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.

Figure 1

Download asset Open asset

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.

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.

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.

1. 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

1. 1. Bar-On YM
   2. Phillips R
   3. Milo R

   (2018) The biomass distribution on Earth

   PNAS 115:6506–6511.

   https://doi.org/10.1073/pnas.1711842115

   • PubMed
   • Google Scholar
2. 1. Barnes BD
   2. Sclafani JA
   3. Zaffos A

   (2021) Dead clades walking are a pervasive macroevolutionary pattern

   PNAS 118:e2019208118.

   https://doi.org/10.1073/pnas.2019208118

   • PubMed
   • Google Scholar
3. 1. Belovsky GE
   2. Slade JB

   (2000) Insect herbivory accelerates nutrient cycling and increases plant production

   PNAS 97:14412–14417.

   https://doi.org/10.1073/pnas.250483797

   • PubMed
   • Google Scholar
4. 1. Benca JP
   2. Duijnstee IAP
   3. Looy CV

   (2018) UV-B-induced forest sterility: Implications of ozone shield failure in Earth’s largest extinction

   Science Advances 4:e1700618.

   https://doi.org/10.1126/sciadv.1700618

   • PubMed
   • Google Scholar
5. 1. Benton MJ
   2. Newell AJ

   (2014) Impacts of global warming on Permo-Triassic terrestrial ecosystems

   Gondwana Research 25:1308–1337.

   https://doi.org/10.1016/j.gr.2012.12.010

   • Google Scholar
6. 1. Berner RA
   2. Canfield DE

   (1989) A new model for atmospheric oxygen over Phanerozoic time

   American Journal of Science 289:333–361.

   https://doi.org/10.2475/ajs.289.4.333

   • PubMed
   • Google Scholar
7. 1. Berner RA

   (2009) Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model

   American Journal of Science 309:603–606.

   https://doi.org/10.2475/07.2009.03

   • Google Scholar
8. 1. Béthoux O
   2. Papier F
   3. Nel A

   (2005) The Triassic radiation of the entomofauna

   Comptes Rendus Palevol 4:609–621.

   https://doi.org/10.1016/j.crpv.2005.06.005

   • Google Scholar
9. 1. Beutel RG
   2. Ge S
   3. Hörnschemeyer T

   (2008) On the head morphology of Tetraphalerus, the phylogeny of Archostemata and the basal branching events in Coleoptera

   Cladistics 24:270–298.

   https://doi.org/10.1111/j.1096-0031.2007.00186.x

   • Google Scholar
10. 1. Beutel R.G
    2. Pohl H
    3. Yan EV
    4. Anton E
    5. Liu SP
    6. Ślipiński A
    7. McKenna DD
    8. Friedrich F

    (2019) The phylogeny of Coleopterida (Hexapoda) - morphological characters and molecular phylogenies

    Systematic Entomology 44:75–102.

    https://doi.org/10.1111/syen.12316

    • Google Scholar
11. 1. Black B.A
    2. Hauri EH
    3. Elkins-Tanton LT
    4. Brown SM

    (2014) Sulfur isotopic evidence for sources of volatiles in Siberian Traps magmas

    Earth and Planetary Science Letters 394:58–69.

    https://doi.org/10.1016/j.epsl.2014.02.057

    • Google Scholar
12. 1. Black BA
    2. Neely RR
    3. Lamarque J-F
    4. Elkins-Tanton LT
    5. Kiehl JT
    6. Shields CA
    7. Mills MJ
    8. Bardeen C

    (2018) Systemic swings in end-Permian climate from Siberian Traps carbon and sulfur outgassing

    Nature Geoscience 11:949–954.

    https://doi.org/10.1038/s41561-018-0261-y

    • Google Scholar
13. 1. Bouchard P
    2. Bousquet Y
    3. Davies A
    4. Alonso-Zarazaga M
    5. Lawrence J
    6. Lyal C
    7. Newton A
    8. Reid C
    9. Schmitt M
    10. Slipinski A
    11. Smith A

    (2011) Family-Group Names In Coleoptera (Insecta)

    ZooKeys 88:1–972.

    https://doi.org/10.3897/zookeys.88.807

    • Google Scholar
14. 1. Burgess SD
    2. Bowring SA

    (2015) High-precision geochronology confirms voluminous magmatism before, during, and after Earth’s most severe extinction

    Science Advances 1:e1500470.

    https://doi.org/10.1126/sciadv.1500470

    • PubMed
    • Google Scholar
15. 1. Condamine FL
    2. Clapham ME
    3. Kergoat GJ

    (2016) Global patterns of insect diversification: towards a reconciliation of fossil and molecular evidence?

    Scientific Reports 6:1–13.

    https://doi.org/10.1038/srep19208

    • Google Scholar
16. 1. Condamine FL
    2. Nel A
    3. Grandcolas P
    4. Legendre F

    (2020) Fossil and phylogenetic analyses reveal recurrent periods of diversification and extinction in dictyopteran insects

    Cladistics 36:394–412.

    https://doi.org/10.1111/cla.12412

    • PubMed
    • Google Scholar
17. 1. Dahl TW
    2. Hammarlund EU
    3. Anbar AD
    4. Bond DPG
    5. Gill BC
    6. Gordon GW
    7. Knoll AH
    8. Nielsen AT
    9. Schovsbo NH
    10. Canfield DE

    (2010) Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish

    PNAS 107:17911–17915.

    https://doi.org/10.1073/pnas.1011287107

    • PubMed
    • Google Scholar
18. 1. Dal Corso J
    2. Mills BJW
    3. Chu D
    4. Newton RJ
    5. Mather TA
    6. Shu W
    7. Wu Y
    8. Tong J
    9. Wignall PB

    (2020) Permo-Triassic boundary carbon and mercury cycling linked to terrestrial ecosystem collapse

    Nature Communications 11:2962.

    https://doi.org/10.1038/s41467-020-16725-4

    • PubMed
    • Google Scholar
19. 1. Deline B
    2. Greenwood JM
    3. Clark JW
    4. Puttick MN
    5. Peterson KJ
    6. Donoghue PCJ

    (2018) Evolution of metazoan morphological disparity

    PNAS 115:E8909–E8918.

    https://doi.org/10.1073/pnas.1810575115

    • PubMed
    • Google Scholar
20. 1. Dixon P

    (2003) VEGAN, a package of R functions for community ecology

    Journal of Vegetation Science 14:927–930.

    https://doi.org/10.1111/j.1654-1103.2003.tb02228.x

    • Google Scholar
21. 1. Dmitriev VYu
    2. Aristov DS
    3. Bashkuev AS
    4. Vasilenko DV
    5. Vřsanský P
    6. Gorochov AV
    7. Lukashevitch ED
    8. Mostovski MB
    9. Ponomarenko AG
    10. Popov YuA
    11. Rasnitsyn AP
    12. Sinitshenkova ND
    13. Sukatsheva ID
    14. Tarasenkova MM
    15. Khramov AV
    16. Shmakov AS

    (2018) Insect diversity from the Carboniferous to Recent

    Paleontological Journal 52:610–619.

    https://doi.org/10.1134/S0031030118060047

    • Google Scholar
22. 1. Doughty CE

    (2017) Herbivores increase the global availability of nutrients over millions of years

    Nature Ecology & Evolution 1:1820–1827.

    https://doi.org/10.1038/s41559-017-0341-1

    • Google Scholar
23. 1. Fei SL
    2. Morin RS
    3. Oswalt CM
    4. Liebhold AM

    (2019) Biomass losses resulting from insect and disease invasions in US forests

    PNAS 116:17371–17376.

    https://doi.org/10.1073/pnas.1820601116

    • PubMed
    • Google Scholar
24. 1. Feng Z
    2. Wang J
    3. Rößler R
    4. Ślipiński A
    5. Labandeira C

    (2017) Late Permian wood-borings reveal an intricate network of ecological relationships

    Nature Communications 8:556.

    https://doi.org/10.1038/s41467-017-00696-0

    • PubMed
    • Google Scholar
25. 1. Feng Z
    2. Bertling M
    3. Noll R
    4. Ślipiński A
    5. Rößler R

    (2019) Beetle borings in wood with host response in early Permian conifers from Germany

    PalZ 93:409–421.

    https://doi.org/10.1007/s12542-019-00476-9

    • Google Scholar
26. 1. Feng Zhuo
    2. Wei H-B
    3. Guo Y
    4. He X-Y
    5. Sui Q
    6. Zhou Y
    7. Liu H-Y
    8. Gou X-D
    9. Lv Y

    (2020) From rainforest to herbland: new insights into land plant responses to the end-Permian mass extinction

    Earth-Science Reviews 204:103153.

    https://doi.org/10.1016/j.earscirev.2020.103153

    • Google Scholar
27. 1. Field DJ
    2. Bercovici A
    3. Berv JS
    4. Dunn R
    5. Fastovsky DE
    6. Lyson TR
    7. Vajda V
    8. Gauthier JA

    (2018) Early evolution of modern birds structured by global forest collapse at the end-Cretaceous mass extinction

    Current Biology 28:1825–1831.

    https://doi.org/10.1016/j.cub.2018.04.062

    • PubMed
    • Google Scholar
28. 1. Fielding CR
    2. Frank TD
    3. McLoughlin S
    4. Vajda V
    5. Mays C
    6. Tevyaw AP
    7. Winguth A
    8. Winguth C
    9. Nicoll RS
    10. Bocking M
    11. Crowley JL

    (2019) Age and pattern of the southern high-latitude continental end-Permian extinction constrained by multiproxy analysis

    Nature Communications 10:385.

    https://doi.org/10.1038/s41467-018-07934-z

    • PubMed
    • Google Scholar
29. 1. Floudas D
    2. Binder M
    3. Riley R
    4. Barry K
    5. Blanchette RA
    6. Henrissat B
    7. Martínez AT
    8. Otillar R
    9. Spatafora JW
    10. Yadav JS
    11. Aerts A
    12. Benoit I
    13. Boyd A
    14. Carlson A
    15. Copeland A
    16. Coutinho PM
    17. de Vries RP
    18. Ferreira P
    19. Findley K
    20. Foster B
    21. Gaskell J
    22. Glotzer D
    23. Górecki P
    24. Heitman J
    25. Hesse C
    26. Hori C
    27. Igarashi K
    28. Jurgens JA
    29. Kallen N
    30. Kersten P
    31. Kohler A
    32. Kües U
    33. Kumar TKA
    34. Kuo A
    35. LaButti K
    36. Larrondo LF
    37. Lindquist E
    38. Ling A
    39. Lombard V
    40. Lucas S
    41. Lundell T
    42. Martin R
    43. McLaughlin DJ
    44. Morgenstern I
    45. Morin E
    46. Murat C
    47. Nagy LG
    48. Nolan M
    49. Ohm RA
    50. Patyshakuliyeva A
    51. Rokas A
    52. Ruiz-Dueñas FJ
    53. Sabat G
    54. Salamov A
    55. Samejima M
    56. Schmutz J
    57. Slot JC
    58. St John F
    59. Stenlid J
    60. Sun H
    61. Sun S
    62. Syed K
    63. Tsang A
    64. Wiebenga A
    65. Young D
    66. Pisabarro A
    67. Eastwood DC
    68. Martin F
    69. Cullen D
    70. Grigoriev IV
    71. Hibbett DS

    (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes

    Science 336:1715–1719.

    https://doi.org/10.1126/science.1221748

    • PubMed
    • Google Scholar
30. 1. Gastaldo RA

    (2019) Ancient plants escaped the end-Permian mass extinction

    Nature 567:38–39.

    https://doi.org/10.1038/d41586-019-00744-3

    • PubMed
    • Google Scholar
31. 1. Goloboff PA
    2. Farris JS
    3. Nixon KC

    (2008) TNT, a free program for phylogenetic analysis

    Cladistics 24:774–786.

    https://doi.org/10.1111/j.1096-0031.2008.00217.x

    • Google Scholar
32. Book

    1. Grimaldi D
    2. Engel MS

    (2005)

    Evolution of the Insects

    Cambridge University Press.

    • Google Scholar
33. 1. Hibbett D
    2. Blanchette R
    3. Kenrick P
    4. Mills B

    (2016) Climate, decay, and the death of the coal forests

    Current Biology 26:R563–R567.

    https://doi.org/10.1016/j.cub.2016.01.014

    • PubMed
    • Google Scholar
34. 1. Hochuli PA
    2. Hermann E
    3. Vigran JO
    4. Bucher H
    5. Weissert H

    (2010) Rapid demise and recovery of plant ecosystems across the end-Permian extinction event

    Global and Planetary Change 74:144–155.

    https://doi.org/10.1016/j.gloplacha.2010.10.004

    • Google Scholar
35. 1. Hughes M
    2. Gerber S
    3. Wills MA

    (2013) Clades reach highest morphological disparity early in their evolution

    PNAS 110:13875–13879.

    https://doi.org/10.1073/pnas.1302642110

    • PubMed
    • Google Scholar
36. 1. Hughes JJ
    2. Berv JS
    3. Chester SGB
    4. Sargis EJ
    5. Field DJ

    (2021) Ecological selectivity and the evolution of mammalian substrate preference across the K–Pg boundary

    Ecology and Evolution 10:8114.

    https://doi.org/10.1002/ece3.8114

    • Google Scholar
37. 1. Kirejtshuk AG
    2. Poschmann M
    3. Prokop J
    4. Garrouste R
    5. Nel A

    (2013) Evolution of the elytral venation and structural adaptations in the oldest Palaeozoic beetles (Insecta: Coleoptera: Tshekardocoleidae)

    Journal of Systematic Palaeontology 12:575–600.

    https://doi.org/10.1080/14772019.2013.821530

    • Google Scholar
38. 1. Kirejtshuk AG

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

    Geosciences 10:73.

    https://doi.org/10.3390/geosciences10020073

    • Google Scholar
39. 1. Krause AJ
    2. Mills BJW
    3. Zhang S
    4. Planavsky NJ
    5. Lenton TM
    6. Poulton SW

    (2018) Stepwise oxygenation of the Paleozoic atmosphere

    Nature Communications 9:4081.

    https://doi.org/10.1038/s41467-018-06383-y

    • PubMed
    • Google Scholar
40. 1. Kurz WA
    2. Dymond CC
    3. Stinson G
    4. Rampley GJ
    5. Neilson ET
    6. Carroll AL
    7. Ebata T
    8. Safranyik L

    (2008) Mountain pine beetle and forest carbon feedback to climate change

    Nature 452:987–990.

    https://doi.org/10.1038/nature06777

    • PubMed
    • Google Scholar
41. 1. Laakso TA
    2. Strauss JV
    3. Peterson KJ

    (2020) Herbivory and its effect on Phanerozoic oxygen concentrations

    Geology 48:410–414.

    https://doi.org/10.1130/G47085.1

    • Google Scholar
42. 1. Labandeira CC
    2. Sepkoski JJ

    (1993) Insect diversity in the fossil record

    Science 261:310–315.

    https://doi.org/10.1126/science.11536548

    • PubMed
    • Google Scholar
43. 1. Labandeira CC
    2. Phillips TL
    3. Norton RA

    (1997) Oribatid mites and the decomposition of plant tissues in Paleozoic coal-swamp forests

    Palaios 12:319.

    https://doi.org/10.2307/3515334

    • Google Scholar
44. 1. Labandeira CC

    (2005) The fossil record of insect extinction: new approaches and future directions

    American Entomologist 51:14–29.

    https://doi.org/10.1093/ae/51.1.14

    • Google Scholar
45. 1. Labandeira CC

    (2007) The origin of herbivory on land: initial patterns of plant tissue consumption by arthropods

    Sect Science 14:259–275.

    https://doi.org/10.1111/j.1744-7917.2007.00152.x

    • Google Scholar
46. 1. Lehmann OER
    2. Ezcurra MD
    3. Butler RJ
    4. Lloyd GT
    5. Angielczyk K

    (2019) Biases with the Generalized Euclidean Distance measure in disparity analyses with high levels of missing data

    Palaeontology 62:837–849.

    https://doi.org/10.1111/pala.12430

    • Google Scholar
47. 1. Lloyd GT

    (2016) Estimating morphological diversity and tempo with discrete character-taxon matrices: implementation, challenges, progress, and future directions

    Biological Journal of the Linnean Society 118:131–151.

    https://doi.org/10.1111/bij.12746

    • Google Scholar
48. 1. McKenna DD
    2. Shin S
    3. Ahrens D
    4. Balke M
    5. Beza-Beza C
    6. Clarke DJ
    7. Donath A
    8. Escalona HE
    9. Friedrich F
    10. Letsch H
    11. Liu SL
    12. Maddison D
    13. Mayer C
    14. Misof B
    15. Murin PJ
    16. Niehuis O
    17. Peters RS
    18. Podsiadlowski L
    19. Pohl H
    20. Scully ED
    21. Yan EV
    22. Zhou X
    23. Ślipiński A
    24. Beutel RG

    (2019) The evolution and genomic basis of beetle diversity

    PNAS 116:24729–24737.

    https://doi.org/10.1073/pnas.1909655116

    • PubMed
    • Google Scholar
49. 1. Montagna M
    2. Tong KJ
    3. Magoga G
    4. Strada L
    5. Tintori A
    6. Ho SYW
    7. Lo N

    (2019) Recalibration of the insect evolutionary time scale using Monte San Giorgio fossils suggests survival of key lineages through the End-Permian Extinction

    Proceedings. Biological Sciences 286:20191854.

    https://doi.org/10.1098/rspb.2019.1854

    • PubMed
    • Google Scholar
50. 1. Naugolnykh SV
    2. Ponomarenko AG

    (2010) Possible traces of feeding by beetles in coniferophyte wood from the Kazanian of the Kama River Basin

    Paleontological Journal 44:468–474.

    https://doi.org/10.1134/S0031030110040131

    • Google Scholar
51. 1. Nelsen MP
    2. DiMichele WA
    3. Peters SE
    4. Boyce CK

    (2016) Delayed fungal evolution did not cause the Paleozoic peak in coal production

    PNAS 113:2442–2447.

    https://doi.org/10.1073/pnas.1517943113

    • PubMed
    • Google Scholar
52. 1. Nowak H
    2. Schneebeli-Hermann E
    3. Kustatscher E

    (2019) No mass extinction for land plants at the Permian-Triassic transition

    Nature Communications 10:384.

    https://doi.org/10.1038/s41467-018-07945-w

    • PubMed
    • Google Scholar
53. 1. Nowak H
    2. Vérard C
    3. Kustatscher E

    (2020) Palaeophytogeographical Patterns Across the Permian–Triassic Boundary

    Frontiers in Earth Science 8:613350.

    https://doi.org/10.3389/feart.2020.613350

    • Google Scholar
54. 1. Pan Y
    2. Birdsey RA
    3. Fang J
    4. Houghton R
    5. Kauppi PE
    6. Kurz WA
    7. Phillips OL
    8. Shvidenko A
    9. Lewis SL
    10. Canadell JG
    11. Ciais P
    12. Jackson RB
    13. Pacala SW
    14. McGuire AD
    15. Piao S
    16. Rautiainen A
    17. Sitch S
    18. Hayes D

    (2011) A large and persistent carbon sink in the world’s forests

    Science 333:988–993.

    https://doi.org/10.1126/science.1201609

    • PubMed
    • Google Scholar
55. 1. Pearson MR
    2. Benson RBJ
    3. Upchurch P
    4. Fröbisch J
    5. Kammerer CF

    (2013) Reconstructing the diversity of early terrestrial herbivorous tetrapods

    Palaeogeography, Palaeoclimatology, Palaeoecology 372:42–49.

    https://doi.org/10.1016/j.palaeo.2012.11.008

    • Google Scholar
56. 1. Ponomarenko AG

    (1969)

    Historical development of archostematan beetles

    Trudy Paleontologicheskogo Instituta AN SSSR 125:1–240.

    • Google Scholar
57. 1. Ponomarenko AG

    (2003)

    Ecological evolution of beetles (Insecta: Coleoptera)

    Acta Zoologica Cracoviensia 46:319–328.

    • Google Scholar
58. 1. Ponomarenko AG

    (2004)

    Beetles (Insecta, Coleoptera) of the late Permian and early Triassic

    Paleontological Journal 38:S185–S196.

    • Google Scholar
59. 1. Ponomarenko AG

    (2016) Insects during the time around the Permian—Triassic crisis

    Paleontological Journal 50:174–186.

    https://doi.org/10.1134/S0031030116020052

    • Google Scholar
60. 1. Reich PB
    2. Luo YJ
    3. Bradford JB
    4. Poorter H
    5. Perry CH
    6. Oleksyn J

    (2014) Temperature drives global patterns in forest biomass distribution in leaves, stems, and roots

    PNAS 111:13721–13726.

    https://doi.org/10.1073/pnas.1216053111

    • PubMed
    • Google Scholar
61. 1. Retallack GJ
    2. Veevers JJ
    3. Morante R

    (1996) Global coal gap between Permian–Triassic extinction and Middle Triassic recovery of peat-forming plants

    Geological Society of America Bulletin 108:195–207.

    https://doi.org/10.1130/0016-7606(1996)108<0195:GCGBPT>2.3.CO;2

    • Google Scholar
62. 1. Šamonil P
    2. Phillips JD
    3. Pawlik Ł

    (2020) Indirect biogeomorphic and soil evolutionary effects of spruce bark beetle

    Global and Planetary Change 195:103317.

    https://doi.org/10.1016/j.gloplacha.2020.103317

    • Google Scholar
63. 1. Schachat SR
    2. Labandeira CC
    3. Clapham ME
    4. Payne JL

    (2019) A Cretaceous peak in family-level insect diversity estimated with mark-recapture methodology

    Proceedings. Biological Sciences 286:2054.

    https://doi.org/10.1098/rspb.2019.2054

    • PubMed
    • Google Scholar
64. 1. Schachat SR
    2. Labandeira CC
    3. Dyer L

    (2021) Are insects heading toward their first mass extinction? Distinguishing turnover from crises in their fossil record

    Annals of the Entomological Society of America 114:99–118.

    https://doi.org/10.1093/aesa/saaa042

    • Google Scholar
65. 1. Schneebeli-Hermann E
    2. Hochuli PA
    3. Bucher H

    (2017) Palynofloral associations before and after the Permian–Triassic mass extinction, Kap Stosch, East Greenland

    Global and Planetary Change 155:178–195.

    https://doi.org/10.1016/j.gloplacha.2017.06.009

    • Google Scholar
66. 1. Schobben M
    2. Foster WJ
    3. Sleveland ARN
    4. Zuchuat V
    5. Svensen HH
    6. Planke S
    7. Bond DPG
    8. Marcelis F
    9. Newton RJ
    10. Wignall PB
    11. Poulton SW

    (2020) A nutrient control on marine anoxia during the end-Permian mass extinction

    Nature Geoscience 13:640–646.

    https://doi.org/10.1038/s41561-020-0622-1

    • Google Scholar
67. 1. Seibold S
    2. Rammer W
    3. Hothorn T
    4. Seidl R
    5. Ulyshen MD
    6. Lorz J
    7. Cadotte MW
    8. Lindenmayer DB
    9. Adhikari YP
    10. Aragón R
    11. Bae S
    12. Baldrian P
    13. Barimani Varandi H
    14. Barlow J
    15. Bässler C
    16. Beauchêne J
    17. Berenguer E
    18. Bergamin RS
    19. Birkemoe T
    20. Boros G
    21. Brandl R
    22. Brustel H
    23. Burton PJ
    24. Cakpo-Tossou YT
    25. Castro J
    26. Cateau E
    27. Cobb TP
    28. Farwig N
    29. Fernández RD
    30. Firn J
    31. Gan KS
    32. González G
    33. Gossner MM
    34. Habel JC
    35. Hébert C
    36. Heibl C
    37. Heikkala O
    38. Hemp A
    39. Hemp C
    40. Hjältén J
    41. Hotes S
    42. Kouki J
    43. Lachat T
    44. Liu J
    45. Liu Y
    46. Luo Y-H
    47. Macandog DM
    48. Martina PE
    49. Mukul SA
    50. Nachin B
    51. Nisbet K
    52. O’Halloran J
    53. Oxbrough A
    54. Pandey JN
    55. Pavlíček T
    56. Pawson SM
    57. Rakotondranary JS
    58. Ramanamanjato J-B
    59. Rossi L
    60. Schmidl J
    61. Schulze M
    62. Seaton S
    63. Stone MJ
    64. Stork NE
    65. Suran B
    66. Sverdrup-Thygeson A
    67. Thorn S
    68. Thyagarajan G
    69. Wardlaw TJ
    70. Weisser WW
    71. Yoon S
    72. Zhang N
    73. Müller J

    (2021) The contribution of insects to global forest deadwood decomposition

    Nature 597:77–81.

    https://doi.org/10.1038/s41586-021-03740-8

    • PubMed
    • Google Scholar
68. 1. Seidl R
    2. Klonner G
    3. Rammer W
    4. Essl F
    5. Moreno A
    6. Neumann M
    7. Dullinger S

    (2018) Invasive alien pests threaten the carbon stored in Europe’s forests

    Nature Communications 9:1626.

    https://doi.org/10.1038/s41467-018-04096-w

    • PubMed
    • Google Scholar
69. 1. Shen S
    2. Crowley JL
    3. Wang Y
    4. Bowring SA
    5. Erwin DH
    6. Sadler PM
    7. Cao C
    8. Rothman DH
    9. Henderson CM
    10. Ramezani J
    11. Zhang H
    12. Shen Y
    13. Wang X
    14. Wang W
    15. Mu L
    16. Li W
    17. Tang Y
    18. Liu X
    19. Liu L
    20. Zeng Y
    21. Jiang Y
    22. Jin Y

    (2011) Calibrating the end-Permian mass extinction

    Science 334:1367–1372.

    https://doi.org/10.1126/science.1213454

    • PubMed
    • Google Scholar
70. 1. Simões TR
    2. Vernygora O
    3. Caldwell MW
    4. Pierce SE

    (2020) Megaevolutionary dynamics and the timing of evolutionary innovation in reptiles

    Nature Communications 11:3322.

    https://doi.org/10.1038/s41467-020-17190-9

    • PubMed
    • Google Scholar
71. 1. Smith DM
    2. Marcot JD

    (2015) The fossil record and macroevolutionary history of the beetles

    Proceedings. Biological Sciences 282:20150060.

    https://doi.org/10.1098/rspb.2015.0060

    • PubMed
    • Google Scholar
72. 1. Stork NE

    (2018) How Many Species of Insects and Other Terrestrial Arthropods Are There on Earth?

    Annual Review of Entomology 63:31–45.

    https://doi.org/10.1146/annurev-ento-020117-043348

    • PubMed
    • Google Scholar
73. 1. Sues HD
    2. Reisz RR

    (1998) Origins and early evolution of herbivory in tetrapods

    Trends in Ecology & Evolution 13:141–145.

    https://doi.org/10.1016/S0169-5347(97)01257-3

    • Google Scholar
74. 1. Sun YD
    2. Joachimski MM
    3. Wignall PB
    4. Yan CB
    5. Chen YL
    6. Jiang HS
    7. Wang LN
    8. Lai XL

    (2012) Lethally hot temperatures during the Early Triassic greenhouse

    Science 338:366–370.

    https://doi.org/10.1126/science.1224126

    • PubMed
    • Google Scholar
75. 1. Tapanila L
    2. Roberts EM

    (2012) The earliest evidence of holometabolan insect pupation in conifer wood

    PLOS ONE 7:e31668.

    https://doi.org/10.1371/journal.pone.0031668

    • PubMed
    • Google Scholar
76. 1. Tong Y-J
    2. Yang H-D
    3. Jenkins Shaw J
    4. Yang X-K
    5. Bai M

    (2021) The relationship between genus/species richness and morphological diversity among subfamilies of jewel beetles

    Sects 12:24.

    https://doi.org/10.3390/insects12010024

    • PubMed
    • Google Scholar
77. 1. Toussaint EFA
    2. Seidel M
    3. Arriaga‐varela E
    4. Hájek J
    5. Král D
    6. Sekerka L
    7. Short AEZ
    8. Fikáček M

    (2016) The peril of dating beetles

    Systematic Entomology 42:1–10.

    https://doi.org/10.1111/syen.12198

    • Google Scholar
78. 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

    • PubMed
    • Google Scholar
79. Book

    1. Ulyshen MD

    (2018) Saproxylic Insects: Diversity, Ecology and Conservation

    Springer.

    https://doi.org/10.1007/978-3-319-75937-1

    • Google Scholar
80. 1. Vajda V
    2. McLoughlin S
    3. Mays C
    4. Frank TD
    5. Fielding CR
    6. Tevyaw A
    7. Lehsten V
    8. Bocking M
    9. Nicoll RS

    (2020) End-Permian (252 Mya) deforestation, wildfires and flooding—an ancient biotic crisis with lessons for the present

    Earth and Planetary Science Letters 529:115875.

    https://doi.org/10.1016/j.epsl.2019.115875

    • Google Scholar
81. 1. van Klink R
    2. Bowler DE
    3. Gongalsky KB
    4. Swengel AB
    5. Gentile A
    6. Chase JM

    (2020) Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances

    Science 368:417–420.

    https://doi.org/10.1126/science.aax9931

    • PubMed
    • Google Scholar
82. 1. Viglietti PA
    2. Benson RBJ
    3. Smith RMH
    4. Botha J
    5. Kammerer CF
    6. Skosan Z
    7. Butler E
    8. Crean A
    9. Eloff B
    10. Kaal S
    11. Mohoi J
    12. Molehe W
    13. Mtalana N
    14. Mtungata S
    15. Ntheri N
    16. Ntsala T
    17. Nyaphuli J
    18. October P
    19. Skinner G
    20. Strong M
    21. Stummer H
    22. Wolvaardt FP
    23. Angielczyk KD

    (2021) Evidence from South Africa for a protracted end-Permian extinction on land

    PNAS 118:e2017045118.

    https://doi.org/10.1073/pnas.2017045118

    • Google Scholar
83. 1. Wagner DL
    2. Grames EM
    3. Forister ML
    4. Berenbaum MR
    5. Stopak D

    (2021) Insect decline in the Anthropocene: death by a thousand cuts

    PNAS 118:e2023989118.

    https://doi.org/10.1073/pnas.2023989118

    • PubMed
    • Google Scholar
84. 1. Wills MA

    (1998) Crustacean disparity through the Phanerozoic: comparing morphological and stratigraphic data

    Biological Journal of the Linnean Society 65:455–500.

    https://doi.org/10.1111/j.1095-8312.1998.tb01149.x

    • Google Scholar
85. 1. Wills MA
    2. Briggs DEG
    3. Fortey RA

    (2016) Disparity as an evolutionary index: a comparison of Cambrian and Recent arthropods

    Paleobiology 20:93–130.

    https://doi.org/10.1017/S009483730001263X

    • Google Scholar
86. 1. Wu Y
    2. Chu D
    3. Tong J
    4. Song H
    5. Dal Corso J
    6. Wignall PB
    7. Song H
    8. Du Y
    9. Cui Y

    (2021) Six-fold increase of atmospheric pCO2 during the Permian–Triassic mass extinction

    Nature Communications 12:2137.

    https://doi.org/10.1038/s41467-021-22298-7

    • Google Scholar
87. 1. Yang LH
    2. Gratton C

    (2014) Insects as drivers of ecosystem processes

    Current Opinion in Insect Science 2:26–32.

    https://doi.org/10.1016/j.cois.2014.06.004

    • PubMed
    • Google Scholar
88. 1. Zhang SQ
    2. Che LH
    3. Li Y
    4. Pang H
    5. Ślipiński A
    6. Zhang P

    (2018) Evolutionary history of Coleoptera revealed by extensive sampling of genes and species

    Nature Communications 9:205.

    https://doi.org/10.1038/s41467-017-02644-4

    • PubMed
    • Google Scholar
89. 1. Zhao XD
    2. Zheng DR
    3. Xie GW
    4. Jenkyns HC
    5. Guan CG
    6. Fang YN
    7. He J
    8. Yuan XL
    9. Xue NH
    10. Wang H
    11. Li S
    12. Jarzembowski EA
    13. Zhang HC
    14. Wang B

    (2020) Recovery of lacustrine ecosystems after the end-Permian mass extinction

    Geology 48:609–613.

    https://doi.org/10.1130/G47502.1

    • Google Scholar

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.

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).”

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

   "This ORCID iD identifies the author of this article:" 0000-0002-8001-9937

• 1,339

  Page views

• 216

  Downloads

• 10

  Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.