Many insects mimic other organisms or use camouflage to hide from predators. For example, some modern animals mimic the organism lichens, which are formed from algae and fungus, and grow almost everywhere on Earth, from the Arctic to the desert.

The most iconic example of an insect mimicking a species of lichen is the peppered moth. During the industrial revolution, darker colored moths were better at surviving. But when the revolution ended and pollution levels declined, species of lichen began to re-emerge and increase the survival of paler moths. Yet, it is unclear how and when insects first evolved this ingenious survival strategy, as distinctive examples of insects mimicking lichens are missing from fossil records.

To answer this question, Fang et al. set out to find fossils of lichen-mimicking insects that occurred at the same time as fossils of lichens. This approach led to the discovery of two new species of lacewing insects and their related species of foliose lichen. Previous work suggested that the foliose lichen, which has a lobe like shape, did not exist more than 65 million years ago. However, the findings of Fang et al. indicate that the foliose lichen existed 165 million years ago during the age of dinosaurs, and therefore arose much earlier than previously thought.

The two new species found in north-eastern China, form a new subgroup within the moth lacewing family that Fang et al. have named ‘Lichenipolystoechotes’. Close examination of both species of lacewing and the lichen under the microscopy revealed a near perfect match in their appearance. The branching patterns of the insects’ wing markings fit the branching patterns of the lichen. Taken together, these findings suggest that, not only did lichen mimics exist in the age of the dinosaurs, but that this strategy of using lichen mimicry as a form of survival was already very effective during this time period.

This discovery suggests that, 165 million years ago, a micro-ecosystem of lichens and insects existed in north-eastern China. It invites new questions about how that ecosystem worked. For example, how did the lichen benefit from its relationship with lacewing insects? Further investigations could reveal the answers and uncover more interesting insects hidden in the fossil record.

Modern insects have dramatic morphological specializations that match various objects of the environment. For instance, the specializations occurring in katydids and butterflies that mimic leaves, stick insects and inchworms that resemble twigs, and orchid mantids that duplicate orchid flowers, provide ecological insights for understanding mimetic associations between insect mimics and their plant models (Stevens, 2011; Gullan and Cranston, 2014; Maran, 2017). These and other fascinating cases reveal that mimesis or camouflage is highly effective when cryptic insects resemble closely the appropriate self-similar background, indicating the complexity of ecological relationships between insect mimics and their imitating models. When and how insects first evolved such an ingenious survival strategy is unclear. A Permian katydid exhibiting a mimicking pattern of wings similar to the modern relatives was considered the oldest case of insect mimicry (Garrouste et al., 2016). However, evidence for a contemporaneous mimetic relationship in this Permian deposit was scarce, and there was no quantitative or other useful data to track the mimetic interactions among the insect, model and predator. More recent cases of insect mimicry have been recorded from the Mesozoic, indicating the existence of several such effective survival strategies. As in morphological specializations involving masterly deceit found in modern insects, several Mesozoic insect taxa developed remarkable structural adaptations resulting in highly accurate resemblances to co-existing models (Wang et al., 2012; Wang et al., 2014; Yang et al., 2020). Prominent among these mimetic insects are Neuroptera (lacewings, antlions and relatives), a nonspeciose relic order consisting of ca. 6000 extant species that engaged in several, impressive instances of mimicry that reveal novel and specialized strategies of deception, of which many are absent today. Striking examples are the Jurassic lacewing Bellinympha (Saucrosmylidae), a compression fossil, mimicking cycadophyte leaves (Wang et al., 2010b), and larvae of the green lacewing Phyllochrysa (Chrysopidae) from amber, modified to resemble co-occurring liverworts (Liu et al., 2018). Besides mimicry, other deceptive modes of appearance have been documented among Mesozoic lacewings, such as camouflaged larvae of chrysopid (green lacewing) and myrmeleontoid (antlion relative) neuropterans in amber, which evolved distinctive debris-carrying behaviors to enhance their predatory effectiveness (Pérez-de la Fuente et al., 2012; Pérez-de la Fuente et al., 2018; Wang et al., 2016; Badano et al., 2018). These cases collectively have promoted understanding of the early evolution of insect mimicry, but also have revealed that the currently species poor Neuroptera had evolved a significant repertoire of specializations involving morphologies and behaviors that adapted to a variety of Mesozoic settings.

In this report, we found an exceptional system of the first lichen mimesis by a fossil lacewing. These occurrences are from the Daohugou 1 locality of Inner Mongolia in northeastern China. The new lichen-like-mimicking insects represent a new genus with two new species and exhibit remarkable wing patterns that accurately resemble the contemporaneous lichen species Daohugouthallus ciliiferus Wang, Krings et Taylor, 2010 (Wang et al., 2010a). The lichen affinity of the D. ciliiferus model previously was doubted due to the absence of evidence for fungal and algal connections that would indicate the presence of lichenization and thus the presence of a mutualistic symbiosis (Honegger et al., 2013; Lücking and Nelsen, 2018). Our SEM results corroborate the actual presence of hyphae connected to algal cells on the D. ciliiferus specimens, indicating the foliose and subfruticose lichen growth forms were in existence during the Middle Jurassic. Present-day lichen-mimicking insects are widely recorded among several diverse orders, especially Coleoptera (beetles), Lepidoptera (moths and butterflies) and Orthoptera (grasshoppers, katydids and crickets), which have evolved unusual specializations of morphology and behavior consistent with co-occurring lichens and other habitation- or appearance similar organisms such as liverworts (Gerson, 1973; Lücking, 2001; Capinera, 2008; Cannon, 2010; Lücking et al., 2010). An extraordinary orthopteran, the lichen dragon katydid from the modern Ecuadorian Andes, provides an excellent disguise of lichens (Braun, 2011). Other predatory and extant chrysopid larvae have a body mask adorned with affixed lichen fragments, an example of aggressive mimicry or the ‘wolf in sheep’s clothing’ syndrome (Skorepa and Sharp, 1971; Slocum and Lawrey, 1976; Wilson and Methven, 1997; Tauber et al., 2014). Importantly, lichen-mimetic or -camouflaged insects have established a specialized lichen-association for feeding or sheltering to obtain survival advantage (Gerson, 1973). Our finding documents the earliest lichen-mimicking insect and reveals that this strategy of mimicry among insects has been in existence for minimally 165 Mya. This ancient association also will provide new insight for exploring the predator–prey relationships among insects and lichens, and the role of habitat during mid-Mesozoic time.

The two new species of Lichenipolystoechotes exhibit a very similar appearance, but they easily can be separated by the distinct differences of branches of the MA and CuA veins. Lichenipolystoechotes species are conspicuous based on their highly prominent, homologous, pigmentation pattern of their forewings, which implies that these insects evolved a similar defensive strategy. The closest extant relatives of Lichenipolystoechotes are Ithonidae (moth lacewings), of which their ecological and biological features are poorly documented (New, 1989). The forewings of the two new species demonstrate a high similarity in their overall appearance, such as the forewing branching pattern (Figures 3A,E and 4A) that matches the thallus branches of the co-occurring foliose to subfruticose lichen Daohugouthallus ciliiferus (Figure 4B–D; Wang et al., 2010a). The entire forewing forms an irregular branching pattern amid rounded, diaphanous fenestrae (windows) that are distributed along the wing center and as U-shaped extensions occurring around the wing border. The pigmented branch pattern of the wings has uneven widths and is angulated outwardly. The variation in width of each forewing vein branch conforms well to the variation in width of the lichen’s branches, indicating a morphological similarity between the wing markings and lichen thallus (Figure 4F; Figure 4—figure supplement 1; Supplementary file 1: Table S1). Lichens often have punctiform pycnidia (asexual reproductive structures) with black spots appearing on their thallus, especially in extant foliose lichen families such as Parmeliaceae (Thell et al., 2012). In Daohugouthallus ciliiferus specimens, punctiform black spots occur, but whether they are pycnidia is uncertain. It is noteworthy that a specimen of L. ramimaculatus displays similar, scattered spots on its wings that resemble the dark spots on the lichen thallus of D. ciliiferus (Figure 4G–I), potentially strengthening the similarity between L. ramimaculatus and D. ciliiferus. Collectively, these details of insect morphology likely enhanced the similarity of the insect with a co-occurring lichen, providing a reasonable inference that the forewing is mimetic with the lichen thallus.

It is generally known that lichens are stable, symbiotic associations of fungi and algae (Lücking and Nelsen, 2018). At the same time, lichens are regarded as pioneers in the colonization of novel surfaces such as bark, rock and soil, which dominate about 7% of the earth's terrestrial surface (Larson, 1987), and have a distribution from the polar regions to the tropics (Lumbsch and Rikkinen, 2017). They are prominent in arctic-alpine vegetation types in wet and higher montane forests (Lumbsch and Rikkinen, 2017). Many extant foliose or fruticose lichens such as taxa of Parmeliaceae are known to be epiphytic or corticolous, and bark surfaces are one of the most common substrates (Lumbsch and Rikkinen, 2017). Daohugouthallus ciliiferus is considered an epiphytic foliose to subfruticose lichen, and often is found entangled with gymnosperm seed cones (Figures 1C and 4D; Wang et al., 2010a). When Lichenipolystoechotes moth lacewings reposed in a habitat rich in D. ciliiferus, a near perfect match of their appearances would assist their concealment. Among extant Neuroptera, similar appearances of lichen-camouflage or related cases have been recorded in some larvae of green lacewings that carry packets of lichen material on their backs to hide themselves (Slocum and Lawrey, 1976; Wilson and Methven, 1997). Although Lichenipolystoechotes probably lacked the same life-habit as modern lichen-carrying chrysopoid larvae, the Jurassic taxa likely acquired a similar survival advantage when they occupied a lichen-rich habitat. Some extant Thyridosmylus species of Osmylidae, another archaic lineage of Neuroptera, possess similar complex wing markings and often occur on moss-laden surfaces of rocks, tree bark and indurated soil surfaces (Winterton et al., 2017; Figure 2B), which exhibit an impressive consistency with their surroundings (pers. observ. by Yongjie Wang). Although Lichenipolystoechotes is a member of Ithonidae, phylogenetically distant to Osmylidae, we infer that their concealment strategy of mimicking cryptogam plants in certain habitats has a deep geochronologic history among ancient lacewing lineages.

Unlike the models of other, co-occurring, plant-mimicking insects, lichen-mimesis of Lichenipolystoechotes appears highly specialized (Figure 5). Modern lichens can produce a variety of lichenic acids (Gerson, 1973) that are unpalatable to many insects and enhance the protective sheltering for animals. Consequently, lichens and lichen-tolerant animals, such as lichen feeding insects and mites, constitute a unique micro-ecosystem. We hypothesize that such a micro-ecosystem existed 165 million-years-ago in Northeastern China that accommodated these trophic, sheltering, defensive and mimetic interactions. Although lichen mimesis is not well documented among extant insects, the most iconic such case of lichen and insect resemblance is the industrial melanism of the peppered moth Biston betularia in nineteenth century Britain (Gerson, 1973; Stevens, 2011). The Industrial Revolution caused elevated levels of soot laden air pollution that resulted in disappearance of lichen shelters for the light-colored morph of B. betularia, as their corresponding habitation sites were changed from lightly tinged to dark-hued lichen surfaces that led to their greater vulnerability to predation. This change resulted in the abrupt increase of the dark colored morph of B. betularia. When lightly hued lichens returned after aerial pollution was thwarted, B. betularia again became dominant as the lightly colored morph. The industrial melanism of B. betularia was believed as a textbook example of Darwinian evolution in action, though it was questioned by some authors (Sargent, 1968; Sargent, 1969; Coyne, 1998; Cook and Saccheri, 2013). Nevertheless, other studies demonstrated that selection pressures such as predation by birds genuinely affected the differential survival of the pale and dark colored morphs of B. betularia under differently hued backgrounds (Howlett and Majerus, 1987; Liebert and Brakefield, 1987; Majerus, 2009; Walton and Stevens, 2018). It is possible that the Jurassic Lichenipolystoechotes could have gained survival advantage from mimesis of a lichen similar to that of modern B. betularia–lichen mimesis. Specifically, if lichen models were present in the habitat occupied by Lichenipolystoechotes, survival of the mimic would be assured. It is noteworthy that the winged adults of Lichenipolystoechotes would not have been always in the shelter of a lichen model; however, when they were, the conditions of mating, laying of eggs and dispersal would be paramount for survival. If so, high-contrast lichen-like markings could contribute to concealment of the insects. Alternatively, such high-contrast markings of Lichenipolystoechotes species also can be interpreted as disruptive coloration, which would confuse the boundaries of moth lacewing and lichen to prevent the detection of a body part essential for survival (Stevens, 2011). Consequently, the lichen-like markings of Lichenipolystoechotes could likely bring the double protections to the insects-background mimicry and disruptive coloration.

Figure 5

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Was there possible benefit to D. ciliiferus from its mimetic association with Lichenipolystoechotes? This is an open question that could raise multiple alternative explanations. Some modern insects such as ants, dipterans and larva of green lacewings are considered to potentially contribute to dispersal of lichens by transporting lichen propagules to new sites of colonization (Gerson, 1973; Keller and Scheidegger, 2016; Ronnås et al., 2017). In a comparison with such relatively small, lichen-carrying insects, Lichenipolystoechotes possessed a considerably larger body size that likely was convenient for dispersal of lichen propagules. Notably, sexual reproductive organs such as apothecia have not been found on the D. ciliiferus thallus based on light-microscopic morphological and SEM anatomical observations; neither were vegetative propagules such as soredia or isidia seen except along marginal lobules that occasionally were present. This hypothesis of zoochory requires additional evidence for support. However, our alternative hypothesis of benefiting D. ciliiferus is based on trophic interactions. As predaceous insects, Lichenipolystoechotes inhabited a lichen-rich environment to evade their predators, but they also could have predated and consumed smaller lichen-feeding animals while simultaneously decreasing herbivore damage to the D. ciliiferus thallus. This latter hypothesis would require additional verification from evidence of a small ecological web of predator, shelter, defensive and mimetic interactions associated with Daohugouthallus and Lichenipolystoechotes in the same deposit.

The accepted oldest lichen fossil was reported from the Early Devonian and lichens have existed minimally for 410 million years (Taylor et al., 1995; Honegger et al., 2013; Lücking and Nelsen, 2018), as have the apterygote insects (Misof et al., 2014). Both archaic Devonian lineages have evolved more derived, diverse clades of lichens and pterygote insects resulting in a myriad of associations among their modern lineages (Figure 6). Although there is virtually no evidence to suggest when and how such association began; in this report, we describe the oldest examples of lichen mimesis that involved two lacewing species resembling a contemporaneous lichen from the same, latest Middle Jurassic deposit. These insect lineages have acquired mimicry association with lichens in less than half of the time (40%) of the duration of both major lineages since the early Devonian (Figure 6). This new finding documents a unique survival strategy among mid-Mesozoic Neuroptera, and others await discovery.

Figure 6

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All data generated or analysed during this study are included in the manuscript and supporting files.

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Thank you for submitting your article "Lichen mimesis in mid-Mesozoic lacewings" for consideration by eLife. Your article has been reviewed by George Perry as the Senior Editor, a Reviewing Editor, and three reviewers. The following individuals involved in review of your submission have agreed to reveal their identity: Robert Lücking (Reviewer #1); Enrique Peñalver (Reviewer #2).

The reviewers have discussed the reviews with one another and the Editor has drafted this decision to help you prepare a revised submission.

We would like to draw your attention to changes in our revision policy that we have made in response to COVID-19 (https://elifesciences.org/articles/57162). Specifically, when editors judge that a submitted work as a whole belongs in eLife but that some conclusions would require additional new data, as they do with your paper, we are asking that the manuscript be revised to limit claims to those supported by data in hand.

Summary:

This manuscript describes two new fossils of lacewings from the Jurassic, establishing a new genus. The wing pattern in these fossils strikingly mimics another fossil from the same stratum, interpreted by the authors as a lichen. The strengths of the manuscript lie in establishing this potential mimetic association, as well as the underlying analysis and rendering in the form of striking imagery and illustrations. The specimens studied are impressive in their fine preservation. Reviewers praised the work as an important discovery and research, writing that the new vegetal mimesis in Mesozoic insects is fascinating, and that it is a superb contribution to the knowledge of the paleobiology and evolution of the insects.

Essential revisions:

1) Consensus among reviewers was that the lichen affinity of Daohugouthallus ciliiferus was inadequately demonstrated. The authors do present micrographs to support their interpretation, but in my view, these are not convincing, as there is no clear evidence of hyphal structures. See for instance Honegger et al., 2013 for comparison. The authors also interpret the irregular dark dots as pycnidia but provide no sectional evidence, when pycnidia can clearly be identified by their internal anatomy, even in fossils older than 400 my (see Taylor et al., 1994 and Honegger et al., 2013). The evidence for Daohugouthallus being a lichen is at best inconclusive and with at least equal probability it could be a bryophyte or other lower plant. One important argument for Daohugouthallus being a bryophyte rather than a lichen is that these bryophyte morphotypes were around since the Devonian, whereas macrolichens with such a morphology did not evolve until after the K-Pg boundary, i.e. 100 my later than the fossil (see references in the annotations).

1a) For publication in eLife, we would require a much more careful assessment of the biological interpretation of Daohugouthallus. It is ok for the authors to state that they believe that this may be a lichen, but may also be something else. This does not detract from the strength of the paper, as interpretation of the mimesis does not depend on the biological interpretation of Daohugouthallus, but the discussion should be adjusted accordingly.

1b) However, this does mean that choice of the generic name Lichenipolystoechotes is over-speculative. Furthermore, reviewers felt that while the new genus can readily be assigned to the polystoechotid genus-group of Ithonidae, the polystoechotid genus-group is not a stable taxonomy taxon, and ID to the family level would be better.

1c) Related to this, at present non-paleobotanists would have difficulty interpreting Figure 4 and the associated discussion; expanded descriptions that potentially could include comparisons with extant correlates would benefit a broader range of readers as the authors developed their (cautious) belief.

1d) Finally, although this approach may be changed completely in revision, we note that it is not clear what the authors mean by "Supplemental Diagnosis". Diagnoses are very conservative elements in taxonomy. In theory, there could be a section named "Original diagnosis" containing exactly the original diagnosis to then comment on it in a subsequent section OR there could be an "Emended diagnosis" containing only the text of a diagnosis (with the correct elements of the original diagnosis mixed with new elements). That "Emended diagnosis" will be diagnosis of this taxon (as all other taxa new research could emended this emended diagnosis, etc.). Of course, after the emended diagnosis a subsequent section can explain the changes done or additions and their relevance. But in the current version of the manuscript, this section is an informal mixture of emended diagnosis and remarks and justification of the changes done.

2) Much of the Discussion section goes into details of extant lichen-related mimicry, mimesis and camouflage and is unrelated to the findings presented in the paper, and otherwise incorrectly interpreted. For instance, lichen mimesis is mostly found in insects that are otherwise not associated with lichens and only frequently co-occur in the same habitat, whereas lichen feeders usually do not exhibit lichen mimesis. There is also no known case where an insect mimicking a lichen would actually aid in its dispersal. Therefore, all this discussion is too speculative or tangential and the discussion should be limited to two aspects: whether Daohugouthallus is in fact a lichen and the evidence leading to the interpretation that the lacewings indeed mimic Daohugouthallus (whether lichen or not), plus giving a context of wing patterns in extant Neuroptera for alternative interpretations. Furthermore, lichens are not plants. Hence the elaboration of the topic of mimicry and mimesis based on plants is misleading. Also, lichens did not evolve into plants as stated at one point.

3) The authors do not offer alternative interpretations for banded wing patterns. These are quite common in diverse insects including extant Neuroptera, and also other animals, but they are not specifically interpreted as lichen mimesis. Rather, such banded patterns represent a general approach to camouflage, by "breaking" the actual shape of the animal. This should be discussed.

4) The relationship between punctiform pycnidia-like dark spots on the talli and minute spots in the wings is not very convincing and the authors could be more conservative in the presentation of this topic. It is difficult to conclude that the small spots in the wings were generated by natural selection during the evolution of this mimetic case when considering the comparative scales in respect to the diaphanous fenestrae with dark limits and these punctiform dark spots. Maybe, the minute spots were visually irrelevant (and also could be artifacts due to fossilization). Do the authors know if there are studies about the relevance of diverse elements of very different size in mimetic cases in extant biota?

5) The cited references require attention, both to ensure the inclusion of recent literature and to confirm that the cited work supports the topic discussed. Overall, a much more careful literature survey is required.

[Editors' note: further revisions were suggested prior to acceptance, as described below.]

Thank you for submitting your revised article "Lichen mimesis in mid-Mesozoic lacewings" for consideration by eLife. The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission.

Summary:

The reviewers felt that the new SEM data (which impressed us!) helped to make a now-sufficient case for interpretation as lichen mimesis. Most other essential revisions were also addressed.

Essential revisions:

We still believe that the discussion on the broader biological context of mimesis remains too far-reaching. This discussion is based on studies with extant organisms; while the authors present a fine example of extinct mimesis documented by fossils, there are no biological data to support the notion that any of the additional factors (e.g. feeding on lichens, lichen dispersal, impact of environmental changes on mimetic patterns) took place in these fossil taxa. Therefore, while it is fine to briefly mention these factors in a general summary paragraph on lichen mimesis, it is too strong to infer that any of these actually applied to the fossil example.

Essential revisions:

1) Consensus among reviewers was that the lichen affinity of Daohugouthallus ciliiferus was inadequately demonstrated. The authors do present micrographs to support their interpretation, but in my view, these are not convincing, as there is no clear evidence of hyphal structures. See for instance Honegger et al., 2013 for comparison. The authors also interpret the irregular dark dots as pycnidia but provide no sectional evidence, when pycnidia can clearly be identified by their internal anatomy, even in fossils older than 400 my (see Taylor et al., 1994 and Honegger et al., 2013). The evidence for Daohugouthallus being a lichen is at best inconclusive and with at least equal probability it could be a bryophyte or other lower plant. One important argument for Daohugouthallus being a bryophyte rather than a lichen is that these bryophyte morphotypes were around since the Devonian, whereas macrolichens with such a morphology did not evolve until after the K-Pg boundary, i.e. 100 my later than the fossil (see references in the annotations).

We fully understand the concerns of the reviewers, because the lichen affinity of Daohugouthallus ciliiferus is at the core of the proposed mimesis relationship. Indeed, the previous figures of Daohugouthallus ciliiferus did not adequately show the distinct structures of hyphae and algae. We conducted an additional SEM analysis of specimens of Daohugouthallus ciliiferus, and fortunately obtained a series of SEM figures that clearly illustrated the inner structure of Daohugouthallus ciliiferus. Our supplementary description, now added in subsection “Emended diagnosis” is:

“upper cortex conglutinate, comprising one cell layer, very thin, c. 1 μm thick (Figure 2A); algal cells globose to near globose, one-celled, mostly 1.5-2.1 μm in diameter, some in framboidal form, anastomosed (Figure 2A, B, F) by or adherent (Figure 2C–H) to the fungal hyphae with a simple wall-to-wall mycobiont-photobiont interface; fungal hyphae filamentous, some shriveled, septate (Figure 2B, C, G, H), 1.2-1.5 μm wide.”

Obviously, the bryophyte or other lower plants could be excluded for the possibility of having such an inner structure. Moreover, no typical bryophytic-grade reproductive structures of antheridia or archegonia were observed in our material.

The new results well match the criteria of the identification of lichen fossil as proposed by Lücking and Nelsen, (2018):

1) Presence of a mycobiont component recognizable as hyphae. The filamentous hyphae of D. ciliiferus is distinctly shown in Figure 2B–F;

2) Presence of a photobiont component in agreement with the morphology of undifferentiated, unicellular or filamentous microalgae. The algal cells of D. ciliiferus are shown by dark arrow in Figure 2C–F are structurally similar to Honegger et al.’s results, except for having a smaller size; and

3) A spatially correlated arrangement of both components in a way that suggests stable interaction in the form of an exosymbiosis. In Figure 2, especially in Figure 2B,C,E,F,H, it is clearly shown that algal cells are anastomosed or adherent to the fungal hyphae, which are very similar to Honegger et al.’s results (cf. Figure 4C,D,E).

Based on the new evidence, we are convinced that D. ciliiferus is a lichen. It is a pity that we did not obtain convincing structures of pycnidia, though we had tried repeatedly. We think this does not affect the lichen identity of D. ciliiferus, considering the solid evidence of hyphae and algae, and the frequent rarity of pycnidia in modern lichens. We deleted any corresponding statements of pycnidia in the revised text.

We admit that the discovery of a Jurassic macrolichen will be greatly challenge to the current knowledge on systematics and evolution of lichen. However, the fossil of D. ciliiferus are real and clearly corroborates the existence of a Jurassic macrolichen. We note that the fossil record of macrolichens is sparse and that 90 percent of fossil occurrences originate from Paleogene ambers (Lücking and Nelson, 2018). As for the significance of the oldest macrolichen and the evolution of lichen, it is beyond the scope of this paper, but it has been considered as our next project.

1a) For publication in eLife, we would require a much more careful assessment of the biological interpretation of Daohugouthallus. It is ok for the authors to state that they believe that this may be a lichen, but may also be something else. This does not detract from the strength of the paper, as interpretation of the mimesis does not depend on the biological interpretation of Daohugouthallus, but the discussion should be adjusted accordingly.

See the details see the above-mentioned comment. Indeed, there were some improper statements in the original paper, and we have made relevant modifications in the revised text.

1b) However, this does mean that choice of the generic name Lichenipolystoechotes is over-speculative. Furthermore, reviewers felt that while the new genus can readily be assigned to the polystoechotid genus-group of Ithonidae, the polystoechotid genus-group is not a stable taxonomy taxon, and ID to the family level would be better.

Lichenipolystoechotes is a typical polystoechotid insect within Ithonidae, based on the particular characters of its venation. Recently, ‘Polystoechotidae’ was synonymized with Ithonidae, as discussed by Winterton and Makarkin, 2010. But this synonymization did not resolve relationships within Ithonidae, and whether Polystoechotinae is a subfamily of Ithonidae, or of some lower rank. As the polystoechotid genus-group was tentatively used for previous fossil ‘polystoechotid lacewings’, our assignment of Lichenipolystoechotes is nomenclaturally valid at the family level as a member of Ithonidae.

1c) Related to this, at present non-paleobotanists would have difficulty interpreting Figure 4 and the associated discussion; expanded descriptions that potentially could include comparisons with extant correlates would benefit a broader range of readers as the authors developed their (cautious) belief.

Figure 4 was intended to present the comparisons of wing patterns of Lichenipolystoechotes species and the thalli of Daohugouthallus specimens. In addition to the overall details in the likenesses of the wing pattern and lichen thallus, a quantitative method was used to measure the variation of branch widths of forewing pattern and lichen thalli to further analytically assess their similarity. In the results, the variation of branch widths of L. ramimaculatus’s forewing pattern is well in accord with the variation of lichen thalli (Figure 4F, Figure 4—figure supplement 1; Supplementary file 1). We provided the supplement explanations of Figure 4 in both the Discussion section and Materials and methods section of the main text.

1d) Finally, although this approach may be changed completely in revision, we note that it is not clear what the authors mean by "Supplemental Diagnosis". Diagnoses are very conservative elements in taxonomy. In theory, there could be a section named "Original diagnosis" containing exactly the original diagnosis to then comment on it in a subsequent section OR there could be an "Emended diagnosis" containing only the text of a diagnosis (with the correct elements of the original diagnosis mixed with new elements). That "Emended diagnosis" will be diagnosis of this taxon (as all other taxa new research could emended this emended diagnosis, etc.). Of course, after the emended diagnosis a subsequent section can explain the changes done or additions and their relevance. But in the current version of the manuscript, this section is an informal mixture of emended diagnosis and remarks and justification of the changes done.

We sincerely appreciate the rigorous review from the reviewer and Editor that address this question. In the text, we have added new evidence of the presence of hyphae and algae within the Daohugouthallusciliiferus structure, which corroborates its lichen affinity. However, in our view, a ‘Supplemental Diagnosis’ should be used when there are major errors in the original diagnosis. Rather, we have combined the mixed contents of elements of the original diagnosis with our supplementary elements into subsection “Emended diagnosis” and have used the subsection “Remarks” to explain these new findings.

2) Much of the Discussion section goes into details of extant lichen-related mimicry, mimesis and camouflage and is unrelated to the findings presented in the paper, and otherwise incorrectly interpreted. For instance, lichen mimesis is mostly found in insects that are otherwise not associated with lichens and only frequently co-occur in the same habitat, whereas lichen feeders usually do not exhibit lichen mimesis. There is also no known case where an insect mimicking a lichen would actually aid in its dispersal. Therefore, all this discussion is too speculative or tangential and the discussion should be limited to two aspects: whether Daohugouthallus is in fact a lichen and the evidence leading to the interpretation that the lacewings indeed mimic Daohugouthallus (whether lichen or not), plus giving a context of wing patterns in extant Neuroptera for alternative interpretations. Furthermore, lichens are not plants. Hence the elaboration of the topic of mimicry and mimesis based on plants is misleading. Also, lichens did not evolve into plants as stated at one point.

First, we should express our thanks for the reviewers’ critical comments that provided some new ideas to improve this paper. The mimicry cases of fossil insects are scarce, and most cases belong to vascular plant mimicry (absence of lichen mimicry). Thus, when we introduce an overview of relevant modern mimicry, plant mimicry was necessarily mentioned. We agree with the reviewer’s criticism that the ‘plant’ was incorrectly used in some places, and we had corrected this in the revised text.

As for the taxonomic attribution of Daohugouthallus, it was discussed in Issue 1 above.

As for the lichen mimesis of insects, we consider it should represent a structural specialization of insects to adapt to the lichen-covered backgrounds. When one insect possessing lichen-like pattern rests on an appropriate, lichen-covered background, we maintain that insects could obtain the survival advantages from this relationship, as Lichenipolystoechotes undoubtedly did. Consequently, such an association can validly be treated as a lichen mimesis. Of course, not all insects interacting with lichens evolve into lichen mimics, and correspondingly they can evolve other biological or behavioral adaptations for survival. We have provided hopefully some clarity in explaining this in the revised paper.

With regard to assistance in the dispersal of the lichen by Lichenipolystoechotes, we have noted extant cases, sourced in the literature, where insects such as lichen-feeding ants and lichen-camouflaged larva of lacewings, could contribute to the dispersal of lichens through the transportation of propagules. As Jurassic Lichenipolystoechotes were winged insects that frequented lichens, we infer that considerable potential was present to contribute to lichen dispersal, akin to extant insects. We agree with the reviewer’s criticism that there is no direct evidence to support this, and we have adjusted this section in the revised paper to reflect this concern. Nevertheless, we aver that our inference of the possibility of such an association is valid.

3) The authors do not offer alternative interpretations for banded wing patterns. These are quite common in diverse insects including extant Neuroptera, and also other animals, but they are not specifically interpreted as lichen mimesis. Rather, such banded patterns represent a general approach to camouflage, by "breaking" the actual shape of the animal. This should be discussed.

This is an important suggestion. The wing markings of Lichenipolystoechotes have a very distinctive condition of (i) banding paralleling longitudinal veins, (ii) particularly shaped diaphanous fenestrae, (iii) a unique distribution of colors and hues, and other features that are quite different than ordinary, run-of-the-mill wing banding in fossil and extant Neuroptera. Nevertheless, we have added alternative explanations in the revised text.

4) The relationship between punctiform pycnidia-like dark spots on the talli and minute spots in the wings is not very convincing and the authors could be more conservative in the presentation of this topic. It is difficult to conclude that the small spots in the wings were generated by natural selection during the evolution of this mimetic case when considering the comparative scales in respect to the diaphanous fenestrae with dark limits and these punctiform dark spots. Maybe, the minute spots were visually irrelevant (and also could be artifacts due to fossilization). Do the authors know if there are studies about the relevance of diverse elements of very different size in mimetic cases in extant biota?

We initially suspected these spots likely to be pycnidia. However, the evidence to reflect that these spots were pycnidia could not be obtained. We agreed with the reviewer’s comments and have accordingly adjusted the revised text.

5) The cited references require attention, both to ensure the inclusion of recent literature and to confirm that the cited work supports the topic discussed. Overall, a much more careful literature survey is required.

We accepted the criticism of the reviewers, and the references have been checked out and updated.

[Editors' note: further revisions were suggested prior to acceptance, as described below.]

Essential revisions:

We still believe that the discussion on the broader biological context of mimesis remains too far-reaching. This discussion is based on studies with extant organisms; while the authors present a fine example of extinct mimesis documented by fossils, there are no biological data to support the notion that any of the additional factors (e.g. feeding on lichens, lichen dispersal, impact of environmental changes on mimetic patterns) took place in these fossil taxa. Therefore, while it is fine to briefly mention these factors in a general summary paragraph on lichen mimesis, it is too strong to infer that any of these actually applied to the fossil example.

We understand the reviewer’s concern. Among studies of fossils, methodologically it is common to reconstruct or infer the biologies, behaviors, and ecological associations of the past organisms based on what we know about living descendant lineages, as well as the available evidence from the fossils themselves. This is the subject matter of paleoecology; and it includes various lines of evidence, such as functional morphology, trace fossils associated with the behaviors of their makers, evidence of various types of interactions among fossils (herbivory, pollination and mimicry come to mind), but also includes ecological uniformitarianism—that the ecologies of modern lineages are relevant for understanding the biologies of their ancestors in those same lineages. To illustrate this latter point, how would one interpret the prolonged saber-like teeth of an extinct lineage of cat-like carnivores, such as Smilodon, without assessing similar developments of such teeth (albeit less extreme) in various modern carnivores? This is a common principle in paleoecology; otherwise, the interpretation of the fossil record becomes a useless exercise since the species we are attempting to understand are not extant. Our reconstruction of the ecology of the fossil should be considered as a hypothesis to be tested from additional evidence. Our inference of “additional factors” is based on deductive reasoning that is informed by ideas, assumptions, general principals and facts, and is presented as a hypothesis to be tested with additional fossil and modern material. We judge that it is necessary to present additional ideas, albeit some based on inference, to our audience in understanding our finding in a broader ecological context. Consequently, we have conditioned our interpretations by presenting them as a hypothesis for further testing. The major modifications were listed as follows:

1) Because we did not obtain definitive evidence for lichen propagules and lichen damage, we modified the corresponding statements about feeding on lichens and lichen dispersal in the revised manuscript. As mentioned in the previous revised version of the manuscript, we considered that the existence of Jurassic lichens probably was supported by the presence of a confined ecological web that would require documentation of lichens and their mimics, and other trophic or trophic-related interactions, as is the case among extant lichen–mimicry–insect webs (another example of ecological uniformitarianism). However, documentation of such a micro-ecological web would require additional evidence.

There is another point to be made in the above context. We note that in paleontology, the oldest known occurrence of a fossil almost always is not the earliest actual occurrence of that fossil. This is due to the vagaries of the fossil record, lack or interest or the number of practitioners of the particular fossil group in question, or mistakes in taxonomic identifications. It is almost certain that there are lichens that are older than the Jurassic. We would like to assert that the previous absence of Jurassic lichens is not a valid reason for establishing the existence of Jurassic lichens, should the fossil record provide positive evidence. We will continue to explore for the presence of Jurassic lichens, and it is hoped that more evidence will be found.

2) As for the “impact of environmental changes on mimetic patterns” passage, this statement had been deleted in the revised manuscript. Because the function of lichen mimesis in Lichenipolystoechotes is virtually same as that of Biston betularia, we cited the classic case to stress the importance of lichen mimesis in a modern context. Accordingly, it would have been easier for an audience to understand our findings.

Author details

1. Hui Fang

   1. College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China
   2. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington DC, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

2. Conrad C Labandeira

   1. College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China
   2. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington DC, United States
   3. Department of Entomology, University of Maryland, College Park, United States

   Contribution

   Conceptualization, Supervision, Validation, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

3. Yiming Ma

   College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China

   Contribution

   Investigation, Visualization, Writing - original draft

   Competing interests

   No competing interests declared

4. Bingyu Zheng

   College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China

   Contribution

   Investigation, Visualization, Methodology, Writing - original draft

   Competing interests

   No competing interests declared

5. Dong Ren

   College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Validation, Investigation, Project administration

   Competing interests

   No competing interests declared

6. Xinli Wei

   State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China

   Contribution

   Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing - review and editing

   For correspondence

   weixl@im.ac.cn

   Competing interests

   No competing interests declared

7. Jiaxi Liu

   College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China

   Contribution

   Conceptualization, Resources, Supervision, Validation, Investigation, Project administration

   For correspondence

   liu-jiaxi@263.net

   Competing interests

   No competing interests declared

8. Yongjie Wang

   College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, China

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Visualization, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   wangyjosmy@foxmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1397-8481

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