Widespread mermithid nematode parasitism of Cretaceous insects
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eLife assessment
This important study greatly expands our knowledge of the fossil record of Mermithid nematodes, modern members of which are ecologically important parasitoids of arthropods, annelids and mollusks today. The most important finding, convincingly presented, is that mermithids parasitized a number of insect clades in the Cretaceous that they are not known to infect today or in Cenozoic amber. The evidence for a shift in exploited hosts from heterometabolous insects in the Cretaceous to holometabolous ones in the Miocene is solid but could be made exceptional by adding a small quantitative analysis with confidence intervals and bar plots from the data already compiled in the supplementary material; potential collection bias should be addressed as well.
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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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Author Response
Reviewer #1 (Public Review):
Mermithid nematodes are ecologically important parasitoids of arthropods, annelids and mollusks today. Their fossil record in amber reaches back into the Early Cretaceous, some 135 million years ago. Luo et al. more than triple this record by presenting, with ample illustrations, exceptionally well preserved new specimens from the beginning of the Late Cretaceous (99 Ma ago) of Myanmar. Their most important finding is that mermithids parasitized a number of insect clades in the Cretaceous that they are not known to infect today or in Cenozoic amber; further, the proportion of holometabolous insects among the hosts is found to be lower in the Cretaceous than in the Cenozoic. The strengths of the paper lie in the specimens, the illustrations of the specimens, and the documentation of when, …
Author Response
Reviewer #1 (Public Review):
Mermithid nematodes are ecologically important parasitoids of arthropods, annelids and mollusks today. Their fossil record in amber reaches back into the Early Cretaceous, some 135 million years ago. Luo et al. more than triple this record by presenting, with ample illustrations, exceptionally well preserved new specimens from the beginning of the Late Cretaceous (99 Ma ago) of Myanmar. Their most important finding is that mermithids parasitized a number of insect clades in the Cretaceous that they are not known to infect today or in Cenozoic amber; further, the proportion of holometabolous insects among the hosts is found to be lower in the Cretaceous than in the Cenozoic. The strengths of the paper lie in the specimens, the illustrations of the specimens, and the documentation of when, where and how the specimens were acquired. Certain nomenclatural aspects of the paper require improvement. A potential weakness of the paper could be collection bias: it is not tested whether the collections used to show the shift toward holometabolous hosts from the mid-Cretaceous to the Cenozoic are representative of the fossil record as it is preserved and accessible today.
Thank you very much for pointing out these issues. We have added a new Figure 10 and Table 1 to our paper. Indeed, collection bias is almost present in all amber biotas. However, we believe we have robust reasons to argue that the shift to holometabolous hosts does exist. Although Kachin amber has only been studied extensively in the last two decades (compared with centuries of study in Baltic amber or Dominican amber), it has become by far the most intensively studied amber biota since its Cretaceous age was appreciated, now comprising an exceptional 700 families (Ross, 2023). Also, the fossil record of holometabolous insects is clearly much better than heterometabolous insects in Kachin amber (1296 spp. vs 465 spp. respectively). But as shown in our paper, the nematodes we found in Kachin amber are mainly associated with heterometabolous insects. Therefore, even if collection bias might exist, such as the presence of some unreported nematode-Holometabola associations, we believe our conclusion about the shift is robust. We also add some explanation in our paper.
Reviewer #2 (Public Review):
This manuscript reports on mermithid nematode fossils from amber which dates from the Cretaceous period. The specimens described in the manuscript consist of insects and associated nematodes which have been trapped in amber and fossilised. The nematodes have been identified as belonging to the Mermithidae family, a family of nematode worm that infect insects. The findings of this manuscript provide an insight into the evolution history of nematodes and parasitism. Despite the ubiquity of both nematodes and parasites in extant ecosystems, fossil records of both are very rare. This is because nematodes and many parasites are soft bodied, and many are located inside their hosts' bodies, thus they rarely become fossilised. Thus, most of what is known about the evolutionary history of nematodes, and evolution of parasitism are based on what could be inferred from extant examples.
The specimens described in this manuscript provides a valuable contribution to our understanding of parasitism in the geological past. These amber specimens are a snapshot of parasite-host interactions - interactions which are commonly found in nature but are rarely captured in fossils. The identification of the specimens as mermithid nematodes are based on sound scientific reasoning. The worms' morphology and position in relation to the insects are consistent with what have been observed with extant mermithid nematodes.
Additionally, one of the values of such parasite fossils is that they provide us with insight into parasite-host combinations or interactions which may have existed throughout the geological past, but no longer exist today or cannot be inferred from extant taxa. It helps fill in major gaps in our understanding of parasitism. This was the case with the amber fossil that contained a bristletail with its nematode parasite.
We are very grateful for the positive and encouraging comments.
Reviewer #3 (Public Review):
The authors provide a timely description of new mermithid nematodes from Cretaceous amber and use it to argue an important shift in insect host exploitation. The descriptions are state-of-the-art and will become valid once the appropriate zoobank numbers are used after publication. The authors also compiled crucial and detailed new information on the host exploitation in amber nematodes in the supplementary material. This data is also depicted in pie diagrams and seems at first glance to support their interpretations of a shifts in host exploitation in fossil amber deposits when analysed appropriately and statistically but such an true analysis and depiction should be part of the main manuscript to do the compilation and interpretation justice. For the sake of reproducibility and the field, such fundamental statistical analysis as well as a statistical comparison with modern hosts would make this broad-sweeping claim of a major host shift and importance of amber deposits containing such nematode-insect interactions since the Cretaceous (even) more robust and fundamental.
Thanks. We realized this drawback and now we calculated the 95% CI using the Agresti-Coull method of the “binom.confint” function from the binom R package (https://cran.r-project.org/package=binom) of R 4.2.2. We also added a new Figure 10 and Table 1 in our paper. But, since we compiled the “occurrence” of invertebrate–nematode associations from these amber localities, it is impossible to compare with modern mermithids. For example, the parasite of Cretacimermis chironomae occurs five times in Kachin amber, but an extant dipteran-parasitized mermithid species can occur many times just in a single pond. However, it is evident that mermithids and all invertebrate-parasitized nematodes prefer to infect holometabolous insects rather than other invertebrates (Poinar, 1975; Poinar, personal observation). We have also added some explanation to our paper.
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eLife assessment
This important study greatly expands our knowledge of the fossil record of Mermithid nematodes, modern members of which are ecologically important parasitoids of arthropods, annelids and mollusks today. The most important finding, convincingly presented, is that mermithids parasitized a number of insect clades in the Cretaceous that they are not known to infect today or in Cenozoic amber. The evidence for a shift in exploited hosts from heterometabolous insects in the Cretaceous to holometabolous ones in the Miocene is solid but could be made exceptional by adding a small quantitative analysis with confidence intervals and bar plots from the data already compiled in the supplementary material; potential collection bias should be addressed as well.
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Reviewer #1 (Public Review):
Mermithid nematodes are ecologically important parasitoids of arthropods, annelids and mollusks today. Their fossil record in amber reaches back into the Early Cretaceous, some 135 million years ago. Luo et al. more than triple this record by presenting, with ample illustrations, exceptionally well preserved new specimens from the beginning of the Late Cretaceous (99 Ma ago) of Myanmar. Their most important finding is that mermithids parasitized a number of insect clades in the Cretaceous that they are not known to infect today or in Cenozoic amber; further, the proportion of holometabolous insects among the hosts is found to be lower in the Cretaceous than in the Cenozoic. The strengths of the paper lie in the specimens, the illustrations of the specimens, and the documentation of when, where and how the …
Reviewer #1 (Public Review):
Mermithid nematodes are ecologically important parasitoids of arthropods, annelids and mollusks today. Their fossil record in amber reaches back into the Early Cretaceous, some 135 million years ago. Luo et al. more than triple this record by presenting, with ample illustrations, exceptionally well preserved new specimens from the beginning of the Late Cretaceous (99 Ma ago) of Myanmar. Their most important finding is that mermithids parasitized a number of insect clades in the Cretaceous that they are not known to infect today or in Cenozoic amber; further, the proportion of holometabolous insects among the hosts is found to be lower in the Cretaceous than in the Cenozoic. The strengths of the paper lie in the specimens, the illustrations of the specimens, and the documentation of when, where and how the specimens were acquired. Certain nomenclatural aspects of the paper require improvement. A potential weakness of the paper could be collection bias: it is not tested whether the collections used to show the shift toward holometabolous hosts from the mid-Cretaceous to the Cenozoic are representative of the fossil record as it is preserved and accessible today.
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Reviewer #2 (Public Review):
This manuscript reports on mermithid nematode fossils from amber which dates from the Cretaceous period. The specimens described in the manuscript consist of insects and associated nematodes which have been trapped in amber and fossilised. The nematodes have been identified as belonging to the Mermithidae family, a family of nematode worm that infect insects.
The findings of this manuscript provide an insight into the evolution history of nematodes and parasitism. Despite the ubiquity of both nematodes and parasites in extant ecosystems, fossil records of both are very rare. This is because nematodes and many parasites are soft bodied, and many are located inside their hosts' bodies, thus they rarely become fossilised. Thus, most of what is known about the evolutionary history of nematodes, and evolution of …
Reviewer #2 (Public Review):
This manuscript reports on mermithid nematode fossils from amber which dates from the Cretaceous period. The specimens described in the manuscript consist of insects and associated nematodes which have been trapped in amber and fossilised. The nematodes have been identified as belonging to the Mermithidae family, a family of nematode worm that infect insects.
The findings of this manuscript provide an insight into the evolution history of nematodes and parasitism. Despite the ubiquity of both nematodes and parasites in extant ecosystems, fossil records of both are very rare. This is because nematodes and many parasites are soft bodied, and many are located inside their hosts' bodies, thus they rarely become fossilised. Thus, most of what is known about the evolutionary history of nematodes, and evolution of parasitism are based on what could be inferred from extant examples.
The specimens described in this manuscript provides a valuable contribution to our understanding of parasitism in the geological past. These amber specimens are a snapshot of parasite-host interactions - interactions which are commonly found in nature but are rarely captured in fossils. The identification of the specimens as mermithid nematodes are based on sound scientific reasoning. The worms' morphology and position in relation to the insects are consistent with what have been observed with extant mermithid nematodes.
Additionally, one of the values of such parasite fossils is that they provide us with insight into parasite-host combinations or interactions which may have existed throughout the geological past, but no longer exist today or cannot be inferred from extant taxa. It helps fill in major gaps in our understanding of parasitism. This was the case with the amber fossil that contained a bristletail with its nematode parasite.
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Reviewer #3 (Public Review):
The authors provide a timely description of new mermithid nematodes from Cretaceous amber and use it to argue an important shift in insect host exploitation. The descriptions are state-of-the-art and will become valid once the appropriate zoobank numbers are used after publication. The authors also compiled crucial and detailed new information on the host exploitation in amber nematodes in the supplementary material. This data is also depicted in pie diagrams and seems at first glance to support their interpretations of a shifts in host exploitation in fossil amber deposits when analysed appropriately and statistically but such an true analysis and depiction should be part of the main manuscript to do the compilation and interpretation justice. For the sake of reproducibility and the field, such fundamental …
Reviewer #3 (Public Review):
The authors provide a timely description of new mermithid nematodes from Cretaceous amber and use it to argue an important shift in insect host exploitation. The descriptions are state-of-the-art and will become valid once the appropriate zoobank numbers are used after publication. The authors also compiled crucial and detailed new information on the host exploitation in amber nematodes in the supplementary material. This data is also depicted in pie diagrams and seems at first glance to support their interpretations of a shifts in host exploitation in fossil amber deposits when analysed appropriately and statistically but such an true analysis and depiction should be part of the main manuscript to do the compilation and interpretation justice. For the sake of reproducibility and the field, such fundamental statistical analysis as well as a statistical comparison with modern hosts would make this broad-sweeping claim of a major host shift and importance of amber deposits containing such nematode-insect interactions since the Cretaceous (even) more robust and fundamental.
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