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.

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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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