[Crustacea • 2018] Molecular Phylogenetics of Swimming Crabs (Portunoidea Rafinesque, 1815) supports A Revised Family-Level Classification and suggests A Single Derived Origin of Symbiotic Taxa ---ScRaBBlE

 (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 (F, H–J) by Nathaniel Evans; photographs (E, G) by Gustav Paulay.

in Evans, 2018.   DOI: 10.7717/peerj.4260 

Abstract

Portunoidea is a diverse lineage of ecologically and economically important marine crabs comprising 8 families and 14 subfamilies. Closely related portunid subfamilies Caphyrinae and Thalamitinae constitute some of this group’s greatest morphological and taxonomic diversity, and are the only known lineages to include symbiotic taxa. Emergence of symbiosis in decapods remains poorly studied and portunoid crabs provide an interesting, but often overlooked example. Yet the paucity of molecular phylogenetic data available for Portunoidea makes it challenging to investigate the evolution and systematics of the group. Phylogenetic analyses, though limited, suggest that many putative portunoid taxa are para- or polyphyletic. Here I augment existing molecular data—significantly increasing taxon sampling of Caphyrinae, Thalamitinae, and several disparate portunoid lineages—to investigate the phylogenetic origin of symbiosis within Portunoidea and reevaluate higher- and lower-level portunoid classifications. Phylogenetic analyses were carried out on sequences of H3, 28S rRNA, 16S rRNA, and CO1 for up to 168 portunoid taxa; this included, for the first time, molecular data from the genera Atoportunus, Brusinia, Caphyra, Coelocarcinus, Gonioinfradens, Raymanninus, and Thalamonyx. Results support the placement of all symbiotic taxa (Caphyra, Lissocarcinus, and two Thalamita) in a single clade derived within the thalamitine genus Thalamita. Caphyrina Paulson, 1875, nom. trans. is recognized here as a subtribe within the subfamily Thalamitinae. Results also support the following taxonomic actions: Cronius is reclassified as a thalamitine genus; Thalamonyx is reestablished 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 s.l. taxa rendered paraphyletic by Caphyrina. A new diagnosis of Thalamitinae is provided. Results also support a more conservative classification of Portunoidea comprising three instead of eight extant families: Geryonidae (Geryonidae + Ovalipidae; new diagnosis provided), Carcinidae (Carcinidae + Pirimelidae + Polybiidae + Thiidae + Coelocarcinus; new diagnosis provided) and Portunidae. Finally, 16s rRNA data suggests family Brusiniidae might not be a portunoid lineage.

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.

 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. 

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.

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.

Nathaniel Evans. 2018. Molecular Phylogenetics of Swimming Crabs (Portunoidea Rafinesque, 1815) supports A Revised Family-Level Classification and suggests A Single Derived Origin of Symbiotic Taxa. PeerJ. 6:e4260.  DOI: 10.7717/peerj.4260

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