Nematodes (roundworms), a group of non-segmented worm-like invertebrates, are some of the most abundant animals on earth in terms of individuals (Lorenzen, 1994; Poinar, 2011). They are distributed worldwide in almost all habitats and play key roles in ecosystems by linking soil food webs, influencing plant growth and facilitating nutrient cycling (Yeates et al., 2009; van den Hoogen et al., 2019; Zhang et al., 2020). The earliest known definite nematode fossil occurs in the Lower Devonian Rhynie Chert inside the cortex cells of an early land plant and has been considered to be a plant parasite (Poinar et al., 2008), but unconfirmed nematode-like fossils and trace fossils may date back to the Precambrian (Poinar, 1979; Parry et al., 2017; De Baets et al., 2021a). Despite their abundance in many extant ecosystems, nematodes are exceedingly rare in the fossil record, since most of them are small, with soft bodies and concealed habits (Poinar, 2011).

The Mermithidae represent a family of nematodes that are obligate invertebrate parasites which occur in insects, millipedes, crustaceans, spiders, molluscs, and earthworms (Nickle, 1972; Poinar, 1979). They can affect the morphology, physiology, and even the behavior of their hosts (Petersen, 1985). The life cycle of mermithids comprises five stages (Poinar and Otieno, 1974; Poinar, 1983 ; Poinar, 2001b). Eggs are deposited in the environment, and the developing embryos moult once and emerge from the eggs as second-stage juveniles. These juveniles are the infective stage that enter the hemocoel of potential hosts. After a relatively rapid growth phase (third stage), mermithids exit hosts as postparasitic juveniles (fourth stage). They then enter a quiescent phase and moult twice to become adults (Poinar, 2015a). They tend to exit their hosts even before maturation, though, if their hosts are stressed (Poinar, 2015b). Hosts usually die when the mermithids exit, which is why mermithids have been widely studied as possible biological control agents, especially against aquatic stages of medically important insects like mosquito larvae (Petersen, 1985). Although mermithids kill their hosts like parasitoids, they are commonly considered as parasites like other nematodes (De Baets et al., 2021a; De Baets et al., 2021b).

Palaeontological records of parasitism provide critical clues about the origination and diversification of important nematode groups, and elucidate the synecology and coevolution of ancient parasites and their hosts. Due to their relatively large size and invertebrate-parasitic habits, mermithid nematodes are most likely of all nematodes to occur as recognizable fossils, especially in amber as they exited their invertebrate hosts that became entrapped in resin (Poinar, 2011). Their fossil record dates back to the Early Cretaceous with Cretacimermis libani from a chironomid midge (Diptera: Chironomidae) in Lebanese amber (~135 Ma; million years ago) (Poinar et al., 1994). However, there is a dearth of examples of other Cretaceous mermithids prior to the present study, with only Cretacimermis chironomae, also from chironomid hosts, Cretacimermis protus from biting midges (Diptera: Ceratopogonidae) and Cretacimermis aphidophilus from an aphid (Hemiptera: Burmitaphididae) in mid-Cretaceous Kachin amber (Poinar and Buckley, 2006; Poinar and Sarto i Monteys, 2008; Poinar, 2011; Poinar, 2017).

Here, we report 16 additional mermithid nematodes associated with their insect hosts in mid-Cretaceous Kachin amber (approximately 99 million years old). These examples triple the diversity of Cretaceous mermithids (from 4 to 13 species) and reveal previously unknown host–parasite relationships. Our study also shows that mermithids were widely distributed in a number of diverse insect lineages by the mid-Cretaceous, but they preferred to parasitize non-holometabolous rather than holometabolous insects, thus providing novel insights into the early evolution of nematode parasitism of insects.

The sixteen new mermithids associated with their insect hosts described above include 10 insect–mermithid associations. The hosts of nine species were previously unrecorded, which triples the diversity of Cretaceous Mermithidae (from 4 to 13 species). In today’s ecosystems, mermithids have been reported from a variety of arthropods, in a range of environments, and often infecting large percentages of host populations and causing mass mortality (Poinar, 1975; Poinar, 1979; Petersen, 1985). Despite their abundance in extant terrestrial ecosystems, mermithids are rare in the fossil record as they are not readily preserved as fossils. Twenty-two fossil mermithid species have been described from the Cenozoic with their hosts (Supplementary file 1: Table S1), mainly from Eocene Baltic amber (11 species) and Miocene Dominican amber (9 species), but only four pre-Cenozoic species associated with only two insect orders have previously been recorded (Poinar and Buckley, 2006; Poinar and Sarto i Monteys, 2008; Poinar, 2011; Poinar, 2017). However, according to our new records, nine insect orders are now known to have been infested by mermithid nematodes in Kachin amber and this number is even higher than that of Baltic amber (~45 Ma) and Dominican amber (~18 Ma) (six and three insect orders, respectively), despite a much longer time spent searching for nematodes in the latter two amber deposits (Poinar, 2011). Together with previously described mermithids in Kachin amber (Poinar, 2001b; Grimaldi et al., 2002; Poinar and Buckley, 2006; Poinar, 2011; Poinar, 2017), our results suggest that mermithid parasitism of insects was actually widespread during the mid-Cretaceous (Figure 8). Mermithids species are usually characterized by strong host specificity, they are specific to a single species or to one or two families of insects, and are almost always lethal to their hosts (Stoffolano, 1973; Petersen, 1985), thus our study indicates that the widespread mermithid parasitism probably already played an important role in regulating the population of insects in Cretaceous terrestrial ecosystems.

Figure 8

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Our study provides new information on fossil host–parasite associations, including three previously unknown host–mermithid associations and first fossil records of four host associations. One is Cretacimermis incredibilis sp. nov., which has completely exited from a bristletail (Archaeognatha). Its tail end is still adjacent to an exit wound on the host (Figure 2D), indicating a true parasitic association. There are no previous extant or extinct records of nematodes attacking bristletails (Poinar, 1975; Poinar, 2011). A second new mermithid–host association is barklice (Psocodea) with three different specimens parasitized by mermithids. No barklice are parasitized by mermithids today (Poinar, 1975), but our specimens imply that such relationship might have been quite common in the mid-Cretaceous. Two members of the extinct planthopper family Perforissidae were also parasitized by mermithids, thus providing the oldest record of mermithid parasitism of planthoppers. The mermithid Heydenius brownii parasitized achiliid planthoppers in Baltic amber (Poinar, 2001a) and this association also occurs in extant planthoppers (Choo et al., 1989; Helden, 2008). Furthermore, our findings are the first fossil records of mermithids parasitizing dragonflies (Odonata), earwigs (Dermaptera), crickets (Orthoptera) and cockroaches (Blattodea), four host associations predicted from extant records (Poinar, 1975).

Nematode body fossils are scarce and mainly known from amber (De Baets et al., 2021b), sometimes together with their hosts (Poinar, 2011). To explore the evolution of nematode–host relationship, we compiled nematode–host records in the three best-studied amber biotas (mid-Cretaceous Kachin amber, Eocene Baltic amber and Miocene Dominican amber; Supplementary file 1: Table S1). Our results indicate that not only the mermithids, but also the nematodes as a whole, experienced a certain degree of host transition between the Cretaceous and Cenozoic (Figure 9). We cannot fully exclude the possibility of collection bias, but its influence is probably low because Kachin amber has been extensively studied in the last two decades and its biota has already become the most diverse known amber biota; moreover, holometabolous insects are much more diverse in the collections than non-holometabolous ones (1296 vs 465 species: Ross, 2023). It is therefore unlikely that holometabolous insects are underrepresented among the known hosts of mermithids. Among the insect hosts of mermithids preserved in Kachin amber, only one of the nine orders (Diptera) is holometabolous (i.e. insects with ‘complete’ metamorphosis), whilst it is four out of six (Hymenoptera, Trichoptera, Lepidoptera and Diptera) in Baltic amber and all three insect host orders (Hymenoptera, Coleoptera and Diptera) are holometabolous in Dominican amber. The situation is similar when referring to the amount of nematode parasitism (Table 1). In Kachin amber, only about 40% of the hosts (in total, not only insects) are holometabolous, while this percentage increases to 80% in Baltic and Dominican amber and this result is acceptable when uncertainty is considered (Figure 9B). Diptera are the most common hosts of nematodes from all three amber biotas; also, the oldest fossil animal that was found to host a mermithid is a dipteran from Early Cretaceous Lebanese amber (Poinar et al., 1994). This is probably because most dipteran larvae develop in moist or aquatic environments that are particularly suitable habitats for nematodes (Poinar, 2011). It is evident that Holometabola are the most important hosts of extant mermithids as well as all invertebrate-parasitizing nematodes (Poinar, 1975) and this hexapod subgroup dominated the insect fauna during the Cretaceous (Labandeira and Sepkoski, 1993; Labandeira, 2005; Sohn et al., 2015; Peters et al., 2017; Zhang et al., 2018; Thomas et al., 2020; Wang et al., 2022). Our study suggests that, except for Diptera, nematodes had not completely exploited Holometabola as hosts in the mid-Cretaceous. This suggests that non-holometabolous insects (i.e. insects without ‘complete’ metamorphosis) were more available as hosts in the mid-Cretaceous and the widespread association between nematodes and Holometabola might have formed later.

Figure 9

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Finally, discovering these nematodes in mid-Cretaceous Kachin amber brings new opportunities to study the evolution of parasitism through the medium of amber. Amber is a unique form of fossilization (Hsieh and Plotnick, 2020). Although amber is patchily distributed in space and time, it is still especially suitable for investigating the evolution of terrestrial parasites associated with arthropods due to preservation potential (De Baets and Littlewood, 2015; Leung, 2017; De Baets et al., 2021a; De Baets et al., 2021b; Leung, 2021; Poinar, 2021). The high diversity of mermithid nematodes during the mid-Cretaceous as shown here provides a glimpse into the structure of ancient parasitic nematode–host associations and their evolution over the past 100 million years.

All data are available in the main text and/or the supplementary materials.

1. 1. Choo HY
   2. Kaya HK
   3. Kim JB

   (1989)

   Agamermis Unka (Mermithidae) Parasitism of Nilaparvata Lugens in rice fields in Korea

   Journal of Nematology 21:254–259..

   • PubMed
   • Google Scholar
2. 1. De Baets K
   2. Littlewood DTJ

   (2015) The importance of fossils in understanding the evolution of parasites and their vectors

   Advances in Parasitology 90:1–51.

   https://doi.org/10.1016/bs.apar.2015.07.001

   • PubMed
   • Google Scholar
3. Book

   1. De Baets K
   2. Dentzien-Dias P
   3. Harrison GWM
   4. Littlewood DTJ
   5. Parry LA

   (2021a) Fossil constraints on the timescale of parasitic helminth evolution

   In: De Baets K, Huntley JW, editors. The Evolution and Fossil Record of Parasitism: Identification and Macroevolution of Parasites. Cham, Switzerland: Springer International Publishing. pp. 231–271.

   https://doi.org/10.1007/978-3-030-42484-8

   • Google Scholar
4. Book

   1. De Baets K
   2. Huntley JW
   3. Klompmaker AA
   4. Schiffbauer JD
   5. Muscente AD

   (2021b) The fossil record of parasitism: its extent and taphonomic constraints

   In: De Baets K, Huntley JW, editors. The Evolution and Fossil Record of Parasitism: Coevolution and Paleoparasitological Techniques. Cham, Switzerland: Springer International Publishing. pp. 1–50.

   https://doi.org/10.1007/978-3-030-52233-9

   • Google Scholar
5. 1. Grimaldi DA
   2. Engel MS
   3. Nascimbene PC

   (2002) Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance

   American Museum Novitates 3361:1–71.

   https://doi.org/10.1206/0003-0082(2002)361<0001:FCAFMB>2.0.CO;2

   • Google Scholar
6. 1. Helden AJ

   (2008) First extant records of mermithid nematode parasitism of Auchenorrhyncha in Europe

   Journal of Invertebrate Pathology 99:351–353.

   https://doi.org/10.1016/j.jip.2008.05.005

   • PubMed
   • Google Scholar
7. 1. Hsieh S
   2. Plotnick RE

   (2020) The representation of animal behaviour in the fossil record

   Animal Behaviour 169:65–80.

   https://doi.org/10.1016/j.anbehav.2020.09.010

   • Google Scholar
8. Book

   1. International Commission on Zoological Nomenclature

   (1999)

   International Code of Zoological Nomenclature (4th ed)

   London: International Trust for Zoological Nomenclature.

   • Google Scholar
9. 1. Labandeira CC
   2. Sepkoski JJ

   (1993) Insect diversity in the fossil record

   Science 261:310–315.

   https://doi.org/10.1126/science.11536548

   • PubMed
   • Google Scholar
10. Book

    1. Labandeira CC

    (2005)

    Fossil history and evolutionary ecology of Diptera and their associations with plants

    In: Yeates DK, Wiegmann BM, editors. The Evolutionary Biology of Flies. New York: Columbia University Press. pp. 217–273.

    • Google Scholar
11. 1. Leung TLF

    (2017) Fossils of parasites: what can the fossil record tell us about the evolution of parasitism

    Biological Reviews 92:410–430.

    https://doi.org/10.1111/brv.12238

    • Google Scholar
12. Book

    1. Leung TLF

    (2021) Parasites of fossil vertebrates: what we know and what can we expect from the fossil record?

    In: De Baets K, Huntley JW, editors. The Evolution and Fossil Record of Parasitism: Identification and Macroevolution of Parasites. Cham: Springer International Publishing. pp. 1–28.

    https://doi.org/10.1007/978-3-030-42484-8

    • Google Scholar
13. Book

    1. Lorenzen S

    (1994)

    The Phylogenetic Systematics of Freeliving Nematodes

    The Ray Society.

    • Google Scholar
14. 1. Misof B
    2. Liu S
    3. Meusemann K
    4. Peters RS
    5. Donath A
    6. Mayer C
    7. Frandsen PB
    8. Ware J
    9. Flouri T
    10. Beutel RG
    11. Niehuis O
    12. Petersen M
    13. Izquierdo-Carrasco F
    14. Wappler T
    15. Rust J
    16. Aberer AJ
    17. Aspöck U
    18. Aspöck H
    19. Bartel D
    20. Blanke A
    21. Berger S
    22. Böhm A
    23. Buckley TR
    24. Calcott B
    25. Chen J
    26. Friedrich F
    27. Fukui M
    28. Fujita M
    29. Greve C
    30. Grobe P
    31. Gu S
    32. Huang Y
    33. Jermiin LS
    34. Kawahara AY
    35. Krogmann L
    36. Kubiak M
    37. Lanfear R
    38. Letsch H
    39. Li Y
    40. Li Z
    41. Li J
    42. Lu H
    43. Machida R
    44. Mashimo Y
    45. Kapli P
    46. McKenna DD
    47. Meng G
    48. Nakagaki Y
    49. Navarrete-Heredia JL
    50. Ott M
    51. Ou Y
    52. Pass G
    53. Podsiadlowski L
    54. Pohl H
    55. von Reumont BM
    56. Schütte K
    57. Sekiya K
    58. Shimizu S
    59. Slipinski A
    60. Stamatakis A
    61. Song W
    62. Su X
    63. Szucsich NU
    64. Tan M
    65. Tan X
    66. Tang M
    67. Tang J
    68. Timelthaler G
    69. Tomizuka S
    70. Trautwein M
    71. Tong X
    72. Uchifune T
    73. Walzl MG
    74. Wiegmann BM
    75. Wilbrandt J
    76. Wipfler B
    77. Wong TKF
    78. Wu Q
    79. Wu G
    80. Xie Y
    81. Yang S
    82. Yang Q
    83. Yeates DK
    84. Yoshizawa K
    85. Zhang Q
    86. Zhang R
    87. Zhang W
    88. Zhang Y
    89. Zhao J
    90. Zhou C
    91. Zhou L
    92. Ziesmann T
    93. Zou S
    94. Li Y
    95. Xu X
    96. Zhang Y
    97. Yang H
    98. Wang J
    99. Wang J
    100. Kjer KM
    101. Zhou X

    (2014) Phylogenomics resolves the timing and pattern of insect evolution

    Science 346:763–767.

    https://doi.org/10.1126/science.1257570

    • PubMed
    • Google Scholar
15. 1. Nickle WR

    (1972)

    A contribution to our knowledge of the Mermithidae (Nematoda)

    Journal of Nematology 4:113–146..

    • PubMed
    • Google Scholar
16. 1. Parry LA
    2. Boggiani PC
    3. Condon DJ
    4. Garwood RJ
    5. Leme JM
    6. McIlroy D
    7. Brasier MD
    8. Trindade R
    9. Campanha GAC
    10. Pacheco MLAF
    11. Diniz CQC
    12. Liu AG

    (2017) Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil

    Nature Ecology & Evolution 1:1455–1464.

    https://doi.org/10.1038/s41559-017-0301-9

    • Google Scholar
17. 1. Peters RS
    2. Krogmann L
    3. Mayer C
    4. Donath A
    5. Gunkel S
    6. Meusemann K
    7. Kozlov A
    8. Podsiadlowski L
    9. Petersen M
    10. Lanfear R
    11. Diez PA
    12. Heraty J
    13. Kjer KM
    14. Klopfstein S
    15. Meier R
    16. Polidori C
    17. Schmitt T
    18. Liu S
    19. Zhou X
    20. Wappler T
    21. Rust J
    22. Misof B
    23. Niehuis O

    (2017) Evolutionary history of the Hymenoptera

    Current Biology 27:1013–1018.

    https://doi.org/10.1016/j.cub.2017.01.027

    • PubMed
    • Google Scholar
18. Book

    1. Petersen JJ

    (1985) Nematodes as biological control agents: Part I. Mermithidae

    In: Baker JR, Muller R, editors. Advances in Parasitology. Academic Press. pp. 307–344.

    https://doi.org/10.1016/s0065-308x(08)60565-5

    • PubMed
    • Google Scholar
19. 1. Poinar GO
    2. Otieno WA

    (1974) Evidence of four Molts in the Mermithidae

    Nematologica 20:370.

    https://doi.org/10.1163/187529274X00456

    • Google Scholar
20. Book

    1. Poinar GO

    (1975)

    Entomogenous Nematodes: A Manual and Host List of Insect-Nematode Associations

    Leiden: E. J. Brill.

    • Google Scholar
21. Book

    1. Poinar GO

    (1979)

    Nematodes for Biological Control of Insects (1st ed)

    Boca Raton: CRC Press.

    • Google Scholar
22. Book

    1. Poinar GO

    (1983)

    The Natural History of Nematodes

    Englewood Cliffs: Prentice Hall.

    • Google Scholar
23. 1. Poinar GO
    2. Acra A
    3. Acra F

    (1994)

    Earliest fossil nematode (Mermithidae) in Cretaceous Lebanese amber

    Fundamental and Applied Nematology 17:475–477.

    • Google Scholar
24. 1. Poinar GO

    (2001a) Heydenius brownii sp. n. (Nematoda: Mermithidae) parasitising a planthopper (Homoptera: Achilidae) in Baltic amber

    Nematology 3:753–757.

    https://doi.org/10.1163/156854101753625263

    • Google Scholar
25. Book

    1. Poinar GO

    (2001b) Nematoda and Nematomorpha

    In: Thorp JH, Covich AP, editors. Ecology and Classification of North American Freshwater Invertebrates. New York: Academic Press. pp. 255–295.

    https://doi.org/10.1016/B978-0-12-374855-3.00009-1

    • Google Scholar
26. 1. Poinar GO
    2. Buckley R

    (2006) Nematode (Nematoda: Mermithidae) and hairworm (Nematomorpha: Chordodidae) parasites in early Cretaceous amber

    Journal of Invertebrate Pathology 93:36–41.

    https://doi.org/10.1016/j.jip.2006.04.006

    • Google Scholar
27. 1. Poinar GO
    2. Kerp H
    3. Hass H

    (2008) Palaeonema phyticum gen. n., sp. n. (Nematoda: Palaeonematidae fam. n.), a Devonian nematode associated with early land plants

    Nematology 10:9–14.

    https://doi.org/10.1163/156854108783360159

    • Google Scholar
28. 1. Poinar GO
    2. Sarto i Monteys V

    (2008) Mermithids (Nematoda: Mermithidae) of biting midges (Diptera: Ceratopogonidae): Heleidomermis cataloniensis n. sp. from Culicoides circumscriptus Kieffer in Spain and a species of Cretacimermis Poinar, 2001 from a ceratopogonid in Burmese amber

    Systematic Parasitology 69:13–21.

    https://doi.org/10.1007/s11230-007-9091-9

    • PubMed
    • Google Scholar
29. Book

    1. Poinar GO

    (2011) The Evolutionary History of Nematodes: As Revealed in Stone, Amber and Mummies

    Brill, Amersfoort.

    https://doi.org/10.1163/9789047428664

    • Google Scholar
30. Book

    1. Poinar GO

    (2015a) Phylum Nemata

    In: Thorp JH, Rogers DC, editors. Thorp and Covich’s Freshwater Invertebrates (Fourth Edition). Boston: Academic Press. pp. 273–302.

    https://doi.org/10.1016/B978-0-12-385026-3.00014-0

    • Google Scholar
31. 1. Poinar GO

    (2015b) The geological record of parasitic nematode evolution

    Advances in Parasitology 90:53–92.

    https://doi.org/10.1016/bs.apar.2015.03.002

    • PubMed
    • Google Scholar
32. 1. Poinar GO

    (2017) A mermithid nematode, Cretacimermis aphidophilus sp. n. (Nematoda: Mermithidae), parasitising an aphid (Hemiptera: Burmitaphididae) in Myanmar amber: a 100 million year association

    Nematology 19:509–513.

    https://doi.org/10.1163/15685411-00003063

    • Google Scholar
33. Book

    1. Poinar GO

    (2021) Fossil record of viruses, parasitic bacteria and parasitic protozoa

    In: De Baets K, Huntley JW, editors. The Evolution and Fossil Record of Parasitism: Identification and Macroevolution of Parasites. Cham: Springer International Publishing. pp. 29–68.

    https://doi.org/10.1007/978-3-030-42484-8

    • Google Scholar
34. 1. Ross AJ

    (2023) Supplement to the Burmese (Myanmar) amber checklist and bibliography, 2022

    Palaeoentomology 6:22–40.

    https://doi.org/10.11646/palaeoentomology.6.1.6

    • Google Scholar
35. 1. Shi G
    2. Grimaldi DA
    3. Harlow GE
    4. Wang J
    5. Wang J
    6. Yang M
    7. Lei W
    8. Li Q
    9. Li X

    (2012) Age constraint on Burmese amber based on U–PB dating of zircons

    Cretaceous Research 37:155–163.

    https://doi.org/10.1016/j.cretres.2012.03.014

    • Google Scholar
36. 1. Sohn JC
    2. Labandeira CC
    3. Davis DR

    (2015) The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): implications for evolutionary diversity and divergence-time estimates

    BMC Evolutionary Biology 15:12.

    https://doi.org/10.1186/s12862-015-0290-8

    • Google Scholar
37. 1. Stoffolano JG

    (1973) Host specificity of entomophilic nematodes—A review

    Experimental Parasitology 33:263–284.

    https://doi.org/10.1016/0014-4894(73)90033-7

    • Google Scholar
38. 1. Szwedo J
    2. Wang B
    3. Soszynska-Maj A
    4. Azar D
    5. Ross A

    (2020) International Palaeoentomological Society Statement

    Palaeoentomology 3:221–222.

    https://doi.org/10.11646/palaeoentomology.3.3.1

    • Google Scholar
39. 1. Thomas JA
    2. Frandsen PB
    3. Prendini E
    4. Zhou X
    5. Holzenthal RW

    (2020) A multigene phylogeny and timeline for Trichoptera (Insecta)

    Systematic Entomology 45:670–686.

    https://doi.org/10.1111/syen.12422

    • Google Scholar
40. Book

    1. Thu K
    2. Zaw K

    (2017) Chapter 23 Gem deposits of Myanmar

    In: Barber AJ, Zaw K, Crow MJ, editors. Myanmar: Geology, Resources and Tectonics. The Geological Society. pp. 497–529.

    https://doi.org/10.1144/M48.23

    • Google Scholar
41. 1. van den Hoogen J
    2. Geisen S
    3. Routh D
    4. Ferris H
    5. Traunspurger W
    6. Wardle DA
    7. de Goede RGM
    8. Adams BJ
    9. Ahmad W
    10. Andriuzzi WS
    11. Bardgett RD
    12. Bonkowski M
    13. Campos-Herrera R
    14. Cares JE
    15. Caruso T
    16. de Brito Caixeta L
    17. Chen X
    18. Costa SR
    19. Creamer R
    20. Mauro da Cunha Castro J
    21. Dam M
    22. Djigal D
    23. Escuer M
    24. Griffiths BS
    25. Gutiérrez C
    26. Hohberg K
    27. Kalinkina D
    28. Kardol P
    29. Kergunteuil A
    30. Korthals G
    31. Krashevska V
    32. Kudrin AA
    33. Li Q
    34. Liang W
    35. Magilton M
    36. Marais M
    37. Martín JAR
    38. Matveeva E
    39. Mayad EH
    40. Mulder C
    41. Mullin P
    42. Neilson R
    43. Nguyen TAD
    44. Nielsen UN
    45. Okada H
    46. Rius JEP
    47. Pan K
    48. Peneva V
    49. Pellissier L
    50. Carlos Pereira da Silva J
    51. Pitteloud C
    52. Powers TO
    53. Powers K
    54. Quist CW
    55. Rasmann S
    56. Moreno SS
    57. Scheu S
    58. Setälä H
    59. Sushchuk A
    60. Tiunov AV
    61. Trap J
    62. van der Putten W
    63. Vestergård M
    64. Villenave C
    65. Waeyenberge L
    66. Wall DH
    67. Wilschut R
    68. Wright DG
    69. Yang J
    70. Crowther TW

    (2019) Soil nematode abundance and functional group composition at a global scale

    Nature 572:194–198.

    https://doi.org/10.1038/s41586-019-1418-6

    • Google Scholar
42. 1. Wang B
    2. Xu C
    3. Jarzembowski EA

    (2022) Ecological radiations of insects in the Mesozoic

    Trends in Ecology & Evolution 37:529–540.

    https://doi.org/10.1016/j.tree.2022.02.007

    • Google Scholar
43. Book

    1. Yeates GW
    2. Ferris H
    3. Moens T
    4. Van Der Putten WH

    (2009) The role of nematodes in ecosystems

    In: Wilson MJ, Kakouli-Duarte T, editors. Nematodes as Environmental Indicators. CAB International. pp. 1–44.

    https://doi.org/10.1079/9781845933852.0000

    • Google Scholar
44. 1. Yu T
    2. Thomson U
    3. Mu L
    4. Ross A
    5. Kennedy J
    6. Broly P
    7. Xia F
    8. Zhang H
    9. Wang B
    10. Dilcher D

    (2019) An ammonite trapped in Burmese amber

    PNAS 116:11345–11350.

    https://doi.org/10.1073/pnas.1821292116

    • PubMed
    • Google Scholar
45. 1. Zhang SQ
    2. Che LH
    3. Li Y
    4. Pang H
    5. Ślipiński A
    6. Zhang P

    (2018) Evolutionary history of Coleoptera revealed by extensive sampling of genes and species

    Nature Communications 9:205.

    https://doi.org/10.1038/s41467-017-02644-4

    • PubMed
    • Google Scholar
46. 1. Zhang Y
    2. Li S
    3. Li H
    4. Wang R
    5. Zhang KQ
    6. Xu J

    (2020) Fungi-nematode interactions: diversity, ecology, and biocontrol prospects in agriculture

    Journal of Fungi 6:206.

    https://doi.org/10.3390/jof6040206

    • PubMed
    • Google Scholar

Author details

1. Cihang Luo

   1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
   2. University of Chinese Academy of Sciences, Beijing, China

   Contribution

   Conceptualization, Validation, Investigation, Visualization, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   chluo@nigpas.ac.cn

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4855-6185

2. George O Poinar

   Department of Integrative Biology, Oregon State University, Corvallis, United States

   Contribution

   Investigation, Visualization, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

3. Chunpeng Xu

   1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
   2. University of Chinese Academy of Sciences, Beijing, China

   Contribution

   Investigation, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

4. De Zhuo

   Beijing Xiachong Amber Museum, Beijing, China

   Contribution

   Investigation, Visualization

   Competing interests

   No competing interests declared

5. Edmund A Jarzembowski

   State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

6. Bo Wang

   State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China

   Contribution

   Conceptualization, Supervision, Funding acquisition, Validation, Investigation, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   bowang@nigpas.ac.cn

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8001-9937

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