Lichen mimesis in mid-Mesozoic lacewings

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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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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