1. Author Response:

    Reviewer #1:

    The manuscript entitled, "Early evolution of beetles regulated by the end-Permian deforestation" by Zhao et al. is a strong, interesting, and well-written study worthy of publication after revision.

    The authors met their goal of documenting and analyzing the diversity of Paleozoic beetle taxonomy, morphological disparity, ecosystem roles, and phylogeny. This, in my opinion, is the strongest portion of the paper as it brings several lines of evidence to show the high diversity of xylophagous beetles, up until the EPME, followed by a distinct extinction of xylophagous beetles and the expansion of ecological roles into a more modern component of beetles.

    A distinct weakness of the paper is the reliance of correlation between biochemical cycling and the evolution of beetles. To address this, we would ideally see isotopic data associated with these statements. My overall suggestion is to make clear that this is speculative and bring other hypotheses to the table, and hopefully rule them out. It isn't very helpful to say something like xylophagous beetles were the main source of nutrient cycling in the Permian without discussing fungus at greater length. Or similarly, implying a drop in O2 was caused by beetles, without describing any of the other biotic/abiotic things going on at that time.

    We really appreciate those insightful comments, and completely agreed that the correlation between carbon cycling and Permian beetles is speculative. We followed the reviewer’s suggestion and toned down the discussion about this correlation. The role of ancient insects in deep-time forest carbon cycle is unclear, partly because the contribution of extant insects to the decomposition of deadwood is poorly understood. Fortunately, a paper published last month reveals the functional importance of insects in the decomposition of deadwood and the forest carbon cycle (Seibold et al., 2021), and thus provide a further support for our conclusion. We added this reference to our paper. Moreover, regarding the Permian biochemical cycling change, we also have added an introduction about other two hypotheses (reduction in the extent of coal swamps and the evolution of lignin-consuming fungi) and ruled them out in the Discussion.

    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 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).”

    Please see lines 261–264:

    “In extant forest ecosystems, insects may account for 29 percent of the total carbon flux from deadwood and thus they have a functional importance in the decomposition of deadwood and the carbon cycle (Seibold et al., 2021).”

    Please see lines 266–269:

    “Permian beetles had probably evolved close interactions with various microorganisms especially lignin-consuming fungi (Nelsen et al., 2016), which also accelerated the decomposition of deadwood.”

    We have added 7 references.

    Berner RA. 2009. Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. American Journal of Science 309: 603–606.

    Dahl TW, Hammarlund EU, Anbar AD, Bond DPG, Gill BC, Gordon GW, Knoll AH, Nielsen AT, Schovsbo NH, and Canfield DE. 2010. Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. PNAS 107: 17911–17915.

    Krause AJ, Mills BJW, Zhang S, Planavsky NJ, Lenton TM, Poulton SW. 2018. Stepwise oxygenation of the Paleozoic atmosphere. Nature Communications 9: 4081.

    Berner RA, Canfield DE. 1989. A new model for atmospheric oxygen over Phanerozoic time. American Journal of Science 289: 333–361.

    Nelsen MP, DiMichele WA, Peters SE, Boyce CK. 2016. Delayed fungal evolution did not cause the Paleozoic peak in coal production. PNAS 113: 2442–2447.

    Floudas TD, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, Vries RPD, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, Labutti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, Mclaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, John FSt, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS. 2012. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715–1719.

    Seibold S, Rammer W, Hothorn T, Seidl R, Ulyshen MD, Lorz J, Cadotte MW, Lindenmayer DB, Adhikari YP, Aragón R, Bae S, Baldrian P, Varandi HB, Barlow J, Bässler C, Beauchêne J, Berenguer E, Bergamin RS, Birkemoe T, Boros G, Brandl R, Brustel H, Burton PJ, Cakpo-Tossou YT, Castro J, Cateau E, Cobb TP, Farwig N, Fernández RD, Firn J, Gan KS, González G, Gossner MM, Habel JC, Hébert C, Heibl C, Heikkala O, Hemp A, Hemp C, Hjältén J, Hotes S, Kouki J, Lachat T, Liu J, Liu Y, Luo YH, Macandog DM, Martina PE, Mukul SA, Nachin B, Nisbet K, O’Halloran J, Oxbrough A, Pandey JN, Pavlíček T, Pawson SM, Rakotondranary JS, Ramanamanjato JB, Rossi L, Schmidl J, Schulze M, Seaton S, Stone MJ, Stork NE, Suran B, Thygeson AS, Thorn S, Thyagarajan G, Wardlaw TJ, Weisser WW, Yoon S, Zhang NL, Müller J. 2021. The contribution of insects to global forest deadwood decomposition. Nature 597: 77–81.

    Below are some more detailed suggestions:

    -It would be helpful to address the evolution of lignin-consuming fungi. Whether or not you can tie fungal symbiosis into the evolution of these beetles, fungal decomposition may (or may not) have accelerated in the Early Permian due to the timeline of particular clades of fungi. Worth a quick sentence or two. See relevant references below.

    Nelsen, M.P., DiMichele, W.A., Peters, S.E. and Boyce, C.K., 2016. Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proceedings of the National Academy of Sciences, 113(9), pp.2442-2447.

    Floudas D, et al. (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715-1719.Abstract/FREE Full TextGoogle Scholar

    Kohler A, et al., Mycorrhizal Genomics Initiative Consortium (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47(4):410-415.CrossRefPubMedGoogle Scholar

    Thank you very much for pointing out this issue. We complete agreed with the reviewer that Permian beetles had probably evolved close interactions with fungi, which also accelerated the decomposition of deadwood. We have revised the text and added the references based on the reviewer’s comments and suggestions. Please see comment 1.

    For the concluding paragraph in the Discussion, there is no acknowledgment to modern studies of xylophagous beetles in relation to climate change. There are many studies of the effects on climate change and xylophagous beetles, ex the North American pine bark beetles. Might be worth saying that the diversity and abundance of xylophagous beetles are extremely sensitive to climate change and can cause forest collapse too.

    Thank you. We have added a sentence and two new references about extant xylophagous beetles and climate change in the concluding paragraph. Please see lines 328–330:

    “In particular, the diversity and abundance of xylophagous beetles are extremely sensitive to climate change and can also cause forest collapse and carbon cycle disturbance (Kurz et al., 2008; Fei et al., 2019; Šamonil et al., 2020).”

    Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L. 2008. Mountain pine beetle and forest carbon feedback to climate change. Nature 452: 987–990.

    Šamonil P, Phillips JD, Pawlik Ł. 2020. Indirect biogeomorphic and soil evolutionary effects of spruce bark beetle. Global and Planetary Change 195: 103317.

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  2. Evaluation Summary:

    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.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)

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  3. Reviewer #1 (Public Review):

    The manuscript entitled, "Early evolution of beetles regulated by the end-Permian deforestation" by Zhao et al. is a strong, interesting, and well-written study worthy of publication after revision.

    The authors met their goal of documenting and analyzing the diversity of Paleozoic beetle taxonomy, morphological disparity, ecosystem roles, and phylogeny. This, in my opinion, is the strongest portion of the paper as it brings several lines of evidence to show the high diversity of xylophagous beetles, up until the EPME, followed by a distinct extinction of xylophagous beetles and the expansion of ecological roles into a more modern component of beetles.

    A distinct weakness of the paper is the reliance of correlation between biochemical cycling and the evolution of beetles. To address this, we would ideally see isotopic data associated with these statements. My overall suggestion is to make clear that this is speculative and bring other hypotheses to the table, and hopefully rule them out. It isn't very helpful to say something like xylophagous beetles were the main source of nutrient cycling in the Permian without discussing fungus at greater length. Or similarly, implying a drop in O2 was caused by beetles, without describing any of the other biotic/abiotic things going on at that time.

    Below are some more detailed suggestions:

    -It would be helpful to address the evolution of lignin-consuming fungi. Whether or not you can tie fungal symbiosis into the evolution of these beetles, fungal decomposition may (or may not) have accelerated in the Early Permian due to the timeline of particular clades of fungi. Worth a quick sentence or two. See relevant references below.

    Nelsen, M.P., DiMichele, W.A., Peters, S.E. and Boyce, C.K., 2016. Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proceedings of the National Academy of Sciences, 113(9), pp.2442-2447.

    Floudas D, et al. (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715-1719.Abstract/FREE Full TextGoogle Scholar

    Kohler A, et al., Mycorrhizal Genomics Initiative Consortium (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47(4):410-415.CrossRefPubMedGoogle Scholar

    For the concluding paragraph in the Discussion, there is no acknowledgment to modern studies of xylophagous beetles in relation to climate change. There are many studies of the effects on climate change and xylophagous beetles, ex the North American pine bark beetles. Might be worth saying that the diversity and abundance of xylophagous beetles are extremely sensitive to climate change and can cause forest collapse too.

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  4. Reviewer #2 (Public Review):

    The study aims at providing a general hypothesis about the early evolution of the megadiverse beetles (Coleoptera) in the Late Permian and Early Triassic, i.e. in the periods of major environmental changes connected to large-scale extinctions in all lineages of organisms. This is achieved by complementing the data about all known fossil beetles ever recorded from these periods, their critical revision, and the subsequent analysis of their taxon diversity over time, morphological diversity over time, and the phylogenetic relationships of the early beetle lineages.

    The principal strength of this study is, in my opinion, in the combination of the multiple evidence and multiple views on the early beetle evolution. The usual phylogenetic view, based on an updated phylogenetic hypothesis, is combined with the taxon diversity measures over time at different levels (family, genus, species), with the formal taxa included or excluded. The latter is a very important improvement to earlier studies in which these two categories were usually mixed, and hence the contribution of the hard-to-grasp formal data was difficult to evaluate. The third view is the one analyzing the morphological diversity over time, which, to my knowledge, is the very first trial to evaluate the evolution of beetles in this way. All these analyses separately show significant and important results helping us to better understand how was beetle fauna looking like in this deep past and why so many ancient groups did not survive until today. Additional insight is, however, gained by combining the results of all these three views, and putting it in the context of the known data about environmental changes, paleobotany, and geology of the P-T period. As a result, the study provides a well-supported view on the evolution of early beetles and their role in the ecosystems, and set new hypotheses which may be further tested in the future.

    There are naturally several weaknesses of the study, partly based on the fact that the studied organisms are fossils (that is, unique, often fragmentary preserved specimens) and that the number of beetle species known from the examined period is already quite high. This is reflected mainly in the phylogenetic analysis, which is reduced into very few terminal taxa, usually with a single species representing the whole family. I would also prefer to see the dataset to be newly compiled and not based on those published previously, and based on the actual examination of the respective specimens (although this is not stated anywhere in the study, my feeling is that not all included taxa were actually re-examined in detail for all characters coded). In this aspect, I strongly believe that a detailed restudy of selected fossils, resulting in a revised (rather than adopted) morphological matrix, is the desired way for future research. Also, including multiple species per family (naturally, only those in which the fossils provide enough characters) may provide a more detailed view on the phylogenetic relationships among the principal clade, and understand the morphological diversity and disparity within each clade. In this aspect, the phylogenetic analysis presented in the study can be significantly improved. However, the detailed genus-level phylogeny of early beetles was not the main purpose of this study, and I agree that the simplified analysis presented in the study provides the information needed for combining the phylogenetic data with those of the other analyses.

    Despite these limitations, the study definitely brings a novel view on the early evolution of beetles, strongly supported by multiple means of evidence, and will set a new starting point in the studies of insect diversity, beetle evolution, and environmental and climatic changes. The authors definitely reached the goal in providing the very clear hypothesis about the early evolution of beetles!

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