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. 2020 Jul 29:9:e59007.
doi: 10.7554/eLife.59007.

Lichen mimesis in mid-Mesozoic lacewings

Hui Fang  1   2 , Conrad C Labandeira  1   2   3 , Yiming Ma  1 , Bingyu Zheng  1 , Dong Ren  1 , Xinli Wei  4 , Jiaxi Liu  1 , Yongjie Wang  1
Affiliations

Lichen mimesis in mid-Mesozoic lacewings

Hui Fang et al. Elife. .

Abstract

Animals mimicking other organisms or using camouflage to deceive predators are vital survival strategies. Modern and fossil insects can simulate diverse objects. Lichens are an ancient symbiosis between a fungus and an alga or a cyanobacterium that sometimes have a plant-like appearance and occasionally are mimicked by modern animals. Nevertheless, lichen models are almost absent in fossil record of mimicry. Here, we provide the earliest fossil evidence of a mimetic relationship between the moth lacewing mimic Lichenipolystoechotes gen. nov. and its co-occurring fossil lichen model Daohugouthallus ciliiferus. We corroborate the lichen affinity of D. ciliiferus and document this mimetic relationship by providing structural similarities and detailed measurements of the mimic's wing and correspondingly the model's thallus. Our discovery of lichen mimesis predates modern lichen-insect associations by 165 million years, indicating that during the mid-Mesozoic, the lichen-insect mimesis system was well established and provided lacewings with highly honed survival strategies.

Keywords: ecology; evolutionary biology; fossil; insect; lichen; mimicry; neuroptera; survival strategy.

Plain language summary

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.

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Conflict of interest statement

HF, CL, YM, BZ, DR, XW, JL, YW No competing interests declared

Figures

Figure 1.
Figure 1.. Photos of the lichen Daohugouthallus ciliiferus Wang, Krings et Taylor, 2010.
(A) Specimen B0476P, with arrows indicating the lobules. (B) Specimen CNU-LICHEN-NN2019001, with arrows indicating the lobules. (C) Specimen CNU-LICHEN-NN2019002P. Scale bars: 5 mm in A–C.
Figure 2.
Figure 2.. Scanning electron microscopy (SEM) micrographs of lichen fossil (CNU-LICHEN-NN2019001).
(A) Thallus longitudinal section containing the cortex, with white arrows pointing to the fungal hyphae, and black ones to the algal cells. The fungal hyphae are interweaved with algal cells. (B–D, F–H) Fungal hyphae indicated by white arrows; algal cells are indicated by black arrows showing entanglement and encirclement by fungal hyphae; septa shown in B, C, G, H. (E) One algal cell indicated by the black arrow, displaying adherence to other fungal hyphae indicated by the white arrow. Scale bars: 5 μm in A, C, D, G, H; 10 μm in B; 3 μm in E; 4 μm in F.
Figure 3.
Figure 3.. Photos and line drawings of Lichenipolystoechotes angustimaculatus gen. et sp. nov., and L. ramimaculatus gen. et sp. nov.
(A–C) Holotype CNU-NEU-NN2016040P/C of L. angustimaculatus, photo of part in (A). Accompanying overlay drawing in (B). Photo of counterpart in (C). (D) Photo of the paratype CNU-NEU-NN2016041 of L. angustimaculatus. (E–H) The holotype CNU-NEU-NN2019006P/C of L. ramimaculatus, with a lichen mimicking forewing pattern. Photo of part in (E); accompanying overlay drawing in (F); photo of counterpart in (G); and accompanying overlay drawing in (H). Scale bars: 5 mm in A–H.
Figure 4.
Figure 4.. The lichen mimicking lacewing Lichenipolystoechotes ramimaculatus gen. et sp. nov. and L. angustimaculatus gen. et sp. nov., and fossils of the contemporaneous lichen Daohugouthallus ciliiferus Wang, Krings et Taylor, 2010.
(A) Photo of part of L. ramimaculatus, with a lichen mimicking forewing pattern, CNU-NEU-NN2019004P. (B–C) Photos of the lichen thallus D. ciliiferus, PB23120; thallus segment in (B); and entire thallus in (C). Photos A–C are at the same scale. (D) Photo of a nearly intact lichen thallus of D. ciliiferus, B0474. (E) Photo of L. angustimaculatus with a lichen mimicking wing pattern; CNU-NEU-NN2016040P. (F) Box scatter plots of measurement data displaying lower and upper extremes, lower and upper quartile, median and average (in the blue dotted line) of branch widths of L. ramimaculatus’s forewing pattern (CNU-NEU-NN2019004C) and thallus branch widths of lichen D. ciliiferus (PB23120, B0474) separately. (Black, red and green dots represent measurement results of branch pattern widths of lichen-mimicking lacewing and thallus widths of the two lichen specimens, respectively.) (G) Part of the wing pattern of L. ramimaculatus, with irregular wing spots. (H, I) Portion of the thallus of D. ciliiferus, with irregular spot-like punctiform pycnidia, B0474 (H), B0476P (I) The dark arrows indicate the spots on wing of L. ramimaculatus and thallus of D. ciliiferus. Scale bars: 5 mm in A–E, 1 mm in G–I.
Figure 4—figure supplement 1.
Figure 4—figure supplement 1.. Measuring lines on lichen-mimicking L. ramimaculatus and lichen D. ciliiferus.
(A) Measuring lines on the forewing of lichen-mimicking L. ramimaculatus, CNU-NEU-NN2019004P. (B) Measuring lines on lichen specimen PB23120. (C) Measuring lines on lichen specimen B0474. Measuring lines are indicated by their red color. Scale bars: 5 mm in A–C.
Figure 5.
Figure 5.. Habitus reconstruction of the lichen mimicking lacewing Lichenipolystoechotes ramimaculatus gen. et sp. nov. on the lichen Daohugouthallus ciliiferus Wang, Krings et Taylor, 2010.
The colors used in the drawing of D. ciliiferus is Taupe, referring to the color of extant lichen Everniastrum cirrhatum. The body of the L. ramimaculatus is reconstructed based on living ithonid species, and the wing is based on the fossil of holotype CNU-NEU-NN2019006P/C. The color of insect is yellowish-brown based on the general coloration of extant polystoechotids. Xiaoran Zuo did the reconstruction drawing.
Figure 6.
Figure 6.. Lichen mimicry and camouflage by insects across major insect lineages.
Time-dated chronogram based on Misof et al., 2014. Specific examples of fossil and modern lichen mimesis by various insect taxa are provided at right. Black dots represent modern insect–lichen-mimetic associations; the star represents the fossil Lichenipolystoechotes–lichen mimicry of this study.
See this image and copyright information in PMC

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