Morphological description and molecular characterization of Heterospinus mccordi n. gen. n. sp. (Acanthocephala: Polymorphidae) from cystacanths infecting a non-native crayfish host, Procambarus clarkii (Decapoda: Cambaridae), in South Carolina, USA

Syst Parasitol (2025) 102:11 https://doi.org/10.1007/s11230-024-10195-8 Morphological description and molecular characterization of Heterospinus mccordi n. gen. n. sp. (Acanthocephala: Polymorphidae) from cystacanths infecting a non‑native crayfish host, Procambarus clarkii (Decapoda: Cambaridae), in South Carolina, USA Gregory K. Rothman · Kristina M. Hill‑Spanik Michael R. Kendrick · Peter R. Kingsley‑Smith · Graham A. Wagner · Isaure de Buron · Received: 6 September 2024 / Accepted: 10 October 2024 © The Author(s) 2024 Abstract A new genus and species within the family Polymorphidae Meyer, 1931 were erected to accommodate cystacanths recovered from the mesentery of individuals from a non-native population of the red swamp crayfish Procambarus clarkii (Girard), collected from South Carolina (USA). Morphological characteristics of the specimens collected included in both sexes a spindle-shaped body with a slender hindtrunk, two fields of markedly different sized spines on the foretrunk, the presence of a middle row of smaller scythe-shaped hooks on a proboscis armed with 19–20 longitudinal rows of 14–16 hooks; and in males, six cement glands, absence of genital spines, and a digitiform and spinose bursa (observed inverted). Sequencing portions of both the mitochondrial cytochrome c oxidase I (COI) and large subunit ribosomal RNA genes was completed, followed by phylogenetic analysis of a concatenated alignment. This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as CF520520-959144ED-A02F-5A87D5CCA3CF. G. K. Rothman · G. A. Wagner · M. R. Kendrick · P. R. Kingsley‑Smith Marine Resources Research Institute, South Carolina Department of Natural Resources, Charleston, SC 29412, USA G. K. Rothman · K. M. Hill‑Spanik · I. de Buron (*) Department of Biology, College of Charleston, Charleston, SC 29412, USA e-mail: Sequences from our specimens appeared in a clade with those of Hexaglandula corynosoma (Travassos, 1915) and Ibirhynchus dimorpha (Schmidt, 1973) but were 27% divergent from both using the COI marker. The genetic divergence of this parasite from other polymorphid genera, along with unique morphological features, justified erecting a new genus and new species. Herein we describe Heterospinus mccordi n. gen. n. sp. bringing the total number of genera within the family Polymorphidae to 16, and we emend and update the latest key that was provided for the genera within this family. This is the first record of polymorphids infecting P. clarkii outside of its native range. The definitive host remains unknown. Introduction Acanthocephalans of the family Polymorphidae Meyer, 1931 primarily parasitize aquatic birds and marine mammals and use various crustaceans as intermediate hosts to complete their life cycle. A morphological diagnostic feature common to individuals in this family is the presence of some pattern of trunk spination (Yamaguti, 1963; Schmidt, 1973). Morphological characters used to differentiate among polymorphid species have primarily been trunk shape, the distribution of spines on the trunk and of hypodermal nuclei in the tegument, presence/absence of genital spines, the armature of the proboscis, and to a lesser Vol.: (0123456789) 11 Page 2 of 18 extent, the number of cement glands (Schmidt, 1973; Presswell et al., 2020). Whereas such criteria can be convenient, morphological identification is typically difficult as many of these characters, supposedly diagnostic, have lost their boundaries over time, and many genera within the family Polymorphidae have overlapping morphological features and only very slight morphological distinctions (Schmidt, 1973; Aznar et al., 2006). This particularity of the family Polymorphidae has led to classification instability (GarcíaVarela et al., 2013) with a history of recurrent reassessments of genera assignment of species within this family (e.g., Schmidt, 1973; 1975; Amin, 1992; Aznar et al., 2006; García-Varela & Pérez-Ponce de León, 2008; García-Varela et al., 2009). Hence, integrating information other than morphology is particularly relevant in the systematics of the family Polymorphidae. The usefulness of ecological parameters, such as the type of intermediate or definitive hosts, was demonstrated with the reintroduction of Profilicollis Meyer, 1931 and Hexaglandula Petrochenko, 1950, and erection of Pseudocorynosoma Aznar, Pérez-Ponce de León, Raga, 2006 (see Nickol et al., 1999; 2002; Aznar et al., 2006, respectively). More recently, the use of DNA sequencing has allowed clarification of the taxonomic arrangement and relationships among some genera of the family (García-Varela & PérezPonce de León, 2008; García-Varela et al., 2009; 2011; 2013; Presswell et al., 2020; Ru et al., 2022), which is currently comprised of 15 accepted genera, including 11 for which molecular data are available (Presswell et al., 2020). The red swamp crayfish Procambarus clarkii (Girard) is native to parts of the Gulf of Mexico coastal plain (Hobbs, 1989; Campos & RodríguezAlmaraz, 1992) but is considered one of the World’s most successful global invaders, primarily due to its trade as a commodity food source (Oficialdegui et al., 2019). Procambarus clarkii is known to have many detrimental impacts to environments where it is introduced (e.g., Twardochleb et al., 2013), including serving as an important host for pathogens, and in turn, contributing to declines in native biodiversity (Martín-Torrijos et al., 2021). In South Carolina (SC), USA, P. clarkii was introduced in the 1970s (Pomeroy & Kahl, 1987) and since its introduction has spread rapidly with concomitant declines in both the occurrence and diversity of native crayfishes (Kendrick et al., 2024). Vol:. (1234567890) Syst Parasitol (2025) 102:11 The parasite community of P. clarkii has been well studied in its native range due to its importance in aquaculture (Edgerton et al., 2002; Longshaw, 2011), with the only reported acanthocephalan infection being by the polymorphid Ibirhynchus dimorpha (Schmidt, 1973) (formerly in Southwellina Witenberg, 1932) in Louisiana USA (Schmidt, 1973; García-Varela et al., 2011). Cystacanth infection in crayfish, also in Louisiana, was mentioned in Font (2007), but with no indication of the species of acanthocephalans encountered or of crayfish examined. Outside of its native range, acanthocephalan diversity associated with P. clarkii is not known, with one study in Hawaii examining specimens for infection by acanthocephalans but finding none (Font, 2007). Examination of P. clarkii in coastal SC revealed infection by polymorphid cystacanths whose morphology and genetics did not match a described species in this family. Herein, we propose the erection of Heterospinus mccordi n. gen. n. sp. based on both morphological and molecular characteristics of cystacanths. This is the first record of a polymorphid infecting P. clarkii in a non-native locality. Materials and Methods Specimen collection Adult spec (...truncated)