Expanding on expansus: a new species of Scaphanocephalus from North America and the Caribbean based on molecular and morphological data

Abstract

Members of the genus Scaphanocephalus mature in accipitrids, particularly osprey, Pandion haliaetus, with metacercaria causing Black Spot Syndrome in reef fishes. In most of the world, only the type species, Scaphanocephalus expansus (Creplin, 1842) has been reported. Recent molecular studies in the Western Atlantic, Mediterranean and Persian Gulf reveal multiple species of Scaphanocephalus, but have relied on 28S rDNA, mainly from metacercariae, which limits both morphological identification and resolution of closely related species. Here we combine nuclear rDNA with mitochondrial sequences from adult worms collected in osprey across North America and the Caribbean to describe species and elucidate life cycles in Scaphanocephalus. A new species described herein can be distinguished from S. expansus based on overall body shape and size. Phylogenetic analysis of the whole mitochondrial genome of Scaphanocephalus indicates a close relationship with Cryptocotyle. We conclude that at least 3 species of Scaphanocephalus are present in the Americas and 2 others are in the Old World. Specimens in the Americas have similar or identical 28S to those in the Mediterranean and Persian Gulf, but amphi-Atlantic species are unlikely in light of divergence in cytochrome c oxidase I and the lack of amphi-Atlantic avian and fish hosts. Our results provide insight into the geographic distribution and taxonomy of a little-studied trematode recently linked to an emerging pathology in ecologically important reef fishes.

Keywords: Black Spot Syndrome; coral reef fish; fluke; helminth; raptor.

Graphical abstract

Figure 1.

Line drawing of type specimen of Scaphanocephalus robustus n. sp. from Pandion halietus from Virginia, USA. Hologenophore for sequence PP456670 (cytochrome c oxidase I) and PP436435 (28S), deposited in the Museum of Southwestern Biology (MSB:Para:49138). Scale bar is 1 mm.

Figure 2.

Phylogenetic analysis of 28 partial 28S sequences of Scaphanocephalus in the present (16 sequences) and prior studies (12 sequences). The maximum likelihood topology is shown and nodes are annotated with posterior probability (Bayesian inference)/bootstrap support (1000 replicates in maximum likelihood). The trimmed alignment was 1048 nt in length. The ML tree was generated using nucleotide substitution model GTR + G; the BI tree using HKY + G. The same tree, with individual sequences labelled with GenBank accessions, is available in Supplementary Fig. 1.

Figure 3.

Histogram of uncorrected P distances in Scaphanocephalus among (a) 33 partial 28S sequences from the present and prior studies and (b) 28 partial cytochrome c oxidase 1 sequences from the present study.

Figure 4.

Phylogenetic analysis of 26 partial CO1 sequences of Scaphanocephalus generated in the present study. The Bayesian inference topology is shown with nodes annotated with posterior probability (Bayesian inference, BI)/bootstrap support (1000 replicates in ML) based on a 415-nt alignment. The ML tree was generated using substitution model GTR + I; the BI tree using HKY + I.

Figure 5.

Phylogenetic analysis of concatenated partial 28S (1059 nt) and CO1 (374 nt) sequences of Scaphanocephalus. The maximum likelihood topology is shown and nodes are annotated with posterior probability (Bayesian inference)/bootstrap support (1000 replicates in maximum likelihood). The ML tree was generated using substitution model GTR + I; the BI tree using HKY + I with unlinked parameters in an alignment partitioned into 28S and CO1.

Figure 6.

Phylogenetic analysis of complete mitochondrial genomes (1059 nt). The maximum likelihood topology is shown and nodes are annotated with posterior probability (Bayesian inference)/bootstrap support (1000 replicates in maximum likelihood). Maximum likelihood and Bayesian inference trees were both generated using substitution model GTR + G + I.