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Widespread mermithid nematode parasitism of Cretaceous insects

Luo, Cihang, Poinar, George O, Xu, Chunpeng, Zhuo, De, Jarzembowski, Edmund A, Wang, Bo·2023·eLife
DOI 10.7554/elife.86283PMC PMC10348742

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Abstract

Mermithid nematodes are obligate invertebrate parasites dating back to the Early Cretaceous. Their fossil record is sparse, especially before the Cenozoic, thus little is known about their early host associations. This study reports 16 new mermithids associated with their insect hosts from mid-Cretaceous Kachin amber, 12 of which include previously unknown hosts. These fossils indicate that mermithid parasitism of invertebrates was already widespread and played an important role in the mid-Cretaceous terrestrial ecosystem. Remarkably, three hosts (bristletails, barklice, and perforissid planthoppers) were previously unknown to be parasitized by mermithids both past and present. Furthermore, our study shows that in contrast to their Cenozoic counterparts, Cretaceous nematodes including mermithids are more abundant in non-holometabolous insects. This result suggests that nematodes had not completely exploited the dominant Holometabola as their hosts until the Cenozoic. This study reveals what appears to be a vanished history of nematodes that parasitized Cretaceous insects.

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Figure 1. Mermithids and their insect hosts from mid-Cretaceous Kachin amber (~99 Ma; million years ago). (A) Cretacimermis incredibilis sp. nov. (holotype) adjacent to its bristletail host. (B) Cretacimermis calypta sp. nov. (holotype) adjacent to its damselfly host. (C) Two separate specimens of Cretacimermis adelphe sp. nov. (upper specimen is holotype) that have emerged from their earwig host. (D) Cretacimermis directa sp. nov. (holotype) adjacent to its cricket host. (E) Cretacimermis longa sp. nov. (holotype) adjacent to its adult cockroach host. (F) Cretacimermis longa sp. nov. (paratype) adjacent to its juvenile cockroach host. (G) Cretacimermis perforissi sp. nov. (holotype) adjacent to its perforissid planthopper host. (H) Cretacimeris perforissi sp. nov. (paratype) adjacent to second perforissid planthopper. Scale bars = 2.0 mm (B, E, F), 1.0 mm (A, C, D, G), 0.5 mm (H).
Figure 1. Mermithids and their insect hosts from mid-Cretaceous Kachin amber (~99 Ma; million years ago). (A) Cretacimermis incredibilis sp. nov. (holotype) adjacent to its bristletail host. (B) Cretacimermis calypta sp. nov. (holotype) adjacent to its damselfly host. (C) Two separate specimens of Cretacimermis adelphe sp. nov. (upper specimen is holotype) that have emerged from their earwig host. (D) Cretacimermis directa sp. nov. (holotype) adjacent to its cricket host. (E) Cretacimermis longa sp. nov. (holotype) adjacent to its adult cockroach host. (F) Cretacimermis longa sp. nov. (paratype) adjacent to its juvenile cockroach host. (G) Cretacimermis perforissi sp. nov. (holotype) adjacent to its perforissid planthopper host. (H) Cretacimeris perforissi sp. nov. (paratype) adjacent to second perforissid planthopper. Scale bars = 2.0 mm (B, E, F), 1.0 mm (A, C, D, G), 0.5 mm (H).CC BY · PubMed Central
Figure 2. Detailed photographs of Cretacimermis incredibilis sp. nov., holotype, NIGP201872 (A–D), Cretacimermis calypta sp. nov., holotype, NIGP201870 (E–H), and Cretacimermis adelphe sp. nov. (upper specimen is holotype and lower specimen is paratype), NIGP201876 (I–K). (A) Habitus of C. incredibilis, some trophosome remains are marked by triangular black arrows. (B) Fine ridges in areas of body bends. (C) Head (arrowed). (D) Tail and the exit wound on the host (arrowed). (E) Habitus except head part of C. calypta, some trophosome remains are marked by triangular black arrows. (F) Detail of body. (G) Head. (H) Tail. (I) Habitus of upper specimen (holotype), opaque body and pointed head. (J) Detail of head. (K) Detail of tail. Scale bars = 0.5 mm (A, E), 0.2 mm (H, I), 0.1 mm (B–D, F, G, J, K). Abbreviations: he, head; ta, tail.
Figure 2. Detailed photographs of Cretacimermis incredibilis sp. nov., holotype, NIGP201872 (A–D), Cretacimermis calypta sp. nov., holotype, NIGP201870 (E–H), and Cretacimermis adelphe sp. nov. (upper specimen is holotype and lower specimen is paratype), NIGP201876 (I–K). (A) Habitus of C. incredibilis, some trophosome remains are marked by triangular black arrows. (B) Fine ridges in areas of body bends. (C) Head (arrowed). (D) Tail and the exit wound on the host (arrowed). (E) Habitus except head part of C. calypta, some trophosome remains are marked by triangular black arrows. (F) Detail of body. (G) Head. (H) Tail. (I) Habitus of upper specimen (holotype), opaque body and pointed head. (J) Detail of head. (K) Detail of tail. Scale bars = 0.5 mm (A, E), 0.2 mm (H, I), 0.1 mm (B–D, F, G, J, K). Abbreviations: he, head; ta, tail.CC BY · PubMed Central
Figure 3. Detailed photographs of Cretacimermis directa sp. nov., holotype, NIGP201873 (A, B) and Cretacimermis longa sp. nov., holotype, NIGP201875 (C–F), paratype, NIGP201877 (G–J). (A) Detail of head. (B) Detail of tail. (C) Host, an adult of Mesoblattinidae (Blattodea), note the hollow abdomen (arrowed) that probably contained the developing nematode. (D) Detail of body. (E) Enlarged details of body. (F) Head. (G) Host, a juvenile of Mesoblattinidae (Blattodea). (H) The termination of the nematode, note the mermithid was in the process of emerging from the host’s body (arrowed). (I) Detail of body. (J) Head, showing loose outer cuticle. Scale bars = 1.0 mm (C, G), 0.5 mm (D), 0.2 mm (H, I), 0.1 mm (A, B, E, F, J). Abbreviations: he, head; ta, tail.
Figure 3. Detailed photographs of Cretacimermis directa sp. nov., holotype, NIGP201873 (A, B) and Cretacimermis longa sp. nov., holotype, NIGP201875 (C–F), paratype, NIGP201877 (G–J). (A) Detail of head. (B) Detail of tail. (C) Host, an adult of Mesoblattinidae (Blattodea), note the hollow abdomen (arrowed) that probably contained the developing nematode. (D) Detail of body. (E) Enlarged details of body. (F) Head. (G) Host, a juvenile of Mesoblattinidae (Blattodea). (H) The termination of the nematode, note the mermithid was in the process of emerging from the host’s body (arrowed). (I) Detail of body. (J) Head, showing loose outer cuticle. Scale bars = 1.0 mm (C, G), 0.5 mm (D), 0.2 mm (H, I), 0.1 mm (A, B, E, F, J). Abbreviations: he, head; ta, tail.CC BY · PubMed Central
Figure 4. Detailed photographs of Cretacimermis perforissi sp. nov., holotype, NIGP201868 (A–E) and paratype, NIGP201878 (F–H). (A) Host, Perforissidae (Hemiptera: Fulgoromorpha), note the hollow abdomen (arrowed) which probably contained the developing nematode. (B) Habitus of the coiled body of C. perforissi, some trophosome remains are marked by triangular black arrows. (C) Detail of body, note artefact ridges on cuticle. (D) Head. (E) Tail. (F) Host, Perforissidae (Hemiptera: Fulgoromorpha), note the broken abdomen that is probably due to the emergence of the mermithid. (G) Front view of host, indicating it is a perforissid planthopper. (H) Detail of body, showing smooth cuticle and dark, fractured trophosomes (arrowed). Scale bars = 0.5 mm (A, B, F), 0.2 mm (G), 0.1 mm (C–E, H). Abbreviations: he, head; ta, tail.
Figure 4. Detailed photographs of Cretacimermis perforissi sp. nov., holotype, NIGP201868 (A–E) and paratype, NIGP201878 (F–H). (A) Host, Perforissidae (Hemiptera: Fulgoromorpha), note the hollow abdomen (arrowed) which probably contained the developing nematode. (B) Habitus of the coiled body of C. perforissi, some trophosome remains are marked by triangular black arrows. (C) Detail of body, note artefact ridges on cuticle. (D) Head. (E) Tail. (F) Host, Perforissidae (Hemiptera: Fulgoromorpha), note the broken abdomen that is probably due to the emergence of the mermithid. (G) Front view of host, indicating it is a perforissid planthopper. (H) Detail of body, showing smooth cuticle and dark, fractured trophosomes (arrowed). Scale bars = 0.5 mm (A, B, F), 0.2 mm (G), 0.1 mm (C–E, H). Abbreviations: he, head; ta, tail.CC BY · PubMed Central
Figure 5. Mermithids and their insect hosts from mid-Cretaceous Kachin amber. Part II. (A) Cretacimermis manicapsoci sp. nov. (holotype) adjacent to its manicapsocid barklouse host. (B) Cretacimermis manicapsoci sp. nov. (paratype) adjacent to second manicapsocid barklouse host. (C) Cretacimermis psoci sp. nov. (holotype) adjacent to its compsocid barklouse host. (D) Cretacimermis cecidomyiae sp. nov. (holotype) emerging from its gall midge (cecidomyiid) host. (E–H) Four specimens of Cretacimermis chironomae Poinar, 2011 emerging from their chironomid hosts. Scale bars = 2.0 mm (A), 1.0 mm (B), 0.5 mm (C–H).
Figure 5. Mermithids and their insect hosts from mid-Cretaceous Kachin amber. Part II. (A) Cretacimermis manicapsoci sp. nov. (holotype) adjacent to its manicapsocid barklouse host. (B) Cretacimermis manicapsoci sp. nov. (paratype) adjacent to second manicapsocid barklouse host. (C) Cretacimermis psoci sp. nov. (holotype) adjacent to its compsocid barklouse host. (D) Cretacimermis cecidomyiae sp. nov. (holotype) emerging from its gall midge (cecidomyiid) host. (E–H) Four specimens of Cretacimermis chironomae Poinar, 2011 emerging from their chironomid hosts. Scale bars = 2.0 mm (A), 1.0 mm (B), 0.5 mm (C–H).CC BY · PubMed Central
Figure 6. Detailed photographs of Cretacimermis manicapsoci sp. nov., holotype, NIGP201879 (A–D), paratype, NIGP201880 (E–G), and Cretacimermis psoci sp. nov., holotype, NIGP201874 (H–J). (A) Barklouse host, Manicapsocidae (Psocoptera). (B) Detail of body. (C) Head. (D) Tail. (E) Barklouse host, Manicapsocidae. (F) Coiled body. (G) Head. (H) Barklouse host, Compsocidae (Psocoptera), note the broken abdomen that is probably due to the emergence of the mermithid. (I) Detail of body. (J) Tail, note artefactual cuticular ridges. Scale bars = 0.5 mm (A), 0.2 mm (E, F, H), 0.1 mm (B–D, G, I, J). Abbreviations: he, head; ta, tail.
Figure 6. Detailed photographs of Cretacimermis manicapsoci sp. nov., holotype, NIGP201879 (A–D), paratype, NIGP201880 (E–G), and Cretacimermis psoci sp. nov., holotype, NIGP201874 (H–J). (A) Barklouse host, Manicapsocidae (Psocoptera). (B) Detail of body. (C) Head. (D) Tail. (E) Barklouse host, Manicapsocidae. (F) Coiled body. (G) Head. (H) Barklouse host, Compsocidae (Psocoptera), note the broken abdomen that is probably due to the emergence of the mermithid. (I) Detail of body. (J) Tail, note artefactual cuticular ridges. Scale bars = 0.5 mm (A), 0.2 mm (E, F, H), 0.1 mm (B–D, G, I, J). Abbreviations: he, head; ta, tail.CC BY · PubMed Central
Figure 7. Mermithids and their Diptera hosts from mid-Cretaceous Kachin amber. (A–C) Cretacimermis cecidomyiae sp. nov., holotype, NIGP201871. (A) Head of cecidomyiid host. (B) Habitus of nematode, some trophosome remains are marked by triangular black arrows. (C) Detail of body. (D–H) First piece with Cretacimermis chironomae Poinar, 2011, NIGP201869. (D) Detail of head of host. (E) Habitus of nematode. (F) Forewing venation of host. (G) Detail of body. (H) Detail of head. (I–K) Second piece of C. chironomae, LYD-MD-NG001. (I) Detail of head of host. (J) Forewing venation of host. (K) Habitus of nematode, note that a portion of the mermithid is still in the host’s abdomen. (L–N) Third piece with C. chironomae, LYD-MD-NG002. (L) Detail of head of host. (M) Forewing venation of host. (N) Detail of head and body. (O–Q) Fourth piece with C. chironomae, NIGP201881. (O) Detail of head of host. (P) Forewing venation of host. (Q) Habitus of two nematodes. Scale bars = 0.2 mm (B, E, K, O–Q), 0.1 mm (A, D, F, G, I, J, L–N), 50 μm (C, H). Abbreviation: he, head.
Figure 7. Mermithids and their Diptera hosts from mid-Cretaceous Kachin amber. (A–C) Cretacimermis cecidomyiae sp. nov., holotype, NIGP201871. (A) Head of cecidomyiid host. (B) Habitus of nematode, some trophosome remains are marked by triangular black arrows. (C) Detail of body. (D–H) First piece with Cretacimermis chironomae Poinar, 2011, NIGP201869. (D) Detail of head of host. (E) Habitus of nematode. (F) Forewing venation of host. (G) Detail of body. (H) Detail of head. (I–K) Second piece of C. chironomae, LYD-MD-NG001. (I) Detail of head of host. (J) Forewing venation of host. (K) Habitus of nematode, note that a portion of the mermithid is still in the host’s abdomen. (L–N) Third piece with C. chironomae, LYD-MD-NG002. (L) Detail of head of host. (M) Forewing venation of host. (N) Detail of head and body. (O–Q) Fourth piece with C. chironomae, NIGP201881. (O) Detail of head of host. (P) Forewing venation of host. (Q) Habitus of two nematodes. Scale bars = 0.2 mm (B, E, K, O–Q), 0.1 mm (A, D, F, G, I, J, L–N), 50 μm (C, H). Abbreviation: he, head.CC BY · PubMed Central
Figure 8. The fossil record of Mermithidae plotted on the phylogenetic tree of insects. The chronogram of the insect tree is modified from Misof et al., 2014 (thin black line); insect orders without a fossil record of mermithid parasitism are excluded. Thick black lines indicate the presence of mermithid parasitism. Rectangles represent the fossil number of species of mermithid not exceeding one, hexagons represent the fossil number of mermithids between two and five (inclusively), and circles represent the fossil number of mermithids more than five. Yellow coloration within the symbols represents previous records, red coloration within the symbols represents records in this paper. 1 – Lebanese amber, Early Cretaceous, approximately 135 Ma; 2 – Kachin amber, mid-Cretaceous, approximately 99 Ma; 3 – Baltic amber, Eocene, approximately 45 Ma; 4 – Rhine lignite (brown coal), Oligocene/Miocene, approximately 24 Ma; 5 – Mexican amber, Early Miocene, approximately 20 Ma; 6 – Dominican amber, Miocene, approximately 18 Ma. 7 – Willershausen, Kreis Osterode, Germany, Late Pliocene, approximately 3 Ma.
Figure 8. The fossil record of Mermithidae plotted on the phylogenetic tree of insects. The chronogram of the insect tree is modified from Misof et al., 2014 (thin black line); insect orders without a fossil record of mermithid parasitism are excluded. Thick black lines indicate the presence of mermithid parasitism. Rectangles represent the fossil number of species of mermithid not exceeding one, hexagons represent the fossil number of mermithids between two and five (inclusively), and circles represent the fossil number of mermithids more than five. Yellow coloration within the symbols represents previous records, red coloration within the symbols represents records in this paper. 1 – Lebanese amber, Early Cretaceous, approximately 135 Ma; 2 – Kachin amber, mid-Cretaceous, approximately 99 Ma; 3 – Baltic amber, Eocene, approximately 45 Ma; 4 – Rhine lignite (brown coal), Oligocene/Miocene, approximately 24 Ma; 5 – Mexican amber, Early Miocene, approximately 20 Ma; 6 – Dominican amber, Miocene, approximately 18 Ma. 7 – Willershausen, Kreis Osterode, Germany, Late Pliocene, approximately 3 Ma.CC BY · PubMed Central
Figure 9. The occurrence frequency of invertebrate–nematode associations from mid-Cretaceous Kachin amber (~99 Ma), Eocene Baltic amber (~45 Ma) and Miocene Dominican amber (~18 Ma). (A) Pie diagrams, the quantity of fossil species is indicated below the orders. (B) Stacked bar plots, error bars represent 95% binomial confidence intervals (for data, see also Table 1).
Figure 9. The occurrence frequency of invertebrate–nematode associations from mid-Cretaceous Kachin amber (~99 Ma), Eocene Baltic amber (~45 Ma) and Miocene Dominican amber (~18 Ma). (A) Pie diagrams, the quantity of fossil species is indicated below the orders. (B) Stacked bar plots, error bars represent 95% binomial confidence intervals (for data, see also Table 1).CC BY · PubMed Central

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Authors
Luo, C., Poinar, G. O., Xu, C., Zhuo, D., Jarzembowski, E. A., & Wang, B.
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2023-07-14
Volume
12
ISSN
2050-084X
DOI
10.7554/elife.86283
PMC
PMC10348742
Cited by
10
References
1
Language
en
Licence
Funders
  • National Natural Science Foundation of China (42125201)
  • Chinese Academy of Sciences (Strategic Priority Research Program XDB26000000)
  • Second Tibetan Plateau Scientific Expedition and Research (2019QZKK0706)
  • CAS President's International Fellowship Initiative
  • UNESCO-IUGS (IGCP Project 679)

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