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Molecular and morphological evidence for nine species in North American Australapatemon (Sudarikov, 1959): a phylogeny expansion with description of the zygocercous Australapatemon mclaughlini n. sp.

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Abstract

Zygocercous (aggregating) cercarial larvae were recently discovered emerging from a physid snail during a molecular survey of cercariae from molluscs in lakes in central Alberta, Canada. This manuscript delves into the characterization of these cercariae through morphological and molecular techniques and provides the first genetic information for a zygocercous larval trematode. Analyses of cytochrome c oxidase I of mitochondrial DNA and two partial regions of nuclear ribosomal DNA sequences revealed the zygocercous cercariae to belong to the genus Australapatemon Sudarikov, 1959. Further analyses of sequences of Australapatemon burti (Miller, 1923), from cercariae and adults collected from across North America, indicate a complex of nine genetically-distinct lineages within this species, a surprising level of diversity. The zygocercous cercariae, along with adult worms collected from ducks in Manitoba, Canada, and from Mexico, represent one of these lineages, and are herein described as Australapatemon mclaughlini n. sp. Seven lineages cannot yet be identified, but one is tentatively identified as Australapatemon burti.

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Acknowledgements

We thank Arlene Oatway of the Advanced Microscopy Facility at the University of Alberta for her assistance with SEM processing and imaging. We also thank Lisa Kish, Valerie K. Phillips, and Mahmoud Tarrabain for assistance with field collections and sample processing in Alberta, where work was funded by Alberta Innovates Energy and Environment Solutions grant 2078 and 2332, and National Sciences and Engineering Research Council (NSERC) grant 418540 (PCH), and in Manitoba by NSERC grant A6979 to J. Daniel Mclaughlin. MAG was partly supported by an NSERC CREATE Host-Parasite Interactions student scholarship. SAL was supported by the Puerto Rico Science, Technology and Research Trust. We also thank Pieter Johnson (University of Colorado), for providing samples from California, and David J. Marcogliese (Environment and Climate Change Canada) for encouraging early phases of this study, which was also funded by the Canadian Federal Government’s Genomics Research Development Initiative, NSERC Discovery Grant (A6979), and by Paul D. N. Hebert at the Center for Biodiversity Genomics, University of Guelph, Canada through funding from NSERC, Genome Canada, the Ontario Genomics Institute and the International Barcode of Life initiative. We acknowledge two anonymous reviewers for their constructive comments on an earlier version of the manuscript.

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Authors and Affiliations

  1. University of Alberta School of Public Health, 357F South Academic Building, Edmonton, AB, T6G 2G7, Canada

    Michelle A. Gordy & Patrick C. Hanington

  2. Department of Biology, University of Puerto Rico at Mayagüez, Box 9000, Mayagüez, 00681–9000, Puerto Rico

    Sean A. Locke

  3. Department of Biology, Cape Breton University, 1250 Grand Lake Road, PO Box 5300, Sydney, NS, B1P 6L2, Canada

    Timothy A. Rawlings

  4. Department of Biology, Concordia University, 7141 Sherbrooke West, Montreal, QC, H4B 1R6, Canada

    Angela R. Lapierre

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  1. Michelle A. Gordy
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Correspondence to Patrick C. Hanington.

Electronic supplementary material

Suppl. Fig. 1

Bayesian inference phylograms of the Strigeidae and outgroups (Diplostomidae) derived from a) partial 28S, and b) partial ITS1–5.8S rDNA gene sequences with posterior probability values followed by bootstrap proportions given above branches. Values less than 0.5 are not reported. Scale bars denote number of substitutions per site. (PDF 3077 kb).

Suppl. Table 1

Review of zygocercous and aggregating cercariae. (XLSX 14 kb).

Suppl. Table 2

Estimates of evolutionary divergence over sequence pairs between and within groups among three genetic markers (cox1, 28S, ITS1–5.8S–ITS2). Each marker is represented by a matrix. Below the diagonal is the number of base pair differences per site from averaging over all sequence pairs between groups (interspecific divergence values), otherwise referred to as p distance values. Values pertaining specifically to the genus Australapatemon are within the grey box. Minimum and maximum mean interspecific divergence values among A. burti lineages are in bold and underlined. Standard error estimates are based on 1000 bootstrap replicates and above the diagonal and are coloured blue. The number of base pair differences per site from averaging over all sequence pairs within each group (intraspecific divergence values) is shown along the diagonal in red. Missing values, represented by a minus sign, are present for groups that contain singletons, and therefore estimates cannot be made. For cox1, the analysis involved 120 nucleotide sequences with a total of 399 positions in the final dataset. For 28S, the analysis involved 14 nucleotide sequences with a total of 807 positions in the final dataset. Finally, for ITS1–5.8S–ITS2, the analysis involved 26 nucleotide sequences with a total of 482 positions in the final dataset (partial ITS1–5.8 s after final trimming). All positions containing gaps and missing data were eliminated. (XLSX 15 kb).

Suppl. Table 3

Statistics for morphometric comparisons of cercariae of lineages 1, 6, 7, 8, and 9 with those of Australapatemon (Cercaria) burti (Miller, 1923), Cercaria laramiensis (Hendrickson & Kingston, 1974), and Cercaria absurda (Miller, 1927). Statistical tests used were Kruskal-Wallis analysis of variance (H), and post hoc multiple comparisons test, with Bonferroni correction for multiple tests. Statistical significance (α = 0.05) is indicated by bold text and an asterisk. Only significant comparisons between lineages/species are listed. (PDF 27 kb).

Suppl. Table 4

Statistics for significant comparisons between cercaria within LIN1. Statistics reported are from a post hoc multiple comparisons test, with Bonferroni correction for multiple tests. Statistical significance (α = 0.05) is indicated by bold text and an asterisk. (PDF 11 kb).

Suppl. Table 5

Summary data from samples from which DNA sequences were obtained. (XLSX 15.9 kb).

Suppl. Table 6

Comparison of morphology of adults in four genetically distinguished lineages of Australapatemon and A. mclaughlini n. sp., with ten species of Australapatemon. Listed are differences between the lineage and the species (e.g., adults of A. mclaughlini n. sp. are smaller than A. anseris, but have larger eggs). TL=total length; OS=oral sucker; PH=pharynx; VS=ventral sucker; FB=forebody; HB=hindbody; HB:FB=hindbody length/forebody length; AT=anterior testis; PT=posterior testis; GC=genital cone. (XLSX 11 kb).

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Gordy, M.A., Locke, S.A., Rawlings, T.A. et al. Molecular and morphological evidence for nine species in North American Australapatemon (Sudarikov, 1959): a phylogeny expansion with description of the zygocercous Australapatemon mclaughlini n. sp.. Parasitol Res 116, 2181–2198 (2017). https://doi.org/10.1007/s00436-017-5523-x

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