (F) Podophthalmus vigil (UF 24543; Moorea Is.); (G) Portunus (Cycloachelous) granulatus (UF 40021; Guam); (H) Portunus (Portunus) sanguinolentus (UF 24538; Moorea Is.). Photographs (A–C, G) by Nathaniel Evans; photographs (D–F, H) by Gustav Paulay.

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Figure 2

Representative non-symbiotic Thalamitinae species.

(A) Cronius ruber (UF 35672; Florida); (B) Thalamitoides spinigera (UF 36697; Farasan Banks); (C) Gonioinfradens paucidentatus (UF 37141; Red Sea); (D) Goniosupradens acutifrons (UF 7114; Okinawa); (E) Charybdis orientalis (UF 41638; Luzon Is.); (F) Thalamonyx gracilipes (UF 42972; Mindoro Is.); (G) Thalamita admete (UF 40031; Guam); (H) Thalamita chaptalii (UF 39917; Palau); (I) Thranita coeruleipes, comb. nov. (UF 40078; Guam); (J) Thalamita cf. philippinensis (UF 43302; Mindoro Is.). Photographs (A, G–I) by Nathaniel Evans; photographs (B–F, J) by Gustav Paulay.

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Figure 3

Representative putative symbiotic Thalamitinae species.

(A) Caphyra loevis (UF 39060); (B) Lissocarcinus cf. laevis (UF 39136; New Caledonia); (C) Lissocarcinus holothuricola (UF 30182; Marquesas); (D) Lissocarcinus orbicularis (UF 23972; Moorea); (E) Zygita murinae, comb. nov. (UF 36721; Farasan Banks); (F) Trierarchus woodmasoni, comb. nov. (UF 40079; Guam); (G) Trierarchus cf. cooperi sp. A, comb. nov. (UF 16023; Moorea Is.); (H) Trierarchus cf. cooperi sp. B, comb. nov. (UF 40100; Guam); (I) Trierarchus rotundifrons, comb. nov. (UF 40067; Guam); (J) Trierarchus squamosus, comb. nov. (USNM 102963; Bikini Atoll; preserved specimen, grayscale, left frontal margin damaged). Photographs (A–C, F, H–J) by Nathaniel Evans; photographs (D, E, G) by Gustav Paulay.

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Figure 4

Representative portunid natatory leg morphology and divergent, symbiotic caphyrine forms.

Typical portunid P5 morphology and terminology: (A) Thranita cf. rubridens (UF 43834). Typical symbiotic caphyrine P5 morphology: (B) Caphyra cf. fulva (UF 11748; host xeniid soft coral); (C) Caphyra loevis (UF 38881; host xeniid soft coral); (D) Lissocarcinus holothuricola (UF 30302; host holothurians); (E) Lissocarcinus laevis (UF 41571; host cerianthids and actinodendronid anemones); (F) Caphyra rotundifrons (=Trierachus rotundifrons, comb. nov., UF 40067A; host Chlorodesmis algae).

Recently, Evans & McKeon (2016) provided compelling evidence that some species of the portunid genus Thalamita also exhibit symbiotic relationships (with soft coral). It has long been suggested that Caphyrinae shares a close, even derived relationship with Thalamita and other taxa in the diverse portunid subfamily Thalamitinae Paulson, 1875 (162 spp.; e.g., see Stephenson & Campbell, 1960). Thalamitinae radiated across the same Indo-Pacific habitats where Caphyrinae and their reef-associated host taxa are found. Consequently, Caphyrinae and Thalamitinae provide an interesting group to investigate the evolution of symbiosis in decapod crustaceans. Unfortunately, like much of Portunoidea, little phylogenetic work has been done on Thalamitinae or Caphyrinae.

The original aim of this study was to investigate the molecular phylogenetic relationships within and between Thalamitinae and Caphyrinae, providing important context for understanding the evolution of symbiosis within portunids. However, preliminary analyses revealed that inclusion of the non-symbiotic Caphyrinae genus Coelocarcinus required analyses be expanded to include the entire superfamily Portunoidea. Consequently, this study compiles and augments the best available molecular data for all of Portunoidea (as of January 2017). Given this broader scope, here I also reevaluate family classifications within the superfamily Portunoidea and subfamily classifications within Portunidae. Finally, for Thalamitinae and Caphyrinae, where taxon sampling is now the densest of any portunoid clade, generic level classifications are also reevaluated and new genera and morphological diagnoses proposed where appropriate.

A brief review of portunoid systematics

Considerable systematic work was carried out on Portunoidea during the 19th and 20th centuries, often in conjunction with work on the morphologically similar Cancroidea (reviewed in Davie, Guinot & Ng, 2015a; Karasawa, Schweitzer & Feldmann, 2008; Schubart & Reuschel, 2009). Toward the end of this period W. Stephenson revised and largely stabilized portunoid classification (Stephenson, 1972). However, morpho-taxonomic work has continued for the group, sometimes revealing surprisingly unique new lineages (e.g., Atoportunus Ng & Takeda, 2003). In recent years genetic data has increasingly been combined with morphology to resolve species complexes (Keenan, Davie & Mann, 1998; Lai, Ng & Davie, 2010; Robles et al., 2007), but neither molecular nor morphological phylogenetic analyses have been widely applied to the group.

To date, only three studies have conducted higher-level molecular phylogenetic analyses of Portunoidea, using 16S rRNA or combinations of CO1, H3, 16S and 28S rRNA for up to 43 portunoid taxa (Mantelatto et al., 2009; Schubart & Reuschel, 2009; Spiridonov, Neretina & Schepetov, 2014). Of these studies, the latter two are the only to include a caphyrine species (Lissocarcinus orbicularis), which was recovered falling sister to, or derived within Thalamitinae (comprised of one and six thalamitine taxa, respectively). Though these studies have significantly improved our understanding of portunoid systematics, synthesis of this work is complicated by a lack of overlap in both taxa and molecular data sampled.

In addition to molecular work, only the generic level morphological cladistic analyses of Portunoidea by Karasawa, Schweitzer & Feldmann (2008) have significantly contributed to our understanding of higher-level phylogenetic relationships within the clade. None of this work analyzed more than approximately 40 of the 455 extant portunoid taxa. Nevertheless, beginning with Ng, Guinot & Davie (2008) four different schemes have been proposed for the familial and subfamilial classification of Portunoidea (Fig. 5). While additional revisions will likely be needed, here I propose a new, more conservative classification scheme for extant portunoids based on more comprehensive molecular phylogenetic analyses of the superfamily.

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Figure 5

Summary of major recent changes to Portunoidea familial and subfamilial classification and a new proposed scheme.

Dashed and arrowed lines trace recognized taxa between studies. Solid arrowed lines highlight notable changes, with numbers indicating the movement of specific genera: 1, Catoptrus and Libystes; 2, Echinolatus and Nectocarcinus; 3, Bathynectes, Macropipus, Necora, Parathranites and Raymanninus; 4, Coelocarcinus; 5, Benthochchascon and Ovalipes; 6, Brusinia; 7, Benthochchascon; 8, Ovalipes; 9, Cronius; 10, Caphyra and Lissocarcinus. Single asterisk*, corresponding study considers subfamily composition and status uncertain given morphological or phylogenetic results, or lack there of; double asterisks**, change made following Davie, Guinot & Ng (2015b); †, extinct family. Figure modeled after Fig. 8 in Spiridonov, Neretina & Schepetov (2014).

Materials and Methods

Morphological terminology

Descriptive work on portunoid crabs has not always used consistent morphological terminology. Morphological terms used here are illustrated in Figs. 4, ​,66 and ​and7,7, and mostly conform to those used by Apel & Spiridonov (1998), Crosnier (1962), Stephenson & Hudson (1957), and Wee & Ng (1995). As in these works, here the demarcation of teeth (or lobes) along the frontal margin of the carapace does not include the inner supraorbital margins, but discussion (or counts) of the teeth along the anterolateral margins does include the exorbital tooth (as tooth number one; Figs. 6A and ​and6B).6B). Standard pereiopod abbreviations are also followed: P1, cheliped; P2–P4, ambulatory legs; P5, natatory (swimming) leg (Fig. 4). Likewise, G1 and G2 denote male first and second gonopods, respectively (Fig. 7).

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Figure 6

Morphological terminology for the carapace, antenna, and cheliped.

Carapace dorsal surface: (A) Cronius edwardsii (USNM 1254607); (B) Thalamita gatavakensis (UF 24660). (C) Stylized ventral surface of antenna and orbit. (D–F) Stylized thalamitine left cheliped: (D), outer surface; (E) dorsal surface; (F) inner surface. AT, positionally homologous portunid anterolateral tooth number.

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Figure 7

Morphology and terminology for stylized left male first gonopod (G1) from representative taxa.

(A) Thalamita granosimana (Thalamita sensu stricto clade 1; composite redrawn from Stephenson & Rees, 1967a, Fig. 27A and 27B); (B) Thalamita spinifera (Thalamita sensu lato “clade” II; redrawn from Crosnier, 1962, Fig. 214); (C) Thranita crenata (“Thalamita” sensu lato clade III; composite redrawn from Crosnier, 1962, Figs. 232 and 233); (D) Zygita murinae (composite redrawn from Spiridonov & Neumann, 2008, Figs. 6 and 7); (E, F) Trierarchus woodmasoni (redrawn from Crosnier, 1975a, Figs. 8J and 8I, respectively); (G) Thalamonyx gracilipes (redrawn from Stephenson & Rees, 1967b, Fig. 2H). (A–E) depict the abdominal (ventral) G1 surface, (F, G) depict distal portion of the sternal (dorsal) G1 surface.

Finally, here I propose new terminology in the form of two numbering schemes to respectively characterize carapace anterolateral teeth and cheliped carinae in Portunidae (Figs. 6A, ​,6B,6B, ​,6D6D and ​and6F).6F). In both cases, indicated structures clearly share positional homology across Portunidae (likely Portunoidea) and adoption of the proposed schemes should bring greater clarity to taxonomic descriptive work on portunids. For example, anterolateral teeth counts are often diagnostic for Thalamita where five teeth are standard, but the fourth is often absent and the first sometimes exhibits a subsidiary tooth. Confusion can arise when diagnoses of Thalamita discuss the form or presence of the “fourth tooth” in disparate species exhibiting a total of four, five or six anterolateral teeth (e.g., compare Figs. 8G–8J). Under the proposed scheme such confusion is avoided; the diagnostic “fourth” anterolateral tooth typically refers to portunid tooth AT7, and is better discussed as such in each of these cases. Likewise a simple count of spines on the upper surface of the cheliped can lead to confusing descriptions when standard spines are absent from different cheliped carinae for different taxa. Although a determination of positional homology for anterolateral teeth may be difficult for select taxa (e.g., Figs. 8E and ​and9E),9E), “transitional” forms may significantly help. For example, while exhibiting nine anterolateral teeth is clearly plesiomorphic within Portunidae (Spiridonov, Neretina & Schepetov, 2014), in Cronius these teeth alternate in size such that each of its five large teeth are separated by a reduced (or subequal) tooth (Fig. 8A). This suggests that the five anterolateral teeth typical to Thalamita likely correspond (in order) to teeth numbers one, three, five, seven, and nine in portunine taxa (compare Figs. 6A and ​and6B).6B). This is supported by additional intermediate forms present in other Thalamitinae taxa (Figs. 8B–8D). Last, it is worth noting that some positionally homologous anterolateral teeth are likely homoplastic, reappearing within derived clades through reversal or parallelism (e.g., AT2* in Fig. 8I).

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Figure 8

Representative partial carapace outlines of Thalamitinae genera, Part 1.

(A) Cronius edwardsii (USNM 1254607); (B) Gonioinfradens paucidentatus (UF 1411-A); (C) Goniosupradens obtusifrons (UF 16599); (D) Charybdis orientalis (USNM 112062); (E) Thalamitoides quadridens (UF 1962); (F) Thalamonyx gracilipes (USNM 127103-A); (G) Thalamita admete (UF 26950-A); (H) Thalamita parvidens (USNM 32855-A; Holotype); (I) Thalamita spinifera (UF 33379); (J) Thalamita bouvieri (UF 41652); (K) Thalamita sima (USNM 1254584-A); (L) Thalamita malaccensis (USNM 274290-A). AT, positionally homologous portunid anterolateral tooth number (see Figs. 6A and ​and6B6B and text). Asterisks indicate a homoplastic anterolateral tooth that arose through parallelism or reversal (see text).

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Figure 9

Representative partial carapace outlines of Thalamitinae genera, Part 2.

(A) Thranita crenata, comb. nov. (UF 39965); (B) Lissocarcinus laevis (UF 41571); (C) Zygita longifrons, comb. nov. (UF 199); (D) Caphyra loevis (UF 38881); (E) Caphyra cf. fulva (UF 38855; epibranchial ridge depicted); (F) Trierarchus rotundifrons, comb. nov. (UF 40143-A); (G) Trierarchus woodmasoni, comb. nov. (UF 40079); (H) Trierarchus cooperi sp. B, comb. nov. (USNM 41125-A); (I) Trierarchus squamosus, comb. nov. (USNM 102963); (J) Trierarchus acanthophallus, comb. nov. (stylized outline redrawn from Chen & Yang, 2008). AT, positionally homologous portunid anterolateral tooth number (see Figs. 6A and ​and6B6B and text).

Results and Discussion

Phylogenetic analyses of up to four molecular markers (16S rRNA, CO1, 28S rRNA, and H3) were carried out on 168 portunoid OTUs, 76 for the first time. Resulting topologies and support values are summarized in Figs. 10–13 and Figs. S1–S6. With few exceptions phylogenetic analyses of the three concatenated data sets recovered consistent topologies that displayed significant support for most of the same clades (Figs. 10–12; Fig. S1). However, analyses of the 174 OTU data set, which had the greatest proportion of missing data, often recovered lower support for each clade (Fig. S1). Clades typically exhibited the greatest support in analyses of the 138 OTU data set, which contained the least amount of missing data (Figs. 10B, 11B and 12B). Nevertheless some topological incongruence was recovered between ML and BI analyses of this 138 OTU concatenated data set (compare nodal asterisks, Figs. 11B and 13B). This conflict was associated with deeper nodes in Portunidae and involved the relative placement of a well-supported “Achelous” sensu lato clade (discussed below). This conflict may be an artifact of the low taxon sampling available for non-thalamitine portunids, a general shortcoming in all analyses. Single marker ML analyses generally recovered poorly resolved topologies, but displayed no significant well-supported conflict with concatenated results (Figs. S2–S5). The following sections present a clade-by-clade discussion of the results for the ML and BI analyses of the 163 and 138 OTU concatenated data sets. The ML topologies for these two data sets are presented together in Figs. 10–12. In text, bootstrap support values (bs) and Bayesian posterior probabilities (pp) are reported together with those for the 163 OTU topology appearing first, followed by those for the 138 OTU topology (e.g., Fig. 10; bs 70%, 100%, pp 0.95, 1.0). Results of the other analyses, including those for the 16S-Brusinia data set, are discussed where relevant.

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Figure 10

Maximum likelihood (ML) phylograms of Portunoidea based on analyses of 163 and 138 OTUs and a 3,313 bp alignment of 16S rRNA, CO1, 28S rRNA, and H3 sequence data, Part 1 (of 3).

(A) ML phylogram based on analyses of 163 OTUs, each with at least 16S rRNA data; (B) ML phylogram based on analyses of 138 OTUs, each with at least 16S rRNA and CO1 data. Support values appear below relevant branches with ML bootstrap values ≥50% (based on 500 replicates) appearing first followed by BI posterior probabilities ≥0.95.

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Figure 11

Maximum likelihood (ML) phylograms of Portunoidea based on analyses of 163 and 138 OTUs and a 3,313 bp alignment of 16S rRNA, CO1, 28S rRNA, and H3 sequence data, Part 2 (of 3).

(A) ML phylogram based on analyses of 163 OTUs, each with at least 16S rRNA data; (B) ML phylogram based on analyses of 138 OTUs, each with at least 16S rRNA and CO1 data. Support values appear below relevant branches with ML bootstrap values ≥50% (based on 500 replicates) appearing first followed by BI posterior probabilities ≥0.95. Asterisk* denotes nodes that topologically conflict with corresponding BI topology (see text and Fig. 13B).

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Figure 12

Maximum likelihood (ML) phylograms of Portunoidea based on analyses of 163 and 138 OTUs and a 3,313 bp alignment of 16S rRNA, CO1, 28S rRNA, and H3 sequence data, Part 3 (of 3).

(A) ML phylogram based on analyses of 163 OTUs, each with at least 16S rRNA data; (B) ML phylogram based on analyses of 138 OTUs, each with at least 16S rRNA and CO1 data. Support values appear below relevant branches with ML bootstrap values ≥50% (based on 500 replicates) appearing first followed by BI posterior probabilities ≥0.95.

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Figure 13

Subsections of ML and BI topologies for Portunoidea based on analyses of 174 and 138 OTUs and a 3,313 bp alignment of 16S rRNA, CO1, 28S rRNA, and H3 sequence data.

(A) A subsection of the 174 OTU ML phylogram representing the Portunus subgenera Cycloachelous, Monomia, and Xiphonectes. Support values appear below relevant branches with ML bootstrap values ≥50% (based on 500 replicates) appearing first followed by BI posterior probabilities ≥0.95. (B) Relevant subsection of the 138 OTU BI majority consensus tree exhibiting topological conflict with the ML phylogram generated from the same concatenated data set (see text and Fig. 11). BI posterior probabilities (≥0.95) appear below each relevant node.

Taxonomic Account

Portuniod family-level morphological diagnoses presented here amend those of Davie, Guinot & Ng (2015b), but do not address or impact diagnoses of Portunidae Rafinesque, 1815, or Brusiniidae Števčić (1991). New diagnoses are also presented for the portunid subfamily Thalamitinae and three new, and two revalidated thalamitine genera. Post-revision names are used for “Species included” lists, with junior synonyms in brackets “[ ].”

• Superfamily Portunoidae Rafinesque, 1815

• Family Geryonidae Colosi, 1923

• Geryonidae Colosi, 1923: 249. Type genus Geryon Krøyer, 1837

• Ovalipidae Spiridonov, Neretina & Schepetov (2014: 420). Type genus Ovalipes Rathbun, 1898

Diagnosis: Carapace ovate, hexagonal or subhexagonal, broader than long (sometimes only slightly so), smooth to moderately granular; regions variously expressed; epibranchial ridge of diffuse granules sometimes present, other carapace ridges not developed; frontal margin shorter than posterior margin, typically divided into even number of lobes or teeth (but sometimes three) with median notch present; supraorbital margin with one or two fissures, often indistinct (if two and distinct, central lobe toothed); infraorbital margin not separated from outer orbital lobe by fissure or notch; anterolateral margin with three to five teeth, shorter than posterolateral margin; posterolateral re-entrant not developed. Basal antennal segment free or fixed, longer than broad. Mesial lobe of first maxilliped endopod not well developed. Chelipeds heterochelous (sometimes weakly so) and heterodontous; merus typically without spines; carpus often with an outer spine; manus with dull, knob-like outer proximal spine. Meri of P2–P5 with antero-distal lobes or spines, sometimes reduced. P5 propodi laterally compressed, sometimes ovate; dactyli ovate, styliform, or lanceolate. Pleon with six somites plus telson typically distinguishable in both sexes with somites three to five in males separated by sutures but immovable. G1 long, opening anterolaterally. G2 thin, more or less approximately as long as G1. Diagnosis modified from Geryonidae and Ovalipidae sensu Spiridonov, Neretina & Schepetov (2014) and Davie, Guinot & Ng (2015b).

Genera included: Benthochascon Alcock & Anderson, 1899; Chaceon Manning & Holthuis, 1981; Echinolatus Davie & Crosnier, 2006; Geryon Krøyer, 1837; Nectocarcinus A. Milne-Edwards, 1861; Ovalipes Rathbun, 1898; Raymanninus Ng, 2000; Zariquieyon Manning & Holthuis, 1989.

Remarks: The placement of Echinolatus and Nectocarcinus within this family is tentative, following Davie, Guinot & Ng (2015b), but may be more appropriately judged “genera incertae sedis” considering remarks by Spiridonov, Neretina & Schepetov (2014). Additional morphological and phylogenetic work will be needed to resolve their placement.

• Family Carcinidae MacLeay, 1838

• Carcinidae MacLeay, 1838: 59. Type genus Carcinus Leach, 1814

• Pirimelidae Alcock, 1899: 95. Type genus Pirimela Leach, 1814

• Polybiidae Ortmann, 1893: 66. Type genus Polybius Leach, 1820

• Thiidae Dana, 1852: 1425. Type genus Thia Leach, 1816

Diagnosis: Carapace hexagonal, subhexagonal, pyriform, or subcircular, rarely quasi-quadrate, typically broader than long; frontal margin sometimes entire, typically with two to four lobes or teeth, and shorter than posterior margin; inner supraorbital lobe weakly defined, significantly reduced, or absent; one or two supraorbital fissures sometimes reduced, rarely absent; anterolateral margin typically convex with five (sometimes four) teeth or lobes (count excluding exorbital tooth when small or poorly developed, e.g., as in some Pirimelinae); posterolateral re-entrant sometimes not developed, rarely absent. Basal antennal segment fixed, longer than wide. Well defined mesial lobe on endopod of first maxilliped sometimes present. Chelipeds typically heterochelous and heterodontous, sometimes symmetrical; merus typically without spines; carpus often with an outer spine; manus sometimes with dull, knob-like outer proximal spine; proximal inner surface of manus fixed finger concave. Meri of P2–P5 typically without antero-distal lobes or spines. P5 dactyli ovate (paddle-like), styliform, ensiform, or lanceolate. Sutures between sternites and episternites incomplete or partially incomplete. Pleonal somites three to five in males typically fused sometimes with traces of sutures, rarely all six somites and telson free (in Thiinae). G1 straight to slightly or distinctly curved, sometimes with spinules and soft setae. G2 distinctly shorter than G1. Vulva typically rounded or ovate, sometimes broader than long. Diagnosis modified from Carcinidae, Pirimelidae, Polybiidae, and Thiidae sensu Spiridonov, Neretina & Schepetov (2014) and Davie, Guinot & Ng (2015b), and including Coelocarcinus sensu Ng, 2002.

Genera included: Bathynectes Stimpson, 1871; Carcinus Leach, 1814; Coelocarcinus Edmondson, 1930; Coenophthalmus A. Milne-Edwards, 1873; Liocarcinus Stimpson, 1871; Macropipus Prestandrea, 1833; Nautilocorystes H. Milne-Edwards, 1837; Necora Holthuis, 1987; Parathranites Miers, 1886; Pirimela Leach, 1816; Polybius Leach, 1820; Portumnus Leach 1814; Sirpus Gordon, 1951; Thia Leach, 1816; Xaiva MacLeay, 1838.

• Family Portunidae Rafinesque, 1815

• Subfamily Thalamitinae Paulson, 1875

• Figures 2–4, ​,66–9 and ​and1414

  

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  Figure 14

  Relevant diagnostic morphology of Trierarchus gen. nov. and Zygita gen. nov.

  (A) Dorsal surface right P5, Trierarchus cooperi (UF 23802). (B–E) Zygita longifrons (UF 199): (B) dorsal surface right P5; (C) ventral surface right P5; (D) outer surface right cheliped; (E) right P4, ambulatory leg. Solid arrows, morphology discussed. Asterisks, important diagnostic traits.

• Thalamitinae Paulson, 1875: 69. Type genus Thalamita Latreille, 1829

• Caphyrinae Paulson, 1875: 69. Type genus Caphyra Guérin, 1832

Diagnosis: Carapace subcircular, subhexagonal or subtrapezoidal; slightly to substantially broader than long. Anterolateral margin with two to nine teeth, but typically four to six, and rarely nearly entire (e.g., some Lissocarcinus and Caphyra); if teeth number greater than six, five are typically large, well developed, and correspond to portunid teeth AT1, AT3, AT5, AT7 and AT9; the remaining being small, subsidiary, or rudimentary teeth appearing between the larger teeth (e.g., Figs. 8A–8C); rarely the first anterolateral tooth appears truncate and notched somewhat resembling a poorly developed additional tooth (e.g., Charybdis feriata). Basal antennal segment transversely broadened or lying obliquely, and entering or filling orbital hiatus; antennal peduncle and flagellum completely or nearly completely excluded from orbit (Fig. 6C). Chelipeds (P1) the same length or longer than ambulatory legs (P2–P4), typically bearing spines on the merus, carpus and manus; manus usually bearing one or more spines along both Carina 1 and Carina 2 and a well-developed outer proximal spine (Figs. 6D–6F; notable exceptions include many Caphyra and Lissocarcinus species). P5 typically with paddle-shaped propodi and dactyli, but sometimes otherwise modified (e.g., Figs. 4 and 14A). G1 with subdistal spinules, spines, bristles, or “hairs.” Diagnosis modified from Thalamitinae and Caphyrinae sensu Apel & Spiridonov (1998), Cronius sensu Garth & Stephenson (1966), and Caphyra sensu Apel & Steudel (2001).

Genera included: Caphyra Guérin, 1832; Charybdis De Haan, 1833; Cronius Stimpson, 1860; Gonioinfradens Leene, 1938; Goniosupradens Leene, 1938, status nov.; Lissocarcinus Adams & White, 1849; Thalamita Latreille, 1829; Thalamitoides A. Milne-Edwards, 1869; Thalamonyx A. Milne-Edwards, 1873, status nov.; Thranita, gen. nov.; Trierarchus, gen. nov.; Zygita, gen. nov.

Remarks: With the addition of Caphyra, Cronius and Lissocarcinus, Thalamitinae now includes 190 species (Spiridonov, Neretina & Schepetov, 2014; Spiridonov, 2017) and is the largest portunoid subfamily. Cronius notably expands the diagnosis of the subfamily to include two species with nine anterolateral teeth. However, Cronius clearly exhibits morphology diagnostic of Thalamitinae including exclusion of the antennal flagellum from the orbit by the basal antennal joint, no more than six large anterolateral teeth, and a G1 with subterminal bristles or “hairs” (Garth & Stephenson, 1966; Spiridonov, Neretina & Schepetov, 2014).

• Genus GoniosupradensLeene, 1938, status nov.

• Figures 2D, ​,4A4A and ​and8C8C

Type species: Portunus erythrodactylus Lamark, 1818, subsequent designation by Davie (2002); gender masculine.

Diagnosis: Carapace subhexagonal, slightly broader than long. Frontal margin with six well-developed teeth or lobes of approximately equal width. Anterolateral margin with five large, well-developed, forward-sweeping teeth corresponding to portunid teeth AT1, AT3, AT5, AT7 and AT9 and one or two subsidiary teeth corresponding to teeth AT2 (always present) and AT4 (sometimes present); subsidiary teeth not significantly swept forward but terminating approximately perpendicular to the anterolateral margin; epibranchial tooth (AT9) subequal to and never significantly extending laterally beyond tooth AT7. Posterior margin of carapace forming a curve with the posterolateral margin. Cheliped carinae 3–5 always well developed. Diagnosis modified from Leene (1938) to include G. hawaiensis, comb. nov., after Edmondson (1954).

Species included: Goniosupradens acutifrons (De Man, 1879); Goniosupradens erythrodactylus (Lamarck, 1818) [=Thalamita pulchra Randall, 1840; Thalamita teschoiraei A. Milne-Edwards, 1859]; G. hawaiensis (Edmondson, 1954), comb. nov.; Goniosupradens obtusifrons (Leene, 1937).

Remarks: Historically, G. hawaiensis (=Charybdis hawaiensis) was considered closely related to Ch. orientalis (Edmondson, 1954), but similarities are superficial. Once thought diagnostic of these species, the first “subsidiary” anterolateral tooth (AT2) is more reduced in G. hawaiensis in a manner consistent with other Goniosupradens. Furthermore, G. hawaiensis, like all Goniosupradens, bears an epibranchial, anterolateral tooth (AT9) subequal to, but never significantly extending laterally beyond the preceding tooth (AT7). The opposite condition is present in Ch. orientalis and most Charybdis (compare Figs. 8C and ​and8D8D).

• Genus Thalamonyx A. Milne-Edwards, 1873, status nov.

• Figures 2F, ​,7G7G and ​and8F8F

Type species: Goniosoma danae A. Milne-Edwards, 1869, subsequent designation by Rathbun, 1922; gender masculine.

Diagnosis: Carapace subhexagonal, approaching subcircular; moderately convex dorsally; mature specimens always slightly broader than long. Frontal margin of carapace not much wider than posterior margin and comprised of two lobes separated by a small, distinct notch and extending forward well beyond the inner supraorbital margin; lobes frequently slightly sinuous or concave near the inner margin such that each appears subtly bilobed. Inner supraorbital margin arched and less than one third as wide as frontal lobes. Five, sharp anterolateral teeth (AT1, AT3, AT5, AT7, and AT9); AT1 largest and directed forward; remaining subequal and swept forward forming an oblique, inclined border similar to that in Charybdis. Chelipeds subequal, not robust, and lightly granular all over; posterior border of merus subtly squamous; manus with one spine present along Carina 1, one spine along Carina 2, and a well-developed outer proximal spine; Carina 3–5 granular but increasingly well developed; Carina 6 granular or smooth and poorly developed; Carina 7 sometimes granular and well developed. Posterior border of P5 propodi without spinules. G1 short, stout, curved, broadening slightly toward a obliquely ending tip; subdistal lateral margin bearing stout, mostly paired bristles numbering approximately nine, preceded by additional thinner bristles; subdistal mesial margin with approximately five long, hook-shaped bristles followed by approximately four mostly straight, variously angled bristles. Female genital opening relatively large, located near anterior margin of sternite.

Species included: Thalamonyx danae (A. Milne-Edwards, 1869) [=Thalamita anomala Stephenson & Hudson, 1957]; Th. gracilipes A. Milne-Edwards, 1869.

Remarks: G1 morphology of this genus is diagnostic (Fig. 7G; see also Stephenson & Rees, 1967b, Fig. 2D; Nguyen, 2013, Fig. 15), as is the female genital opening (pers. comm. V. Spiridonov, 2017). Ng, Guinot & Davie (2008, Note 25, p. 158) created some confusion by misidentifying the type species of this genus which is G. danae A. Milne-Edwards, 1869, not Th. danae Stimpson, 1858. When Stephenson & Hudson (1957) designated Thalamonyx a junior synonym of Thalamita, the species Th. danae (A. Milne-Edwards, 1869) became a secondary homonym of Th. danae Stimpson, 1858. Consequently, Th. danae (A. Milne-Edwards, 1869) was given the new specific epithet Th. anomala (Stephenson & Hudson, 1957). In accordance with Article 59.4 of ICZN (1999), Th. danae (A. Milne-Edwards, 1869) is reinstated here as a valid species and Th. anomala (Stephenson & Hudson, 1957) its junior synonym. Though no Th. danae (A. Milne-Edwards, 1869) specimens were examined for this study, its sister status with Th. gracilipes (sampled here) is without question. The synonymization of these species has been discussed, but has never been fully investigated or formally adopted (discussed in Stephenson & Rees, 1967b). Finally, as others have noted, the Thalamonyx specimen illustrated by Crosnier (1962, Fig. 153) is that of an immature male; both its carapace and G1 are not fully developed and should not be used to diagnose adult specimens.

• Genus Thranita, gen. nov.

• Figures 2I, ​,4A,4A, ​,7C7C and ​and9A9A

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Type species: Thalamita crenata Rüppell, 1830, by present designation; gender feminine.

Diagnosis: Carapace subhexagonal, always broader than long, somewhat flattened and never significantly convex; frontal margin with six well-developed, bluntly rounded lobes of approximately even width; anterolateral margin with five (rarely four) well-developed sharp teeth corresponding to portunid teeth AT1, AT3, AT5, AT7, and AT9 (Fig. 9A); exorbital tooth (AT1) always entire; AT7 sometimes reduced or absent (e.g., in Thranita pseudopelsarti). Basal antennal segment always transversely broadened, never laying significantly oblique to orbital hiatus. G1 long, slightly tapering (Fig. 7C), rarely with a laterally recurved tip (e.g., as in Thranita foresti); never stout with a laterally flared tip.

Species included: Thranita cerasma (Wee & Ng, 1995), comb. nov. [=Thalamita cerasma rectifrons Crosnier & Moosa, 2002]; Thranita coeruleipes (Hombron & Jacquinot, 1846), comb. nov.; Thranita crenata (Rüppell, 1830), comb. nov.; Thranita danae (Stimpson, 1858), comb. nov. [=Thalamita stimpsoni A. Milne-Edwards, 1861; Thalamita prymna var. proxima Montgomery, 1931]; Th. foresti (Crosnier, 1962), comb. nov. [=?Thalamita helleri Hoffmann, 1874]; Thranita gurjanovae (Tien, 1969), comb. nov.; Thranita holthuisi (Stephenson, 1975), comb. nov.; Thranita kotoensis (Tien, 1969), comb. nov.; Thranita pelsarti (Montgomery, 1931), comb. nov.; Thranita prymna (Herbst, 1803), comb. nov. [=Thalamita crassimana Dana, 1852; Thalamita pyrmna var. annectans Laurie, 1906]; Thranita pseudopelsarti (Crosnier, 2002), comb. nov.; Thranita rubridens (Apel & Spiridonov, 1998), comb. nov.; Thranita spinicarpa (Wee & Ng, 1995), comb. nov.; Thranita spinimana (Dana, 1852), comb. nov.; Thranita starobogatovi (Tien, 1969), comb. nov.; Thranita tenuipes (Borradaile, 1902), comb. nov.; Thranita williami (Spiridonov, 2017), comb. nov.

Remarks: Sometimes referred to as the “Prymna” group (after Thalamita prymna; Stephenson & Hudson, 1957), members of this clade include nearly all large species of Thalamita sensu lato and have long been recognized as morphologically similar. Though several of these species were not available (or suitable) for molecular analyses (e.g., Th. cerasma, Th. pelsarti, and Th. williami), they have always been considered morphologically most similar to species that were included here (e.g., Wee & Ng, 1995; Spiridonov, 2017). Although there is no striking single synapomorpy for Thranita, all members share a similar shaped carapace with six frontal lobes of approximately uniform shape and width (Fig. 9A) and a relatively long, gradually tapering G1 (Fig. 7C). This combination of characters is not seen in any other Thalamita clade.

Etymology: Thalamita Latreille, 1829 (and its suppressed, objective synonym Thalamites Guérin, 1829, a nomen oblitum; Low, Ng & Evenhuis, 2013) was named after Thalamite, the title given to oarsmen occupying the lowest tier of a trireme (a three-tiered ancient Greek warship). Keeping with this tradition, Thranita originates from Thranite, the title given to oarsmen occupying the upper tier of a trireme. Gender feminine.

• Genus Trierarchus, gen. nov.

• Figures 3F–3J, ​,4F,4F, ​,7E,7E, ​,7F,7F, ​,9F9F–9J and 14A

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Type species: Thalamita woodmasoni Alcock, 1899, by present designation; gender masculine.

Diagnosis: Carapace subhexagonal to subcircular, typically broader than long and somewhat convex; frontal margin flat or rounded and comprised of one to six (typically four) weakly distinguished lobes; four lobed specimens typically with median lobes approximately three times the width of lateral lobes; inner supraorbital margin sometimes nearly absent (e.g. Tr. rotundifrons) but typically subtly rounded and oblique with a breadth never greater than one-third the total breadth of the frontal lobes; anterolateral margin not reduced nor exhibiting a significantly concave epibranchial ridge (e.g., as in some Caphyra; Fig. 9E); anterolateral margin with four well-developed teeth swept forward corresponding to portunid teeth AT1, AT3, AT5 and AT9; a rudimentary tooth AT7 sometimes present (Figs. 9F–9J). Carapace and chelipeds subtly to substantially granular and covered with plumose setae. Chelipeds with posterior surface of merus bearing distinct granular squamiform markings; manus with weakly squamiform markings extending ventrally from Carina 5 to a poorly defined Carina 6. P5 dactyli typically lancelet-shaped, especially in juveniles, but approaching paddle-shaped in larger specimens (Figs. 14A and ​and3F,3F, respectively). G1 curved and swelling slightly toward a club-shaped end with a bluntly rounded tip; subterminal bristles always present on abdominal-mesial surface, typically dense and comprised of several rows extending sparsely or densely to the sternal surface, merging with bristles of the lateral abdominal surface that extend to tip (Figs. 7E and ​and7F);7F); larger subterminal bristle sockets distinct and often visible when bristles are damaged or missing.

Species included: Trierarchus acanthophallus (Chen & Yang, 2008), comb. nov.; Trierarchus cooperi (Borradaile, 1902), comb. nov.; Trierarchus corrugatus (Stephenson & Rees, 1961), comb. nov.; Trierarchus crosnieri (Vannini, 1983), comb. nov.; Trierarchus demani (Nobili, 1905), comb. nov. [=?Thalamita trilineata Stephenson & Hudson, 1957; ?Thalamita invicta Thallwitz, 1891]; Trierarchus hanseni (Alcock, 1899), comb. nov.; Trierarchus procorrugatus (Dai et al., 1986), comb. nov.; Trierarchus quadridentatus (Dai, Cai & Yang, 1996), comb. nov.; Trierarchus rotundifrons (A. Milne-Edwards, 1869), comb. nov.; Trierarchus sankarankuttyi (Crosnier & Thomassin, 1974), comb. nov.; Trierarchus squamosus (Stephenson & Hudson, 1957), comb. nov.; Trierarchus woodmasoni (Alcock, 1899), comb. nov.; Trierarchus taprobanicus (Alcock, 1899), comb. nov.

Remarks: The most diagnostic morphology of Trierarchus includes the G1, anterolateral margin and presence of squamiform markings and plumose setae. The G1 can be particularly useful (e.g., see also Crosnier, 1975a, Fig. 8; Crosnier & Thomassin, 1974, Fig. 8D; Chen & Yang, 2008, Fig. 7; Dai et al., 1986, Fig. 137A), however, both Tr. squamosus and Tr. rotundifrons possess divergent G1s (Stephenson & Hudson, 1957, Figs. 2K and 3K; Stephenson & Campbell, 1960, Figs. 1H and 2J). Additionally, Tr. rotundifrons is overall morphologically highly divergent from other members of this genus, likely due to its ecology as an obligate commensal. This species is smooth and lacks squamiform markings, most plumose setae, and most carinae on the chelipeds. Furthermore, its P5 dactyli are highly modified for firmly grasping host algae (Fig. 4F). Nevertheless, Tr. rotundifrons clearly displays a morphological affinity with other Trierarchus, most notably Tr. woodmasoni (compare Figs. 3F, ​,3I,3I, ​,9F9F and ​and9G).9G). Likewise, while Tr. rotundifrons was originally described in Camptonyx Heller, 1861, (an available junior synonym of Caphyra) it shares no close morphological or ecological affinity to C. polita (Heller, 1861), the type species of this invalid genus. Caphyra polita is a soft coral commensal with close morphological affinity to C. fulva (sampled here) and other Caphyra sensu stricto taxa (Crosnier, 1975b). Finally, it is worth noting that species delineations within Trierarchus remain problematic and a revision of this new genus is needed (e.g., see Crosnier, 1975a). Morphologically Tr. sankarankuttyi and Tr. procorrugatus have a strong affinity with Tr. cooperi, but they were described from limited material and interspecific differences were inadequately addressed (see Crosnier & Thomassin, 1974; Dai et al., 1986). Furthermore, while two well supported, genetically distinct Tr. cf. cooperi lineages were recovered here (sp. A and sp. B; Figs. 3G and ​and3H),3H), examination of multiple DNA barcoded specimens from each lineage failed to reveal clear morphological distinctions between the taxa (from preliminary analyses with unpublished data; but see discussion of color below). Moreover, many individuals from both OTUs fit a diagnosis of Tr. corrugatus (Stephenson & Rees, 1961). This inter- and intraspecific variation likely explains why Crosnier (1962) synonymized this species with Tr. cooperi, though they are currently treated as distinct (Ng, Guinot & Davie, 2008; Nguyen, 2013). Comparison of sequenced specimens of Tr. woodmasoni from across the Indo-Pacific (from preliminary analyses with unpublished data) also suggests that Tr. crosnieri, Tr. taprobanicus, and Tr. woodmasoni may be intraspecific variants. Thus, Trierarchus is likely comprised of fewer valid species than currently recognized, but more detailed studies will be needed.

Ecology: Members of Trierarchus typically inhabit high-energy, shallow marine environments, often in association with algae (Vannini, 1983; Hay et al., 1989; UF collection data; personal observations). In Guam Tr. rotundifrons is always found in association with Chlorodesmis algae in exposed reefs, Tr. cf. cooperi is recovered by sieving living Halimeda (note light green live color in sp. B; Fig. 3H), and Tr. woodmasoni is reliably recovered from sieving Sargassum and other co-distributed algae. Around Moorea Island, French Polynesia, Tr. cf. cooperi is typically recovered by sieving and breaking coral rubble from fore reef environments. However, unlike Tr. cf. cooperi recovered in Guam, the species collected in Moorea (sp. A; Fig. 3G) displays a live color mottled with red, orange and purple hues—shades common among coralline algae, sponges and other encrusting marine life in such substrate. Nevertheless, with the exception of Tr. rotundifrons, which is demonstrably an obligate commensal (Hay et al., 1989), other symbiotic associations suggested for this genus remain speculative and need further study. Finally, in contrast to other species, the rarely collected Tr. squamosus appears to prefer protected lagoonal waters, but no further microhabitat or live color data are available for the species.

Etymology: A trierach (Latin trierachus) is the captain of a trireme, an ancient Greek warship. For context see Etymology of Thranita (above). Gender masculine.

• Genus Zygita, gen. nov.

• Figures 3E, ​,7D,7D, ​,9C,9C, 14B–14E

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Type species: Goniosoma longifrons A. Milne-Edwards, 1869, by present designation; gender feminine.

Diagnosis: Carapace subhexagonal, approximately 1.5 times broader than long; frontal margin with six well-developed teeth of approximately even width separated by deep notches; inner supraorbital margin oblique and spiniform; anterolateral margin with five large, well-developed sharp teeth forming an oblique, inclined border reminiscent of Thalamonyx and Charybdis (Fig. 9C). Infraorbital lobe well developed and terminating in a spiniform or blunt point. Carapace, chelipeds and ambulatory legs subtly to substantially granular and covered with plumose setae (easily worn away in preserved specimens). Cheliped meri with a ventral anterodistal spine; carpus with additional dorsal spine between the typical three outer spines and a well-developed inner spine; manus Carina 4 distinct, granular and ending distally in a sharp or dull spinule (Fig. 14D), squamiform sculpture extending ventrally from Carina 5 to a poorly defined Carina 6. Meri of P2–P4 bearing a ventral posterodistal spine (Fig. 14E). P5 coxae bearing a stout, well-developed spinule dorsad; ischia with granular to spiniform distal border; meri with both a dorsal and ventral posterodistal spine; carpi with a well-developed spine on ventral posterodistal border; dactyli lancelet-shaped (especially in juveniles), but approaching paddle-shaped in larger individuals (Figs. 14B and 14C). G1 curved and tapering with a row of 1–12 subterminal bristles on lateral margin beginning just behind the tip; bristles continue sparsely across sternal surface extending to the mesial margin; mesial margin with similar, sometimes numerous spines beginning immediately behind tip (Fig. 7D).

Species included: Zygita longifrons (A. Milne-Edwards, 1869), comb. nov. [=Thalamita spinimera Stephenson & Rees, 1967; Thalamita yoronensis Sakai, 1969]; Zygita murinae (Zarenkov, 1971), comb. nov.

Remarks: The distinct morphology of this rarely collected genus is well known and deserving of generic rank (Stephenson & Rees, 1967a; Spiridonov & Neumann, 2008). The most diagnostic traits include the presence of a sharp or dull spinule at the distal end of manus Carina 4; meri of the ambulatory legs bearing a ventral posterodistal spine (Fig. 14E; asterisked); P5 coxa bearing a stout, well-developed dorsal spinule (Fig. 14B; asterisked); P5 carpus with a well-developed spine on the ventral posterodistal border (Fig. 14C; asterisked).

Ecology: In their original description of Thalamita spinimera, Stephenson & Rees (1967a) suggested these crabs were “ectocommensal” on Alcyonaria (=Octocorallia). However, this was based on one specimen collected from soft coral. A subsequent revision of this group by Spiridonov & Neumann (2008) failed to confirm this association, but only considered seven specimens. Evans & McKeon (2016) compiled compelling in situ photographs and collections records for 24 specimens and found that 46% (11 specimens) were found in association with soft corals (seven on nephtheid soft corals) in what is likely a facultative association.

Etymology: Zygita originates from Zygite, the title given to oarsmen occupying the middle tier of a trireme (a three-tiered ancient Greek warship). For context see Etymology of Thranita (above). Gender feminine.

Conclusion

This study constitutes the most comprehensive molecular phylogenetic analyses of Portunoidea to date, but highlights numerous areas where additional work is needed. Results support a more conservative classification of Portunoidea with three instead of eight extant families: Geryonidae (Geryonidae + Ovalipidae; new diagnosis provided), Carcinidae (Carcinidae + Pirimelidae + Polybiidae + Thiidae + Coelocarcinus; new diagnosis provided) and Portunidae. Limited molecular data also suggest that the family Brusiniidae may still be valid, but might not be a portunoid lineage. A major aim of this study was to investigate the molecular phylogenetic origin of symbiosis within Portunoidea by substantially increasing taxon sampling of the subfamilies Caphyrinae and Thalamitinae. Results support a shared ancestry of all symbiotic taxa (Caphyra, Lissocarcinus, and two Thalamita) derived within the thalamitine genus Thalamita. Consequently, Caphyrina Paulson, 1875, nom. trans., should be considered a subtribe within the subfamily Thalamitinae. Although the nature, degree, and phylogenetic pattern of symbiosis within Caphyrina needs further study, this clade is clearly dominated by symbiotic taxa and likely originated from a symbiotic ancestor. Results presented here also support the following taxonomic actions within Thalamitinae: Cronius is reclassified as a thalamitine rather than a portunine genus; Thalamonyx is reinstated as a valid genus; Goniosupradens is raised to the generic rank; and three new genera (Zygita gen. nov., Thranita gen. nov., and Trierarchus gen. nov.) are described to accommodate some Thalamita sensu lato taxa rendered paraphyletic by Caphyrina. A new diagnosis of Thalamitinae has also been provided.

Supplemental Information

Acknowledgments

Funding Statement

This work was supported through the National Science Foundation grant DEB-1406368 (DDIG; Co-PI Nathaniel Evans, PI Gustav Paulay), research funds made available during a Smithsonian Peter Buck Predoctoral Fellowship, and The Crustacean Society Fellowship funds in Graduate Studies. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References