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Early evolution of beetles regulated by the end-Permian deforestation

  1. Xianye Zhao
  2. Yilun Yu
  3. Matthew E Clapham
  4. Evgeny Yan
  5. Jun Chen
  6. Edmund A Jarzembowski
  7. Xiangdong Zhao
  8. Bo Wang  Is a corresponding author
  1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, China
  2. University of Chinese Academy of Sciences, China
  3. Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, China
  4. Department of Earth and Planetary Sciences, University of California, Santa Cruz, United States
  5. Palaeontological Institute, Russian Academy of Sciences, Russian Federation
  6. Institute of Geology and Paleontology, Linyi University, China
  7. Department of Earth Sciences, Natural History Museum, United Kingdom
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Cite this article as: eLife 2021;10:e72692 doi: 10.7554/eLife.72692

Abstract

The end-Permian mass extinction (EPME) led to a severe terrestrial ecosystem collapse. However, the ecological response of insects—the most diverse group of organisms on Earth—to the EPME remains poorly understood. Here, we analyse beetle evolutionary history based on taxonomic diversity, morphological disparity, phylogeny, and ecological shifts from the Early Permian to Middle Triassic, using a comprehensive new dataset. Permian beetles were dominated by xylophagous stem groups with high diversity and disparity, which probably played an underappreciated role in the Permian carbon cycle. Our suite of analyses shows that Permian xylophagous beetles suffered a severe extinction during the EPME largely due to the collapse of forest ecosystems, resulting in an Early Triassic gap of xylophagous beetles. New xylophagous beetles appeared widely in the early Middle Triassic, which is consistent with the restoration of forest ecosystems. Our results highlight the ecological significance of insects in deep-time terrestrial ecosystems.

Editor's evaluation

The study proposes a new evolutionary-ecological scenario for Late Paleozoic and early Mesozoic beetles, supported by the summary of all available knowledge about early beetle fossils, including analyses of their taxon and morphological diversity and phylogenetic relationships. The effects of xylophagous beetles during the Paleozoic may have played a fundamental role in global biochemical cycles. The results advance our understanding of the evolutionary success of beetles and the many ways in which large environmental changes may affect biodiversity in general.

https://doi.org/10.7554/eLife.72692.sa0

Introduction

The end-Permian mass extinction (EPME; approximately 252 million years ago) was the most severe extinction event in the Phanerozoic (Benton and Newell, 2014). The EPME was primarily caused by the eruption of the Siberian flood basalts (Burgess and Bowring, 2015; Fielding et al., 2019), which generated excessive emissions of thermogenic methane, CO2, and SO2 that cascaded rapid global warming (Wu et al., 2021; Black et al., 2018), oceanic acidification and anoxia/euxinia (Schobben et al., 2020), aridification and other shifts in the hydrological cycle (Sun et al., 2012), acid rain (Black et al., 2014), wildfires (Shen et al., 2011), and ozone destruction (Benca et al., 2018). The response of terrestrial ecosystems to the EPME is quite heterogeneous, probably due to biotic, topographic, and latitudinal differences (Fielding et al., 2019; Zhao et al., 2020; Dal Corso et al., 2020). Moreover, how terrestrial ecosystems were affected during the EPME is still highly controversial (Benton and Newell, 2014; Gastaldo, 2019). Terrestrial tetrapods and plants are considered to have been severely affected by the EPME mostly based on diversity and taxonomic composition (Benton and Newell, 2014; Viglietti et al., 2021); however, such mass extinction was questioned by a more comprehensive dataset of plant macro- and microfossils (Gastaldo, 2019; Nowak et al., 2019). Similarly, Permian insects are thought to have suffered a significant extinction (Labandeira and Sepkoski, 1993; Béthoux et al., 2005; Labandeira, 2005; Condamine et al., 2020; Condamine et al., 2016), but this was not supported by other molecular phylogenetic and fossil record analyses (Ponomarenko, 2016; Dmitriev et al., 2018; Montagna et al., 2019; Schachat et al., 2019). In addition, the ecological response of insects to the EPME remains poorly understood (Benton and Newell, 2014; Schachat et al., 2021).

Beetles (Coleoptera) are the most speciose group of extant insects (Stork, 2018), with a stratigraphic range dating back to at least the lowest Permian (Ponomarenko, 2016; Kirejtshuk et al., 2013). They have a rich fossil record since the Permian and display a wide array of lifestyles (Figure 1; Ponomarenko, 1969; Ponomarenko, 2003). Their fossil record thus offers a unique and complementary perspective for studying the ecological response of insects to the EPME. The evolutionary history of Coleoptera has been widely investigated through molecular phylogenetic analyses (Condamine et al., 2016; McKenna et al., 2019; Zhang et al., 2018), morphological phylogenetic analyses (Beutel et al., 2008; Beutel et al., 2019), and fossil record analyses (Ponomarenko, 2003; Ponomarenko, 2016; Smith and Marcot, 2015). Although a long-term Palaeozoic-Mesozoic turnover of beetle assemblages is supported by almost all analyses, the detailed ecological response to the EPME and its explanatory mechanisms remain unclear. Most of the Permian and Triassic beetles belong to stem groups (extinct suborders or families; Figure 1), and thus they show character combinations and evolutionary history that cannot be inferred or predicted from phylogenetic analysis of modern beetles. In particular, two problems were ignored by previous analyses. First, phylogenetic relationships of some key fossils remain poorly resolved, particularly in their evolutionary relationships to modern taxa. Second, there are two complementary taxonomic systems for Permian and Triassic beetles: one is artificial formal taxa (based on isolated elytra that cannot be definitely classified into any natural group), and the other is the natural taxonomy (commonly based on more complete fossils including bodies and elytra). The formal taxa, like trace fossil taxa, lack comprehensive phylogenetic data (Ponomarenko, 2004), and thus they cannot be used unreservedly for biodiversity and phylogenetic analyses, but can be helpful in the morphospace analysis. These issues cloud the temporal resolution of coleopteran biodiversity in deep time and complicate the evolutionary trajectory of beetles but can be overcome through a combination of multiple analytical methods. Therefore, taxonomic diversity, morphological disparity, and ecological shifts are best evaluated jointly to better understand how the EPME has shaped the evolutionary history of beetles.

Examples of Permian beetles.

(A and B) Tshekardocoleidae, Moravocoleus permianus Kukalová, 1969, photograph and reconstruction. (C and D) Permocupedinae, Permocupes sojanensis Ponomarenko, 1969, photograph and reconstruction. (E) Tshekardocoleidae, Sylvacoleus richteri Ponomarenko, 1963, elytra photograph. (F) Taldycupedinae, Taldycupes reticulatus Ponomarenko, 1969, elytra photograph. Scale bars represent 1 mm.

Here, we compile an updated database of beetles from the Early Permian to Middle Triassic based on the taxonomic revision of fossils (including formal taxa). We analyse the evolution of taxonomic diversity, morphological disparity, and palaeoecological shifts of beetles from the Early Permian to Middle Triassic through phylogenetic and palaeoecological reconstructions and morphospace analyses of fossil material. Our results suggest that xylophagous (feeding on or in wood) beetles probably played a key and underappreciated role in the Permian carbon cycle and that the EPME had a profound ecological influence on beetle evolution. These results provide new insights into the ecological role of insects in deep-time terrestrial ecosystems and the ecological response of insects to deforestation and global warming.

Results

Taxonomic diversity

We compiled an updated database of beetles (21 families, 125 genera, and 299 species) from the Early Permian to Middle Triassic based on the taxonomic revision of natural and formal taxa (Figure 2—source data 1). Our database contains 18 families, 109 genera, and 220 species of natural taxa. There is a steady increase of families from the Early Permian to Middle Triassic, which is consistent with the result of Smith and Marcot, 2015, whose analyses were only conducted at the family level. The diversity of natural taxa displays almost the same trajectory at both species and genus levels (Figure 2C and E). The diversity is roughly stable in the Early Permian (Cisuralian), mainly represented by Tshekardocoleidae (Figure 1), increases rapidly in the Middle Permian (Guadalupian) and Late Permian (Lopingian), with the rise of the major clades Permocupedidae (Permocupedinae and Taldycupedinae) and Rhombocoleidae. Subsequently, it plunges in the Early Triassic and recovered gradually from the Anisian (early Middle Triassic). In the Ladinian (late Middle Triassic), the diversity clearly exceeds that of the Late Permian (Figure 2C and E). From the Middle Triassic, the Permian coleopteran assemblage characterized by Tshekardocoleidae, Permocupedidae, and Rhombocoleidae is completely replaced by a Triassic assemblage dominated by Cupedidae, Phoroschizidae and Triaplidae.

Figure 2 with 1 supplement see all
Diversity of Coleoptera from the Early Permian to Middle Triassic.

Natural taxa and mixed taxa (natural taxa and formal taxa) are counted at family, genus, and species levels separately. (A) Family-level diversity of natural taxa. (B) Family-level diversity of mixed taxa. (C) Genus-level diversity of natural taxa. (D) Genus-level diversity of mixed taxa. (E) Species-level diversity of natural taxa. (F) Species-level diversity of mixed taxa. Abbreviations: P1, Early Permian; P2, Middle Permian; P3, Late Permian; T1, Early Triassic; T2, Middle Triassic.

Our database also contains 3 families, 17 genera, and 79 species of formal taxa. A considerable proportion of Permian beetles belong to such taxa (Permosynidae, Schizocoleidae, and Asiocoleidae). These formal taxa mostly belong to stem groups, but some should probably be attributed to the two extant suborders Adephaga and Polyphaga. Both species and genus-level diversities of formal taxa show a gradual increase from the Middle to Late Permian, but decrease distinctly from the Triassic (Figure 2—figure supplement 1). The mixed taxa diversity (combining natural and formal taxa) displays the same trajectory to that of natural taxa at both species and genus levels (Figure 2D and F).

Phylogeny

We carried out a phylogenetic analysis based on 93 adult and larval characters across 15 natural taxa representing all natural families of Coleoptera from the Early Permian to Middle Triassic (Figure 3—source data 1). Our parsimony analysis result is consistent with a previous analysis (Beutel et al., 2008), and confirms that Tshekardocoleidae, Permocupedidae (Permocupedinae and Taldycupedinae), and Rhombocolediae are the stem group of Coleoptera (Figure 3A, Figure 3—figure supplement 1).

Figure 3 with 1 supplement see all
Ecological shifts of Coleoptera from the Early Permian to Middle Triassic.

(A) Simplified phylogeny of Coleoptera from the Early Permian to Middle Triassic. Thick lines indicate the known extent of the fossil record. The branches representing stem groups are shown in red. The ‘dead clade walking’ pattern is symbolized by the dashed line. For details of the phylogenetic analysis, see Figure 3—figure supplement 1. (B) Genus percentage of xylophagous groups from the Early Permian to Middle Triassic. Yellow graded band represents the ‘coal gap’.

Figure 3—source data 1

Character state matrix for the phylogenetic analysis.

https://cdn.elifesciences.org/articles/72692/elife-72692-fig3-data1-v2.xlsx

Morphological disparity

We chose beetle elytra—hardened forewings primarily serving as protective covers for the hindwings and body underneath—to perform the morphological disparity analysis for three reasons: (1) elytra are the most commonly preserved fossils of Palaeozoic and Mesozoic beetles, and they are easily accessible in the literature and in online databases; (2) Permian and Triassic elytra display complex morphological structure (Ponomarenko, 1969); (3) elytra morphology has long been studied in relation to taxonomic diversity of living and extinct beetles (Ponomarenko, 2004; Tong et al., 2021).

We assembled two discrete character matrices (at species and genus levels) based on 35 characters of 197 genera and 346 species (including undetermined species and unnamed specimens) for morphological disparity analyses (Figure 4—source data 1). The taxa were ordinated into a multivariate morphospace using both principal coordinates analysis (PcoA) and non-metric multidimensional scaling (NMDS) with two distance metrics, including the generalized Euclidean distance (GED) and maximum observable rescale distance (MORD). We chose both sum of variance (sov) and product of variance (pov) as the proxy for morphological disparity due to their robustness in sample size (Simões et al., 2020). The use of discrete characters produces results that have non-metric properties, but this approach can be used to elucidate broad patterns of similarities and clustering within multidimensional space (Lloyd, 2016; Deline et al., 2018).

The patterns of morphospace occupation of beetles in different time-bins are shown in three-dimensional plots delimited by combinations of the first three axes of the PcoA and NMDS results based on MORD metrics (Figure 4A, Figure 4—figure supplement 1). The morphological disparity results of two ordination methods within the MORD and GED matrix shows the same trajectory at both genus and species levels. The evolutionary pattern of morphological disparity is robust in different disparity metrics. Disparity is low in the Early Permian, with a significant increase during the Middle Permian. It is roughly stable in the Middle and Late Permian, subsequently showing a distinct plunge in the Early Triassic, slightly recovering in the Middle Triassic but is still significantly lower than in the Middle and Late Permian (Figure 4, Figure 4—figure supplements 18).

Figure 4 with 8 supplements see all
Morphospace comparisons of Coleoptera from the Early Permian to Middle Triassic.

(A) Morphospace three-dimensional (3D) plot ordinated by principal coordinates analysis (PcoA), maximum observable rescale distance (MORD) matrices, based on species-level dataset. (B and C) Disparity comparisons ordinated by PcoA, MORD matrices, based on species-level dataset, proxy by pov and sov. Abbreviations: pov, product of variance; sov, sum of variance; P1, Early Permian; P2, Middle Permian; P3, Late Permian; T1, Early Triassic; T2, Middle Triassic.

Figure 4—source data 1

Fossil character matrix for the morphospace analysis.

https://cdn.elifesciences.org/articles/72692/elife-72692-fig4-data1-v2.xlsx
Figure 4—source data 2

Result of permutation test for morphological disparity.

https://cdn.elifesciences.org/articles/72692/elife-72692-fig4-data2-v2.xlsx

Discussion

Our results demonstrate that beetles display a steady accumulation of taxonomic diversity throughout the Permian (Figure 2). The earliest definite beetles are Tshekardocoleidae (including the genus Coleopsis) from the Early Permian of Germany, Czech Republic, USA, and Russia (Figure 1), although the origin of Coleoptera is dated to the Carboniferous by molecular phylogenetic analysis (McKenna et al., 2019; Zhang et al., 2018; Toussaint et al., 2016). The coleopteran diversity radiation in the Middle Permian is consistent with an expansion of morphological disparity, corresponding to the appearance of multiveined, smooth, and striate elytra as well as some other patterns (Figure 4, Figure 4—figure supplement 1). Taxonomic diversity and morphological disparity were decoupled during the Late Permian when taxonomic diversity increased but morphological disparity was almost stable (Figures 2 and 4). The abrupt Middle Permian increase of coleopteran morphological disparity conforms to the early burst model of clade disparity commonly arising early in radiations (Simões et al., 2020; Hughes et al., 2013).

The Permian coleopteran assemblage was dominated by stem groups including Tshekardocoleidae, Permocupedidae (Permocupedinae and Taldycupedinae), and Rhombocolediae in terms of richness and abundance. These ancient beetles were most likely xylophagous because they display a prognathous head, a characteristic elytral pattern with window punctures, a cuticular surface with tubercles (or scales), and a plesiomorphic pattern of ventral sclerites, very similar to the extant wood associated archostematans (Figure 1; Kirejtshuk et al., 2013; Ponomarenko, 1969). Moreover, Permian trace fossils showing wood boring provide convincing evidence for the xylophagous habit of these ancient beetles (Naugolnykh and Ponomarenko, 2010; Feng et al., 2019). Aquatic or semi-aquatic beetles including Phoroschizidae and Ademosynidae, belonging to the suborder Archostemata, first appeared in the Middle Permian and diversified in the Late Permian (Ponomarenko, 2003). The three other suborders of Coleoptera, comprising Polyphaga, Adephaga, and Myxophaga, most likely evolved by the Late Permian, but definite fossils are rare at this time.

Permian beetles probably played an important ecological role in forest ecosystems because most Permian beetles were most likely xylophagous insects that consumed living and dead woody stems (Figure 3). Some Permian xylophagous beetles fed on living wood tissues (Feng et al., 2017; Feng et al., 2019), which likely reduced tree productivity and could have caused extensive tree mortality. Insect-mediated tree mortality is known to result in large transfers of carbon from biomass to dead organic matter (Seidl et al., 2018; Fei et al., 2019). The other Permian xylophagous beetles were likely saproxylic (feeding on dead wood) (Ponomarenko, 2003), and they could also impact terrestrial carbon dynamics by accelerating wood decomposition (Ulyshen, 2018). Saproxylic animals first appeared in the Devonian and are mainly represented by small invertebrates such as oribatid mites, until the Permian (Labandeira et al., 1997; Labandeira, 2007). Whereas grazing by micro- and meso-invertebrates (nematodes, collembolans, enchytraeids and oribatid mites) did not significantly affect wood decomposition, consumption by macro-invertebrates (dominated by saproxylic beetles and termites in modern ecosystems) significantly sped up wood decomposition (Tapanila and Roberts, 2012). In addition to those that directly facilitated decomposition by consuming wood, Permian saproxylic beetles are likely to have had a variety of indirect effects on decomposition, including creating tunnels that facilitate the movement of fungi into wood (Naugolnykh and Ponomarenko, 2010; Feng et al., 2017), and vectoring fungi and other decay organisms on or within their bodies, like their extant counterparts (Ulyshen, 2016). In conclusion, Permian beetles that feed on living and dead wood probably could impact terrestrial carbon dynamics by reducing forests’ carbon sequestration capacity, and by converting live materials to dead organic matter and subsequent decomposition.

The oxygen concentration of the atmosphere began to rise in the early Palaeozoic, probably with a peak in the Carboniferous and large decline from the beginning of the Permian (Dahl et al., 2010; Berner, 2009; Krause et al., 2018). The reason for this plunge was attributed to a tectonic- or climate-driven reduction in the extent of coal swamps (Berner and Canfield, 1989) or to the evolution of lignin-consuming fungi (Floudas et al., 2012). However, global recoverable coal is only equivalent to a few percent of the oxygen budget in the atmosphere, and thus cannot account for the large drop of atmospheric oxygen (Nelsen et al., 2016). Furthermore, lignin-consuming fungi may have been present before the Carboniferous (Nelsen et al., 2016). Recently, a new geochemical model proposed that the development of Permian terrestrial herbivores may have limited transport and long-term burial of terrestrial organic compounds in marine sediments, resulting in less organic carbon burial and attendant declines in atmospheric oxygen (Laakso et al., 2020). Herbivorous insects and amniotes are thought to be the major herbivorous animals during the Permian and thus are considered to be the most important drivers of the Permian change in biogeochemical cycles of carbon (Laakso et al., 2020). However, Permian herbivorous amniotes mainly fed on leaves, stems, roots, and rhizomes (Sues and Reisz, 1998; Pearson et al., 2013) and could normally digest cellulose by fermentation but could not consume lignin, as in extant herbivorous vertebrates (Pearson et al., 2013). The majority of terrestrial plant biomass is stored in forest woody tissue consisting of decay-resistant lignin (Hibbett et al., 2016; Bar-On et al., 2018). In modern forests, the total carbon stock in woody tissue (including living and dead wood) is approximately 340 Pg carbon, much more than 72 Pg carbon in roots (below ground), 43 Pg carbon in foliage, and 43 Pg carbon in litter (Reich et al., 2014; Pan et al., 2011). In extant forest ecosystems, insects may account for 29% of the total carbon flux from dead wood and thus they have a functional importance in the decomposition of dead wood and the carbon cycle (Seibold et al., 2021). During the Permian, beetles were probably the dominant consumers of woody tissue, while a few other insect groups may have sometimes fed on dead wood (such as stem dictyopterans and protelytropterans) (Grimaldi and Engel, 2005). Permian beetles had probably evolved close interactions with various microorganisms, especially lignin-consuming fungi (Nelsen et al., 2016), which also accelerated the decomposition of dead wood. The Early Permian onset of the decrease in oxygen concentrations is consistent with the origin and radiation of the xylophagous beetles in the fossil record. Therefore, we propose that Permian xylophagous beetles could have been responsible for at least part of the change in Permian biogeochemical cycles in Laakso’s model (Laakso et al., 2020).

As the most taxonomically and functionally diverse group of living organisms on Earth (Stork, 2018), extant insects have significant effects on terrestrial carbon and nutrient cycling by modulating the quality and quantity of resources that enter the detrital food web (Belovsky and Slade, 2000; Kurz et al., 2008; Yang and Gratton, 2014; Seibold et al., 2021). However, the effects of insects on terrestrial ecosystems in deep time have been viewed as unimportant or overlooked (Doughty, 2017). Permian beetles were among the principal degraders of wood and played a fundamental role in deep-time carbon and nutrient cycling and niche creation. Insects may have been one of the major regulating factors of forest ecosystems at least from the Permian.

Our results show that both the taxonomic diversity and morphological disparity dropped dramatically during the Early Triassic (Figures 2 and 4). Combined with the phylogenetic results (Figure 3), our suite of analyses yields a clear ecological signal from beetles across the Permian/Triassic boundary: all xylophagous stem-group beetles become extinct near the Permian-Triassic boundary or abruptly decreased in the Early Triassic (a pattern called ‘dead clade walking’; Barnes et al., 2021), while aquatic phoroschizid and ademosynid lineages crossed the Permian/Triassic boundary and diversified in the Middle Triassic. Coleoptera recovered in taxonomic diversity during the Middle Triassic by the rise of new predatory and herbivorous groups, synchronized with the recovery of terrestrial ecosystems (Zhao et al., 2020). However, the morphological disparity is significantly lower than that of the Middle and Late Permian due to the lack of stem-group beetles that possess complex elytra structures (Figure 4, Figure 4—figure supplement 1). Polyphagan groups increased in taxonomic diversity during the Middle Triassic, which is a transitory epoch from a Palaeozoic stem-group beetle assemblage to a Mesozoic polyphagan-dominated assemblage.

Xylophagous groups are absent or rare in Early Triassic coleopteran assemblages, becoming widespread again from the Middle Triassic, mainly represented by more derived archostematans (such as Cupedidae) and polyphagans (Ponomarenko, 2003). This gap in xylophagous beetles coincided chronologically with the gap in coal deposition (‘coal gap’), a time during which peat-forming forests were rare or absent (Figure 3B), extending across at least the entire Early Triassic (Benton and Newell, 2014; Retallack et al., 1996; Nowak et al., 2020; Zhao et al., 2020). During the latest Permian and earliest Triassic, gymnosperm-dominated forests abruptly collapsed (Vajda et al., 2020) and were replaced by other biomes (such as isoetalean-dominated herbaceous heathlands; Feng et al., 2020) in most areas due to extreme conditions including aridity (Sun et al., 2012), wildfires (Shen et al., 2011), and ozone destruction (Benca et al., 2018). In some regions, the plant extinction was less severe, or the recovery was rapid (Hochuli et al., 2010), or there may have been multiple crises during the Early Triassic (Schneebeli-Hermann et al., 2017), but even short-term ecosystem disruption could have led to extinctions among xylophagous beetles. Previous studies have not provided a clear picture of insect evolution in response to possible environmental stresses, nor of their response to the EPME (Benton and Newell, 2014). Our results show for the first time that the demise of most forests (deforestation event; Vajda et al., 2020) most likely resulted in the extinction of most Palaeozoic xylophagous beetles, analogous to the extinction of tree-dwelling birds and mammals resulting from end-Cretaceous deforestation (Field et al., 2018; Hughes et al., 2021).

Our results reveal an Early Triassic gap in xylophagous beetles, suggesting that early archaic beetles experienced the severe ecological consequences of end-Permian deforestation. Extant insects are suffering from dramatic declines in abundance and diversity largely due to the anthropogenic deforestation and global warming (van Klink et al., 2020; Wagner et al., 2021). However, xylophagous insects have been largely neglected in studies of the current extinction crisis (van Klink et al., 2020). In particular, the diversity and abundance of xylophagous beetles are extremely sensitive to climate change and can also entail forest collapse and carbon cycle disturbance (Kurz et al., 2008; Fei et al., 2019; Šamonil et al., 2020). Our findings may help to better understand future changes in insect diversity and abundance and its consequences faced with global environmental change.

Materials and methods

Diversity analysis

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We compiled an updated database of all coleopteran species from the Early Permian to Middle Triassic from published literature in the early 1800s through to early 2020. In addition, we incorporated data from other open access database projects, including the Fossil Insect Database (EDNA) and Paleobiology Database (PBDB). We re-examined all published occurrences and taxonomy of Coleoptera from the Early Permian to Middle Triassic (Figure 2—source data 1). We standardized and corrected for nomenclatural consistency of all taxa using a classification of extinct beetle taxa above the genus rank (Bouchard et al., 2011). The data were filtered and cleaned by removing or reassigning illegitimate, questionable, and synonymous taxa and converting local to global chronostratigraphic units (Supplementary file 1).

We allocated fossil species into 12 stage-level time-bins covering the Early Permian-Middle Triassic interval (from the Asselian to Ladinian, 298–237 Ma). Considering the short duration of the Induan and Olenekian stages, we combined both stages into one time-bin. The formal taxa were erected based only on isolated elytra that cannot be classified definitely into any natural group. Thus, we separately counted the diversity of natural, formal, and mixed groups (Figure 2, Figure 2—figure supplement 1). The species Coleopsis archaica was attributed to Tschekardocoleidae by Kirejtshuk et al., 2013, but was later elevated to a new family Coleopseidae by Kirejtshuk, 2020. We followed the former opinion because it is premature to erect a family without a detailed cladistic analysis. We determined the stratigraphical ranges of families, genera, and species as the maximum and minimum ages in stage-level time-bins. All diversity was calculated using the range-through method.

Phylogenetic analysis

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In light of the new taxa and characters available for further testing the phylogenetic status of ancient stem-group beetles, we reconstructed the phylogenetic relationships among the stem groups by incorporating the presently described new taxa and revised characters coding into the previous dataset (Beutel et al., 2008). The morphological characters used for phylogenetic analysis comprise 93 adult and larval characters (Figure 3—source data 1). Unknown characters were coded as ‘?’. The taxon sampling contains two megalopterans as outgroups (Sialis and Chauliodes) and 13 coleopteran ingroup taxa (five extant and eight extinct) representing all four coleopteran extant suborders and their stem groups (Supplementary file 2). Compared to previous character matrices, we added the subfamily Taldycupedinae and three new characters (Supplementary file 3). The matrix was analysed in TNT version 1.1, through parsimony analysis and using traditional search (Goloboff et al., 2008). All characters were equally weighed and unordered (1000 replicates and 1000 trees saved per replication). Bootstrap values, consistency index, and retention index were provided (Figure 3—figure supplement 1).

Morphospace analysis

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We performed morphospace analyses with our newly assembled discrete character matrices (Figure 4—source data 1; Supplementary file 4). The analyses were performed using the free software R. 4.0.4. Both the MORD matrix and GED matrix were calculated based on two discrete character matrices (Lloyd, 2016; Wills, 1998). Recent research has revealed that the GED matrix creates a systematic bias in cases with a high percentage of missing data, and the MORD matrix can provide greater fidelity under these circumstances (Lloyd, 2016; Lehmann et al., 2019). We then ordinated all taxa into a multivariate morphospace with both PcoA and NMDS.

For PcoA, we used the function ‘ordinate cladistic matrix’ in package ‘Claddis’ with a cailliez method to correct the negative eigenvalues (Lloyd, 2016). Two disparity matrices were used to evaluate the volume of the morphospace, including the sum and product of the variances (Wills et al., 2016). The product metrics was normalized by taking the nth root (n equals the number of axes used for calculating disparity metrics). We used the scores on all axes that together comprise 90% of total variance to calculate those disparity metrics. We chose a permutation test (two-tailed) to test the null hypothesis of no difference between insect disparity of different time-bins. Each test run used 5000 replications. The test statistic was obtained by using the disparity metric of an older time-bin to minus that of a younger time-bin. If the proportion in the null distribution greater than the observed value of the test statistic is smaller than 0.025, the insect disparity of an older time-bin was considered significantly larger than that of a younger time-bin, and if the proportion was greater than 0.975, the insect disparity of a younger time-bin was considered significantly larger than that of an older time-bin (Figure 4—source data 2).

We also performed permutation tests with sample size corrected. For two design groups with different sample sizes, we first performed subsampling of the group with more samples to obtain equal sample sizes. Based on the newly obtained two groups with equal sample sizes, we calculated the observed value of the test statistic. Then we randomly permutated those species into different groups once and calculated a test statistic. We repeated this procedure (subsampling and permutation) 10,000 times and obtained a null distribution plus a group of observed values. We then calculated a set of proportions greater than the observed values in the null distribution. By analogy, if the median of the proportions is equal to or smaller than 0.025, the insect disparity of an older time-bin is significantly larger than that of a younger time-bin. If the median proportion is considered significantly greater than 0.975, the insect disparity of a younger time-bin is larger than that of an older time-bin (Figure 4—figure supplements 47).

For NMDS, we used the function ‘metaMDS’ in package ‘vegan’ with the number of dimension settings to 3 (Dixon, 2003). Both non-metric fit and linear fit were very high (larger than 0.90; Figure 4—figure supplements 47) and the stresses were smaller than 0.2, which implies that the ordinations are relatively good. Then we repeated all the previous analyses with this NMDS morphospace and acquired a similar result. The two disparity metrics of each time-bin were calculated based on two different distance matrices and two different ordination methods (Figure 4, Figure 4—figure supplements 15). The distribution was simulated under 500 bootstraps. Thirty-one undetermined specimens from the Grès à Voltzia Formation (Lower/Middle Triassic boundary, France) were included in our database and their age was attributed to the early Middle Triassic in our analysis (Figure 4, Figure 4—figure supplements 15). Considering that the age of these specimens is controversial, we repeated all our analyses assuming that the age of these specimens is Early Triassic; the result is consistent with the previous one (Figure 4—figure supplements 6 and 7).

Data availability

All source data are available at https://doi.org/10.5061/dryad.7m0cfxpvd. In addition, the source data files (Supplementary Data 1-4) have been provided for figures 2-4 and appendix figures 1-10.

The following data sets were generated
    1. Zhao X
    2. Yu Y
    3. Clapham M
    4. Yan E
    5. Chen J
    6. Jarzembowski E
    7. Zhao X
    8. Wang B
    (2021) Dryad Digital Repository
    Dataset of Early evolution of beetles regulated by the end-Permian deforestation.
    https://doi.org/10.5061/dryad.7m0cfxpvd

References

  1. Book
    1. Grimaldi D
    2. Engel MS
    (2005)
    Evolution of the Insects
    Cambridge University Press.
    1. Ponomarenko AG
    (1969)
    Historical development of archostematan beetles
    Trudy Paleontologicheskogo Instituta AN SSSR 125:1–240.
    1. Ponomarenko AG
    (2003)
    Ecological evolution of beetles (Insecta: Coleoptera)
    Acta Zoologica Cracoviensia 46:319–328.
    1. Ponomarenko AG
    (2004)
    Beetles (Insecta, Coleoptera) of the late Permian and early Triassic
    Paleontological Journal 38:S185–S196.
    1. Ulyshen MD
    (2016) Wood decomposition as influenced by invertebrates
    Biological Reviews of the Cambridge Philosophical Society 91:70–85.
    https://doi.org/10.1111/brv.12158

Decision letter

  1. George H Perry
    Senior and Reviewing Editor; Pennsylvania State University, United States
  2. Martin Fikacek
    Reviewer

Our editorial process produces two outputs: (i) public reviews designed to be posted alongside the preprint for the benefit of readers; (ii) feedback on the manuscript for the authors, including requests for revisions, shown below. We also include an acceptance summary that explains what the editors found interesting or important about the work.

Decision letter after peer review:

Thank you for submitting your article "Early evolution of beetles regulated by the end-Permian deforestation" for consideration by eLife. Your article has been reviewed by 2 peer reviewers, and the evaluation has been overseen by George Perry as the Senior and Reviewing Editor. The following individual involved in review of your submission has agreed to reveal their identity: Martin Fikacek (Reviewer #3).

The reviewers have discussed their reviews with one another and the Reviewing Editor. The two reviewers have provided clear and excellent feedback regarding essential and suggested changes in their individual reviews; I refer you to their comments below to help you prepare a revised submission to eLife.

Reviewer #2 (Recommendations for the authors):

Lines:

31 remove "a" "… by xylophagous stem groups with high diversity and disparity, ".

182 McKenna, not Mckenna.

207 change to "consumed".

208-211 Sentence from lines 208-211 could be rephrased to:

Some Permian xylophagous beetles fed on living wood tissues (Feng et al., 2017, 2019), which likely reduced tree productivity and could have caused extensive tree mortality. Insect-mediated tree mortality is known to result in large transfers of carbon from biomass to dead organic matter (Seidl et al., 2018; Fei et al., 2019).

The original text made it sound like there was data on this carbon transfer in the Permian.

215 add commas to "small invertebrates, such as oribatid mites, until the".

243-245 This is pretty correlative. A stronger argument would look at the other proposed causes of decreasing O2 in the Early Permian (ex. fires, see Glasspool 2006) and show a stronger relationship between atm O2 and the evolution of beetle xylophagy.

The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. August 2006 Proceedings of the National Academy of Sciences 103(29):10861-5.

246 change to something like "…been responsible for at least a portion of the change of biogeochemical cycles of carbon…".

253-255 Cite the statement for “Permian beetles were the principal degraders of wood”, and/or say something like “… among the principal”..".

280 include "and" between the Vajada et al., 2020 citation and "were".

Reviewer #3 (Recommendations for the authors):

This is a very nicely done and written study, I definitely like the multi-approach and multi-evidence approach which together brings a very clear view and very well-supported hypotheses about the early evolution of beetles and their roles in the ancient ecosystems. I provided my "praise" already in the public review, so here I will focus on some critique and recommendations.

My specialization is beetle systematics and phylogenetics, so the part I can comment on most in detail is naturally the phylogenetic analysis. As I mentioned in the public statement, I agree that the analysis provided is good enough for this study, which was not focused only on the phylogeny and which aims at the more general view. However, I did not find any information on whether the actual species included in the analysis were really reexamined and whether the characters included were double-checked (which would be the ideal way), or whether the dataset was simply adopted from Beutel (2008) and updated by few new characters and few new taxa (which is the way most people do, but it naturally risks that some mistakes of misinterpretations present in the published matrices are adopted and copied again and again). As far as I knew, Beutel´s (2008) dataset was compiled largely from the literature without reexamining the actual fossils, which is why it should be used with care.

If I can ask about one specific character: you follow the view presented in old papers (and adopted in the matrix by Beutel 2008) that the earliest beetles had 13-segmented antennae. This is really illustrated in many reconstructions by Ponomarenko, but as far as I remember, most of these fossils actually do not have antennae preserved. There were I think only two fossils of Tschekardocoleidae which antennae were preserved, and from the photos available in the literature, I had strong doubts about their antennae being 13-segmented, it always looked like normal 11-segmented beetle antennae. I am asking not only because this character is included in the morphology matrix (as a single character, it would likely not change the topology too much even when coded incorrectly), but also because you provide the new reconstruction of the Tschekardocoleid beetles (again with 13-segmented antennae), so it would be good to double-check this character to be sure you are just not reproducing the old mistake again and again.

In general, I also believe that including more taxa into the analysis would be desirable, not just a single taxon per family, but I agree that for this study you need a simplified phylogeny only and your approach hence can be considered as justified.

Few other questions:

(1) You state that Tschekardocoleidae is the oldest beetle, but you do not mention Coleopsis archaica anywhere in the paper (sorry if I overlooked it). Does it mean you do not consider this fossil as the representative of Coleoptera? It would be good to provide some sentence about that, to make it clear for the reader why this fossil is not considered (e.g., if you directly exclude it from beetles, or if you just consider it as doubtful and hence better do not include it in your analyses).

(2) There are also larval characters in your morphology matrix, but it is unclear to me which larvae were coded - can you provide some information in your list of taxa included in the analysis about which taxon has only adult data, and which has also larval data? And in the case of larvae coded, can you provide some justification of why the larva you coded is supposed to belong to the respective adult? In fossils, associating larvae with adults is a tricky task and often the associations are kind of guesses, so it would be good to know your arguments supporting the larva-adult associations for the taxa in which you coded larvae.

(3) You compare fossils data about the origin of some beetles groups with the molecular time trees results - that is perfect. But better cite more than one time tree study (you only mention McKenna 2019). This is because all molecular time trees are subject to bias and mistakes, partly introduced by specific methods used, partly by more or less carefully done selection of calibrating fossils and the way how they are implemented in the study. All that means, that we can be confident basically only about the results which are revealed repeatedly in various independent timetree studies, and hence ideally a reference to multiple studies is needed.

(4) I am not a specialist in beetle ecology and environmental sciences, but when reading the discussion connecting the early beetles to carbon cycling and dead-wood decay, I got some questions for which I did not find any reply in the text:

– You state in the introduction that since all early beetle lineages are extinct, it is hard to apply the knowledge about modern beetle lineages fully - I totally agree with this, the phylogenetic position of the early beetles is so basal that the simple parallels with modern beetles do not need to work. But after (correctly) stating that in the introduction, you use precisely the "parallel with modern beetles" approach to state that the ancient beetles were wood-boring because they looked like modern wood-boring Archostemata. I kind of feel that there are two problems hidden in this: (1) the parallel "looks same so it lived the same" may not necessarily work for 100% (as you stated in the introduction), and (2) I am not sure how much is actually known about the detailed biology of modern Archostemata (I know they are referred as wood-boring in all general chapters but are there actually some studies about their lifestyle?). I am not saying that these issues disqualify your conclusions, but maybe a more careful phrasing, and in some cases, more detailed and direct support of some statements (like wood-boring Archostemata) would make the text easier to read and would present your conclusions as more sound.

– I am not really good at general paleontology and geology etc., so reading your general discussions about environmental changes at P-T was interesting. But I would maybe sometimes welcome to have a little bit more information provided, not to just found the reference to the paper. Some parts are really cool lists and summaries of recently published studies, but it would be simply beneficial for readers without general paleo-knowledge like me not to need to dig into all these papers to understand your conclusions. I know there likely is a strong length limitation for the manuscript, but I ask even the editor, in this case, to make it possible to provide a little bit more information than just a list of references.

https://doi.org/10.7554/eLife.72692.sa1

Author response

Reviewer #2 (Recommendations for the authors):

Lines:

31 remove "a" "… by xylophagous stem groups with high diversity and disparity, ".

Thank you. We have corrected it. Please see line 31.

182 McKenna, not Mckenna.

Thank you. We have corrected it. Please see line 187.

207 change to "consumed".

Thank you. We have corrected it. Please see line 214.

208-211 Sentence from lines 208-211 could be rephrased to:

Some Permian xylophagous beetles fed on living wood tissues (Feng et al., 2017, 2019), which likely reduced tree productivity and could have caused extensive tree mortality. Insect-mediated tree mortality is known to result in large transfers of carbon from biomass to dead organic matter (Seidl et al., 2018; Fei et al., 2019).

The original text made it sound like there was data on this carbon transfer in the Permian.

Thank you and revised. Please see lines 214–218. “Some Permian xylophagous beetles fed on living wood tissues (Feng et al., 2017, 2019), which likely reduced tree productivity and could have caused extensive tree mortality. Insect-mediated tree mortality is known to result in large transfers of carbon from biomass to dead organic matter (Seidl et al., 2018; Fei et al., 2019).”

215 add commas to "small invertebrates, such as oribatid mites, until the".

Thank you. We have corrected it. Please see line 223.

243-245 This is pretty correlative. A stronger argument would look at the other proposed causes of decreasing O2 in the Early Permian (ex. fires, see Glasspool 2006) and show a stronger relationship between atm O2 and the evolution of beetle xylophagy.

The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. August 2006 Proceedings of the National Academy of Sciences 103(29):10861-5.

Thank you. Scott and Glasspool (2006) concluded that oxygen levels are a significant control on long-term fire occurrence and suggested that more fire may lead to increased charcoal production and further increased levels of oxygen. However, they did not refer to the reason about the decrease of oxygen. So we did not cite this reference. We have added other two hypotheses about the reason for the oxygen plunge (reduction in the extent of coal swamps and the evolution of lignin-consuming fungi) and ruled them out in the Discussion. Please see comment 1.

246 change to something like "…been responsible for at least a portion of the change of biogeochemical cycles of carbon…".

Thank you and revised. Please see line 272–273.

253-255 Cite the statement for “Permian beetles were the principal degraders of wood”, and/or say something like “… among the principal”..".

Thank you. We have add “… among the principal degraders…”. Please see line 280.

280 include "and" between the Vajada et al., 2020 citation and "were".

Thank you. We have corrected it. Please see line 307.

Reviewer #3 (Recommendations for the authors):

This is a very nicely done and written study, I definitely like the multi-approach and multi-evidence approach which together brings a very clear view and very well-supported hypotheses about the early evolution of beetles and their roles in the ancient ecosystems. I provided my "praise" already in the public review, so here I will focus on some critique and recommendations.

My specialization is beetle systematics and phylogenetics, so the part I can comment on most in detail is naturally the phylogenetic analysis. As I mentioned in the public statement, I agree that the analysis provided is good enough for this study, which was not focused only on the phylogeny and which aims at the more general view. However, I did not find any information on whether the actual species included in the analysis were really reexamined and whether the characters included were double-checked (which would be the ideal way), or whether the dataset was simply adopted from Beutel (2008) and updated by few new characters and few new taxa (which is the way most people do, but it naturally risks that some mistakes of misinterpretations present in the published matrices are adopted and copied again and again). As far as I knew, Beutel´s (2008) dataset was compiled largely from the literature without reexamining the actual fossils, which is why it should be used with care.

If I can ask about one specific character: you follow the view presented in old papers (and adopted in the matrix by Beutel 2008) that the earliest beetles had 13-segmented antennae. This is really illustrated in many reconstructions by Ponomarenko, but as far as I remember, most of these fossils actually do not have antennae preserved. There were I think only two fossils of Tschekardocoleidae which antennae were preserved, and from the photos available in the literature, I had strong doubts about their antennae being 13-segmented, it always looked like normal 11-segmented beetle antennae. I am asking not only because this character is included in the morphology matrix (as a single character, it would likely not change the topology too much even when coded incorrectly), but also because you provide the new reconstruction of the Tschekardocoleid beetles (again with 13-segmented antennae), so it would be good to double-check this character to be sure you are just not reproducing the old mistake again and again.

In general, I also believe that including more taxa into the analysis would be desirable, not just a single taxon per family, but I agree that for this study you need a simplified phylogeny only and your approach hence can be considered as justified.

Thank you. We completely agreed with the reviewer that most of early beetles need re-examination. We examined some early beetle fossils deposited in Moscow, and found that the original descriptions of some species are not correct probably due to the poor preservation. Therefore, we only use the best-preserved species to represent the higher-level taxa (family). A comprehensive revision of all fossils are very important, but is beyond the scope of our paper. Regarding the phylogeny, we mainly followed the Beutel’s (2008) dataset, which is the only dataset for the fossil beetles. As the statement of the reviewer, the simplified phylogeny is enough for illustrating the effect of end-Permian extinction to the beetle evolution.

We are grateful to the reviewer to point out the issue about the segmentation of the antennae. We re-examined the Russian specimens and discussed this issue with several colleagues including Rolf Beutel. We completely agreed with the reviewer that Tschekardocoleidae and Permocupedidae have most likely only 11-segmented antennae. We have revised the matrix and figures (Fig. 1B, D). We also carefully re-examined the matrix of the phylogenetic analysis and corrected several characters. Our new phylogenetic result is almost the same as the previous one (Figure 3-figure supplement 1).

Few other questions:

(1) You state that Tschekardocoleidae is the oldest beetle, but you do not mention Coleopsis archaica anywhere in the paper (sorry if I overlooked it). Does it mean you do not consider this fossil as the representative of Coleoptera? It would be good to provide some sentence about that, to make it clear for the reader why this fossil is not considered (e.g., if you directly exclude it from beetles, or if you just consider it as doubtful and hence better do not include it in your analyses).

Thank you very much for pointing out this issue. Coleopsis archaica was included in our database. This species was attributed to Tschekardocoleidae by Kirejtshuk et al. (2014), but later was elevated to a new family Coleopseidae by Kirejtshuk (2020). We followed the former opinion because it is premature to erect a family without a detailed cladistic analysis. This has been clarified in the revised version of the manuscript. Please see line 184. “The earliest definite beetles are Tshekardocoleidae (including the genus Coleopsis) from the Early Permian …”. Please see lines 353–356. “The species Coleopsis archaica was attributed to Tschekardocoleidae by Kirejtshuk et al. (2014), but was later elevated to a new family Coleopseidae by Kirejtshuk (2020). We followed the former opinion because it is premature to erect a family without a detailed cladistic analysis.”

We also added a reference.

Kirejtshuk AG. 2020. Taxonomic review of fossil coleopterous families (Insecta, Coleoptera). Suborder Archostemata: superfamilies Coleopseoidea and Cupedoidea. Geosciences 10: 73.

(2) There are also larval characters in your morphology matrix, but it is unclear to me which larvae were coded - can you provide some information in your list of taxa included in the analysis about which taxon has only adult data, and which has also larval data? And in the case of larvae coded, can you provide some justification of why the larva you coded is supposed to belong to the respective adult? In fossils, associating larvae with adults is a tricky task and often the associations are kind of guesses, so it would be good to know your arguments supporting the larva-adult associations for the taxa in which you coded larvae.

Thank you. In the phylogeny dataset, larval characters of all extinct groups were coded “unknown”, due to the lack of larval fossils.

(3) You compare fossils data about the origin of some beetles groups with the molecular time trees results - that is perfect. But better cite more than one time tree study (you only mention McKenna 2019). This is because all molecular time trees are subject to bias and mistakes, partly introduced by specific methods used, partly by more or less carefully done selection of calibrating fossils and the way how they are implemented in the study. All that means, that we can be confident basically only about the results which are revealed repeatedly in various independent timetree studies, and hence ideally a reference to multiple studies is needed.

We are grateful for the suggestion. We have added two references to the Discussion section.

(4) I am not a specialist in beetle ecology and environmental sciences, but when reading the discussion connecting the early beetles to carbon cycling and dead-wood decay, I got some questions for which I did not find any reply in the text:

– You state in the introduction that since all early beetle lineages are extinct, it is hard to apply the knowledge about modern beetle lineages fully - I totally agree with this, the phylogenetic position of the early beetles is so basal that the simple parallels with modern beetles do not need to work. But after (correctly) stating that in the introduction, you use precisely the "parallel with modern beetles" approach to state that the ancient beetles were wood-boring because they looked like modern wood-boring Archostemata. I kind of feel that there are two problems hidden in this: (1) the parallel "looks same so it lived the same" may not necessarily work for 100% (as you stated in the introduction), and (2) I am not sure how much is actually known about the detailed biology of modern Archostemata (I know they are referred as wood-boring in all general chapters but are there actually some studies about their lifestyle?). I am not saying that these issues disqualify your conclusions, but maybe a more careful phrasing, and in some cases, more detailed and direct support of some statements (like wood-boring Archostemata) would make the text easier to read and would present your conclusions as more sound.

Thank you very much. We completely agreed with the reviewer that we are not 100% certain that these extinct beetles are wood-boring. We deduced their palaeoecology based on morphological comparisons and potential trace fossils, following the previous studies (e.g., Ponomarenko, 1969; Naugolnykh and Ponomarenko, 2010). We toned down the statement of the palaeoecology throughout the Discussion part. Please see lines 200 and 213. “These ancient beetles were most likely xylophagous”. “most Permian beetles were most likely xylophagous insects”.

– I am not really good at general paleontology and geology etc., so reading your general discussions about environmental changes at P-T was interesting. But I would maybe sometimes welcome to have a little bit more information provided, not to just found the reference to the paper. Some parts are really cool lists and summaries of recently published studies, but it would be simply beneficial for readers without general paleo-knowledge like me not to need to dig into all these papers to understand your conclusions. I know there likely is a strong length limitation for the manuscript, but I ask even the editor, in this case, to make it possible to provide a little bit more information than just a list of references.

Thank you. There are two paragraphs about the P-T environmental changes in the Discussion section. We followed the reviewer’s suggestion and enlarged both paragraphs.

Regarding the Permian environment, we have added an introduction about the change of atmospheric oxygen and included several hypothesis. Please see lines 237–249. “The oxygen concentration of the atmosphere began to rise in the early Palaeozoic, probably with a peak in the Carboniferous and large decline from the beginning of the Permian (Dahl et al., 2010; Berner, 2009; Krause et al, 2018). The reason for this plunge was attributed to a tectonic- or climatic-forced reduction in the extent of coal swamps (Berner and Canfield, 1989) or to the evolution of lignin-consuming fungi (Floudas et al., 2012). However, global recoverable coal is only equivalent to a few percent of the oxygen budget in the atmosphere, and thus cannot account for the large drop of atmospheric oxygen (Nelsen et al., 2016). Furthermore, lignin-consuming fungi may have been present before the Carboniferous (Nelsen et al., 2016). Recently, a new geochemical model proposed that the development of Permian terrestrial herbivores may have limited transport and long-term burial of terrestrial organic compounds in marine sediments, resulting in less organic carbon burial and attendant declines in atmospheric oxygen (Laakso et al., 2020).”

Regarding the Early Triassic coal gap, we have added a brief introduction. Please see lines 302–306. “This gap in xylophagous beetles coincided chronologically with the gap in coal deposition (“coal gap”), a time during which peat-forming forests were rare or absent (Figure 3B), extending across at least the entire Early Triassic (Benton and Newell, 2014, Retallack et al., 1996; Nowak et al., 2020; Zhao et al., 2020).”

https://doi.org/10.7554/eLife.72692.sa2

Article and author information

Author details

  1. Xianye Zhao

    1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
    2. University of Chinese Academy of Sciences, Beijing, China
    Contribution
    Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft, Writing - review and editing
    Competing interests
    No competing interests declared
  2. Yilun Yu

    1. University of Chinese Academy of Sciences, Beijing, China
    2. Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China
    Contribution
    Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft, Writing - review and editing
    Competing interests
    No competing interests declared
  3. Matthew E Clapham

    Department of Earth and Planetary Sciences, University of California, Santa Cruz, Santa Cruz, United States
    Contribution
    Investigation, Validation, Writing - review and editing
    Competing interests
    No competing interests declared
  4. Evgeny Yan

    Palaeontological Institute, Russian Academy of Sciences, Moscow, Russian Federation
    Contribution
    Investigation, Visualization, Writing - review and editing
    Competing interests
    No competing interests declared
  5. Jun Chen

    1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
    2. Institute of Geology and Paleontology, Linyi University, Linyi, China
    Contribution
    Formal analysis, Investigation, Methodology, Writing - review and editing
    Competing interests
    No competing interests declared
  6. Edmund A Jarzembowski

    1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
    2. Department of Earth Sciences, Natural History Museum, London, United Kingdom
    Contribution
    Investigation, Writing - review and editing
    Competing interests
    No competing interests declared
  7. Xiangdong Zhao

    1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
    2. University of Chinese Academy of Sciences, Beijing, China
    Contribution
    Investigation, Writing - review and editing
    Competing interests
    No competing interests declared
  8. Bo Wang

    State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, China
    Contribution
    Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - original draft, Writing - review and editing
    For correspondence
    bowang@nigpas.ac.cn
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8001-9937

Funding

Chinese Academy of Sciences (XDA19050101 XDB26000000)

  • Bo Wang

National Natural Science Foundation of China (42125201 41688103)

  • Bo Wang

Natural Scientific Foundation of Shandong Province (ZR2020YQ27)

  • Jun Chen

Russian Science Foundation (21-14-00284)

  • Evgeny Yan

Chinese Academy of Sciences (2020VCA0020)

  • Edmund A Jarzembowski

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Acknowledgements

We are grateful to George Perry, Martin Fikáček, and two anonymous reviewers for invaluable comments that improved this manuscript. We thank AG Ponomarenko, RG Beutel, AP Rasnitsyn, AG Kirejtshuk, J Xue, H Xu, B Huang, and H Zeng for helpful discussion, and D Yang for reconstructions. BW thanks members of the palaeoentomological laboratory of the Palaeontological Institute (Russian Academy of Sciences) for their help during his visit to Moscow (2010).

Senior and Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Reviewer

  1. Martin Fikacek

Publication history

  1. Received: August 1, 2021
  2. Preprint posted: October 13, 2021 (view preprint)
  3. Accepted: November 3, 2021
  4. Accepted Manuscript published: November 8, 2021 (version 1)
  5. Version of Record published: November 11, 2021 (version 2)

Copyright

© 2021, Zhao et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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