No Tail No Fail: Life Cycles of the Zoogonidae (Digenea)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sampling
2.2. Morphological Analysis
2.3. Molecular Analysis
2.4. Visualization
3. Results
3.1. General Observations
3.2. Molecular Data and Life Cycles Elucidation
3.3. Phylogenetic Position of Pseudozoogonoides subaequiporus
3.4. Infection Data and Morphological Descriptions
3.4.1. Maritae of Zoogonoides viviparus
3.4.2. Metacercariae of Zoogonoides viviparus
3.4.3. Sporocysts, Developing and Infective Cercariae of Zoogonoides viviparus (Figure 3A–C and Figure 4)
3.4.4. Maritae of Pseudozoogonoides subaequiporus
3.4.5. Metacercariae of Pseudozoogonoides subaequiporus (Figure 5)
3.4.6. Sporocysts, Developing and Infective Cercariae of Pseudozoogonoides subaequiporus (Figure 3D–F and Figure 6)
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Host | Number of Dissected Individuals | Zoogonid Infection | ||
---|---|---|---|---|
Gastropoda | Buccinidae | Buccinum undatum Linnaeus, 1758 | 2174 | + |
B. scalariforme Møller, 119 | 19 | + | ||
Neptunea despecta (Linnaeus, 1758) | 103 | + | ||
Naticidae | Cryptonatica affinis (Gmelin, 1791) | 270 | - | |
Euspira pallida (Broderip & GB Sowerby I, 1829) | 24 | - | ||
Amauropsis islandica (Gmelin, 1791) | 3 | - | ||
Capulidae | Ariadnaria borealis (Broderip & G. B. Sowerby I, 1829) | 28 | - | |
Margaritidae | Margarites helicinus (Phipps, 1774) | 17 | - | |
Muricidae | Boreotrophon clavatus (G. O. Sars, 1878) | 8 | - | |
Annelida | Nereididae | Nereis pelagica Linnaeus, 1758 | 11 | - |
Pectinariidae | Cistenides hyperborea Malmgren, 1866 | 9 | - | |
Nephtyidae | Nephtys sp. | 8 | + | |
Polynoidae | Lepidonotus squamatus (Linnaeus, 1758) | 5 | - | |
Orbiniidae | Scoloplos armiger (Müller, 1776) | 4 | - | |
Trichobranchidae | Terebellides stroemii Sars, 1835 | 1 | - | |
Lumbrineridae | Scoletoma fragilis (O.F. Müller, 1776) | 1 | - | |
Bivalvia | Mytilidae | Musculus discors (Linnaeus, 1767) | 31 | - |
Cardiidae | Serripes groenlandicus (Mohr, 1786) | 66 | + | |
Ciliatocardium ciliatum (Fabricius, 1780) | 39 | + | ||
Nuculanidae | Nuculana pernula (O. F. Müller, 1779) | 394 | + | |
Yoldiidae | Yoldia hyperborea (Gould, 1841) | 78 | + | |
Portlandia arctica (Gray, 1824) | 6 | - | ||
Nuculidae | Ennucula tenuis (Montagu, 1808) | 5 | - | |
Decapoda | Paguridae | Pagurus pubescens Krøyer, 1838 | 12 | - |
Pandalidae | Pandalus montagui Leach, 1814 | 8 | - | |
Thoridae | Eualus gaimardii (H. Milne Edwards, 1837) | 4 | - | |
Crangonidae | Crangon crangon (Linnaeus, 1758) | 2 | - | |
Sabinea septemcarinata (Sabine, 1824) | 1 | - | ||
Ophiuroidea | Ophiuridae | Ophiura robusta (Ayres, 1852) | 67 | - |
Ophiopholidae | Ophiopholis aculeata (Linnaeus, 1767) | 40 | - |
ID | Species | Stage | Host Species | GenBank Accession Numbers | |
---|---|---|---|---|---|
28S rDNA | 5.8S rDNA+ITS2 | ||||
G7.3 | Zoogonoides viviparus | Marita | Limanda limanda | OP956058 | OP956013 |
G7.2 | Z. viviparus | Marita | Anarhichas lupus | OP956059 | OP956014 |
A5.36 | Z. viviparus | Marita | L. limanda | OP956060 | OP956015 |
G7.8 | Putative Z. viviparus | Metacercaria | Nephthys sp. | OP956061 | OP956016 |
G7.5 | Putative Z. viviparus | Metacercaria | Nuculana pernula | OP956062 | OP956017 |
G7.4 | Putative Z. viviparus | Metacercaria | Ciliatocardium ciliatum | OP956063 | OP956018 |
G7.9 | Putative Z. viviparus | Sporocyst with cercariae | Buccinum undatum | OP956064 | OP956019 |
G7.10 | Putative Z. viviparus | Sporocyst with cercariae | B. undatum | OP956065 | OP956020 |
A5.37 | Putative Z. viviparus | Sporocyst with cercariae | B. undatum | OP956066 | OP956021 |
A5.38 | Putative Z. viviparus | Sporocyst with cercariae | B. undatum | OP956067 | OP956022 |
G7.6 | Pseudozoogonoides subaequiporus | Marita | A. lupus | OP956068 | OP956023 |
G7.7 | P. subaequiporus | Marita | A. lupus | OP956069 | OP956024 |
D9.6 | Putative P. subaequiporus | Metacercaria | N. pernula | OP956070 | OP956025 |
D9.7 | Putative P. subaequiporus | Metacercaria | N. pernula | OP956071 | OP956026 |
D9.4 | Putative P. subaequiporus | Sporocyst with cercariae and metacercariae | Neptunea despecta | OP956072 | OP956027 |
D11.3 | Putative P. subaequiporus | Sporocyst with cercariae and metacercariae | B. undatum | OP956073 | OP956028 |
G7.1 | Lepidophyllum steenstrupi | Marita | A. lupus | OP956074 | OP956029 |
AG4.12 | Zoogonidae gen. sp. | Sporocyst with germ balls | B. scalariforme | OP956075 | OP956030 |
Product | Primer | Sequence (5′-3′), Forward (F) and Reverse (R) | Thermocycling Profile | Reference |
---|---|---|---|---|
18S rDNA | 18S1A | F, GGCGATCGAAAAGATTAAGCCATGCA | 94 °C—1 m 52 °C—1 m 72 °C—1 m ×35 | [32] primers and conditions |
32 | R, CGAAGTCCTATTCCATTATTC | |||
652 | F, GCAGCCGCGGTAATTCCAGCTC | |||
28 | R, AGCGACGGGCGGTGTGT | |||
28S rDNA | digl2 | F, AAGCATATCACTAAGCGG | 95 °C—30 s 54 °C—30 s 72 °C—2 m ×40 | [33] primers and conditions |
1500R | R, GCTATCCTGAGGGAAACTTCG | [34] primers and conditions | ||
5.8S+ITS2 | 3S | F, GTACCGGTGGATCACGTGGCTAGTG | 94 °C—30 s 55 °C—30 s 72 °C—1 m ×30 | [35] primers |
ITS2.2 | R, CCTGGTTAGTTTCTTTTCCTCCGC |
Zoogonoides viviparus (Maritae) n = 10 | Z. viviparus (Metacercariae) n = 6 | Z. viviparus (Cercariae) n = 11 | Pseudozoogonoides subaequiporus (Maritae) n = 12 | P. subaequiporus (Cercariae) n = 11 | |
---|---|---|---|---|---|
Length | 766 (665–831) | 385 (341–446) | 388 (337–451) | 747 (622–929) | 301 (248–385) |
Width | 246 (206–281) | 115 (101–137) | 139 (125–158) | 295 (237–341) | 118 (98–136) |
Forebody, length | 273 (227–294) | 172 (151–196) | 179 (153–242) | 255 (219–304) | 128 (96–180) |
Length:forebody ratio | 1:0.36 (0.31–0.39) | 1:0.45 (0.40–0.50) | 1:0.46 (0.43–0.54) | 1:0.34 (0.29–0.39) | 1:0.42 (0.35–0.48) |
Oral sucker | 114 (88–137) × 127 (102–144) | 68 (59–81) × 73 (60–99), n = 7 | 73 (63–79) × 73 (65–83) | 129 (107–152) × 130 (113–146) | 58 (50–66) × 57 (50–66) |
Ventral sucker | 187 (168–222) × 182 (164–202) | 99 (82–114) × 94 (82–132), n = 7 | 103 (93–119) × 87 (71–98) | 138 (127–156) × 137 (121–182) | 60 (54–65) × 60 (55–66) |
Sucker ratio | 1:1.66 (1.43–1.99) | 1:1.47 (1.33–1.68) n = 7 | 1:1.40 (1.19–1.63) | 1:1.08 (0.97–1.27) | 1:1.05 (0.92–1.24) |
Stylet | - | - | 16 (12–20) × 5 (4–6) n = 9 | - | 13 (10–16) × 4 (3–5) n = 8 |
Pharynx | 37 (30–55) × 47 (43–50) | 23 (18–36) × 30 (24–34), n = 7 | 23 (17–36) × 29 (26–32) | 40 (28–50) × 45 (36–53) | 19 (15–21) × 23 (21–25) |
Esophagus | 84 (71–95) | 52 (36–77) | 61 (46–76) | 78 (44–97) | 43 (26–69) |
Cirrus-sac | 261 (210–296) × 52 (44–65) | 95 (81–115) × 23 (19–27), n = 4 | 87 (62–102) × 19 (17–23) | 278 (203–325) × 74 (64–89) | 67 (56–85) × 14 (12–15) |
Ovary | 96 (77–121) × 72 (60–89) | 31 (21–41) × 28 (18–39), n = 5 | 28 (24–30) × 23 (20–27) | 102 (81–150) × 93 (75–144) | 18 (17–20) × 15 (14–17) |
Testis, anterior | 87 (65–123) × 72 (53–94) | 39 (23–57) × 31 (18–47), n = 5 | 48 (42–57) × 36 (33–40) | 112 (78–144) × 83 (64–103) | 25 (16–30) × 18 (12–23) |
Testis, posterior | 83 (67–113) × 75 (63–101) | 37 (25–57) × 31 (21–44), n = 5 | 45 (40–50) × 33 (27–37) | 99 (78–138) × 80 (67–112) | 25 (18–30) × 19 (14–23) |
Eggs | 64 (56–76) × 28 (23–31) | - | - | 70 (61–79) × 30 (27–33), n = 10 | - |
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Kremnev, G.; Gonchar, A.; Uryadova, A.; Krapivin, V.; Skobkina, O.; Gubler, A.; Krupenko, D. No Tail No Fail: Life Cycles of the Zoogonidae (Digenea). Diversity 2023, 15, 121. https://doi.org/10.3390/d15010121
Kremnev G, Gonchar A, Uryadova A, Krapivin V, Skobkina O, Gubler A, Krupenko D. No Tail No Fail: Life Cycles of the Zoogonidae (Digenea). Diversity. 2023; 15(1):121. https://doi.org/10.3390/d15010121
Chicago/Turabian StyleKremnev, Georgii, Anna Gonchar, Alexandra Uryadova, Vladimir Krapivin, Olga Skobkina, Arseniy Gubler, and Darya Krupenko. 2023. "No Tail No Fail: Life Cycles of the Zoogonidae (Digenea)" Diversity 15, no. 1: 121. https://doi.org/10.3390/d15010121
APA StyleKremnev, G., Gonchar, A., Uryadova, A., Krapivin, V., Skobkina, O., Gubler, A., & Krupenko, D. (2023). No Tail No Fail: Life Cycles of the Zoogonidae (Digenea). Diversity, 15(1), 121. https://doi.org/10.3390/d15010121