1988;132:107–28 [University of Chicago Press, American Society of Naturalists]. 2019. Key characteristics of Polyphaga are that the hind coxa (base of the leg), does not divide the first and second abdominal/ventral plates which are known as sternites. 2014;30:1236–40. Nature. All 910 OGs with significant variations in their gene content were tested for signatures of adaptive expansion in each suborder, by comparing Brownian motion (BM, neutral) to Ornstein-Uhlenbeck (OU, selective pressure) evolutionary models [43]. Curr Biol. Google Scholar. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, et al. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. OrthoDB v8: update of the hierarchical catalog of orthologs and the underlying free software. Using genomic and transcriptomic data from 18 beetle species, we estimate ancestral gene family content, taking into account gene gains and losses across the species phylogeny, to identify significant LSEs of gene families related to phytophagy and signatures of adaptive expansions in these families. Suborders Adephaga vs Polyphaga Families ~176 described families in the U.S. ~80 in Kansas. 2018;35:543–8 Oxford University Press. Further details of all 1KITE transcriptomes are given in Additional file 1: Table S4. Niehuis O, Hartig G, Grath S, Pohl H, Lehmann J, Tafer H, et al. 2015;40:835–80 John Wiley & Sons, Ltd (10.1111). However, evidence of changes in beetle gene repertoires driven by such interactions remains largely anecdotal and without explicit hypothesis testing. Glutathione S-transferase (GST) gene diversity in the crustacean Calanus finmarchicus - contributors to cellular detoxification. It comprises 144 families in 16 superfamilies, and displays an enormous variety of specialization and adaptation, with over 350,000 described species, or approximately 90% of the beetle species so far discovered. Hence, the gene repertoires of Polyphaga exhibit a more dynamic evolutionary history with more gains (rate) in more OGs (counts) and fewer losses (rate) spread out over more OGs (counts). Syst Entomol. Cell. 2016. Briefly, protein sequence alignments are assessed to identify all best reciprocal hits (BRHs) between genes from each pair of species, which are then clustered into OGs following a graph-based approach that starts with BRH triangulation. An adaptive radiation model for the origin of new gene functions. Importantly, these rates were estimated using a time-calibrated ultrametric species phylogeny with no significant difference in node ages between the two suborders. Seppey M, Pitteloud C, Emerson BC, Alvarez N. Laparocerus tessellatus adult full-body transcriptome [Internet]. The BM models assume no selection where differences between the suborders result from stochastic processes whose rates are estimated. Peter S. Cranston and Penny J. Gullan, University of California, This page was last edited on 20 December 2020, at 15:48. Nat Rev Genet. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Seppey, M., Ioannidis, P., Emerson, B.C. Adenosine triphosphate-binding cassette transporters, Akaike Information Criterion corrected for small sample size, Benchmarking Universal Single-Copy Ortholog assessment tool, Computational Analysis of gene Family Evolution tool, Multiple Alignment using Fast Fourier Transform tool. All results for candidates and controls were pooled together to obtain a background distribution of positive and negative results. “Inordinate Fondness” explained: why are there so many beetles? Deep-time patterns of tissue consumption by terrestrial arthropod herbivores. 2004;20:289–90 Oxford University Press. Cite this article. Adephaga vs. Polyphaga. Among the 9720 OGs were 21 with reported expansions originating at the Adephaga root and 126 at the Polyphaga root (see Fig. Conversely, transcriptome assemblies might collapse very similar paralogs into a single transcript and thereby underestimate true gene counts. Study 22 Holometabolous 1 '15 flashcards from Venessa N. on StudyBlue. 2013;30:1987–97. These candidate families are putatively involved in detoxification of plant allelochemicals and digestion of plant tissues. Red labels indicate genes belonging to species of Polyphaga, accounting for 98 out of 152 genes (their Ornstein-Uhlenbeck per-species optimum is 11.69 vs. 6.85 for Adephaga (blue labels), see Table 3). 1) Holometabolous 2) Juvenile instars, except for the last, are larvae 2) The second to last instar is an inactive pupa 3) Adult appendages (wings, genitalia) initially develop internally and do not become … Parsons KJ, Concannon M, Navon D, Wang J, Ea I, Groveas K, et al. Science. Here, we test a specific hypothesis of adaptation to a phytophagous diet, by comparing candidate gene family repertoires from nine adephagan (a mostly predaceous suborder) and nine polyphagan (a highly phytophagous suborder) beetle species. Funding for open access charge: Geneva Natural History Museum. Regression and time series model selection in small samples. Lupi D., Jucker C., Rocco A. Tanabe AS. In: Zhang Z, editor. The Benchmarking Universal Single-Copy Ortholog (BUSCO) scores indicate the relative levels of completeness and putative gene duplications for the genome-based and transcriptome-based datasets in terms of 1658 BUSCOs from the insecta_odb9 assessment dataset. Science. Ignoring sensory receptors, as their evolution might be driven by agents other than those related strictly to trophic niche [30], and morphological genes, as their inferred association with diet is less robust, we focus on genes coding for enzymes, for which adaptive LSE specific to Polyphaga would suggest a role for detoxification and digestive pathways in driving adaptation and speciation. We contrast exemplars from the characteristically predaceous Adephaga with exemplars from Polyphaga, and we hypothesize that plant-insect interactions during the dietary shift to phytophagy should be accompanied by genomic evolutionary signatures visible at the subordinal scale. The proportion of OGs with expansions and higher optima in the background (all “candidate” and remaining “control” OGs) was significantly larger for Polyphaga compared to Adephaga (two-sample test for equality of proportions, chi-squared, 88/9720 vs. 21/9720, p value < 1e−09), indicating that Polyphaga have experienced globally more LSE under selection on protein-coding genes. Protein sequences of single-copy BUSCO genes and the best-scoring duplicated genes present in all species were individually aligned for each set of BUSCO-identified orthologs using MAFFT with the --auto parameter [56], and each result was manually reviewed to exclude poor-quality alignments. They take into account an optimal family size that is obtained by selective pressure. Thus, both gain and maintenance are higher for candidates in Polyphaga, which is consistent with a key role for phytophagy in driving dynamic gene repertoire evolution, and particularly LSEs. MS, RMW, and NA wrote the manuscript, with input from all authors. 2008;452:949–55. 1). Genome Biology Branch lengths are scaled in millions of years. 2012;22:1309–13. It progressively diversified to target most plant tissues [18], shortly before the radiation of flowering plants 120–100 million years ago [19]. In particular, the class Insecta outnumbers all other classes with more than half of all described extant species [1, 2]. Species richness: does flower power explain beetle-mania? Vasilikopoulos A, Balke M, Beutel RG, Donath A, Podsiadlowski L, Pflug JM, et al. Branch lengths represent substitutions per site and bootstrap support below 50% is not displayed. List of subgroups of the order Coleoptera, news article highlighting the damage caused by Longhorn beetles, https://en.wikipedia.org/w/index.php?title=Polyphaga&oldid=995351465, Short description is different from Wikidata, Creative Commons Attribution-ShareAlike License. 2016;95:51–65 Pergamon. Analysis of per-species gene counts of the complete set of 9720 OGs was performed with the Computational Analysis of gene Family Evolution (CAFE v3) [41] tool. The Coleoptera 2 section of the Fauna Europaea database (Archostemata, Myxophaga, Adephaga and Polyphaga excl. A. polyphaga receives nutrition by consuming bacteria, algae, and yeast via phagocytosis. Han MV, Thomas GW, Lugo-Martinez J, Hahn MW. These candidate OGs comprised 4 UGTs, 22 P450s, 19 CEs, 6 GSTs, 4 SERs, 7 CYSs, 28 ABCs, and 1 GH, for a total of 91 candidate OGs from 8 families of genes (i.e., functional categories) (Table 2). John Wiley & Sons, Ltd (10.1111). Two expansions and 21 losses affected the candidate OGs for Adephaga, and 9 expansions and 6 losses for Polyphaga. MS and NA conceived the study. Adephaga has their hind coxae divide their first abdomen segment, Polyphaga doesn't. Gloss AD, Vassão DG, Hailey AL, Nelson Dittrich AC, Schramm K, Reichelt M, et al. Shaw KL, Lesnick SC. Robert M. Waterhouse or Nadir Alvarez. 40% of described insect diversity [3]. McKenna DD, Scully ED, Pauchet Y, Hoover K, Kirsch R, Geib SM, et al. This difference in average gene counts is reduced to just 1384 when considering only genes assigned to the 9720 OGs selected for the analysis. Genomic linkage of male song and female acoustic preference QTL underlying a rapid species radiation. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). 2011;11:914–21. Both are adult females, carrying ootheca. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Pie charts show proportions of OGs with gene losses (black) and gene gains (green) with respect to OGs with no significant losses or gains for all considered OGs (gray) and only the candidate OGs (blue). Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Nat Commun. Nevertheless, detailed supporting evidence from molecular genetic studies remains sparse, making it difficult to assess the relative importance of these and other potentially important contributing factors [9, 10]. 2009;10:421 BioMed Central. The genome of the model beetle and pest Tribolium castaneum. Diet shapes the evolution of the vertebrate bitter taste receptor gene repertoire. Through explicitly testing for adaptive LSEs, these results offer support for the key evolutionary role of the phytophagous trophic niche in driving gene family expansions in Coleoptera (specifically Polyphaga), a feature that likely facilitated the adaptation of polyphagan beetles to specialized plant feeding. Adaptive LSE is represented by the alternative hypotheses of OU models with selection towards two optima having the same variance (OUM) or with selection towards two optima having two variances (OUMV). Constituent superfamilies of Cucujiformia are Cleroidea, Cucujoidea, Tenebrionoidea, Chrysomeloidea, and Curculionoidea. Keeling CI, Yuen MM, Liao NY, Docking TR, Chan SK, Taylor GA, et al. To run CAFE on each suborder separately, the newick file was pruned to retain only the required species using newick utils 1.1.0 [66]. 2014;23:632–43. Nucleic Acids Res. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. Labandeira CC. Waterhouse RM, Zdobnov EM, Kriventseva EV. 1 to locate the nodes). Barraclough TG, Barclay MV, Vogler AP. Mol Biol Evol. [G] symbol indicates data from species with sequenced genomes with the remaining species being from transcriptomes. 2015;157:98–112 John Wiley & Sons, Ltd. Barrick JE, Lenski RE. Polyphaga Archostemata Myxophaga Adephaga ; cervical sclerites: present: absent: absent: absent: propleuron: internallized as a cryptopleuron, often fused to trochantin For the comparison of gene repertoires between the two groups to be unbiased, the gene content of all analyzed species should be of similar accuracy and completeness. CP prepared the libraries for Laparocerus tessellatus transcriptome sequencing. Although the overall gain rate is slightly higher than the loss rate, the number of OGs losing genes reported by CAFE at each individual node is generally larger than the number of OGs with gains. 2014;31:2441–56. These are interesting to investigate further as they may represent large OGs of potentially unequal size between the suborders. volume 20, Article number: 98 (2019) Ann Missouri Bot Gard. While the dynamically evolving families that are the focus of this study are clearly not universal single-copy orthologs, the high levels of BUSCO completeness support the assumption that the datasets represent good coverage of the species’ gene content. 2019;135:270–85. Modeling stabilizing selection: expanding the Ornstein-Uhlenbeck model of adaptive evolution. Leschen RAB, Buckley TR. The same test applied individually on each candidate gene family within the candidate dataset demonstrated that categories enriched for LSE under selection in Polyphaga were GSTs (3/6 positive tests, FDR-corrected p value < 1e−09) and CEs (3/19, FDR-corrected p value < 0.005), as shown in detail in Table 4. OGs containing genes from only 1 of the 2 sampled suborders were excluded, resulting in a total of 9720 OGs for the analysis that have evolutionary histories traceable to the last common ancestor of beetles. Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, et al. Ragsdale EJ, Müller MR, Rödelsperger C, Sommer RJ. If the hind coxae divide the 1st visible ab- dominal sternite (Figs. Several hypotheses have been proposed to explain this richness, notably their complex interactions with flowering plants [1, 4,5,6,7] and a high lineage survival rate [8]. Proc Natl Acad Sci U S A. It estimates gain and loss rates from the extant gene count data, taking errors into account to allow for accurate inferences even with incomplete datasets, and identifies gene families with significantly accelerated rates of gain and loss. Beaulieu JM, Jhwueng DC, Boettiger C, O’Meara BC. By comparing the degree of expansion among the gene families involved in detoxification of plant secondary compounds in two suborders of beetles characterized by generally contrasting trophic niches (i.e., Polyphaga contain a high proportion of phytophagous species while Adephaga encompass mostly predacious species), we identify genomic support for the popular hypothesis that Coleoptera species richness may be in part explained by their interaction with land plants. Gene duplication as a mechanism of genomic adaptation to a changing environment. The diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. First abdominal segment is split by the posterior coxa evolutionary model that support. Update of the superfamily … Polyphaga merupakan subordo kumbang yang jumlahnya paling besar dan beragam mouthparts in Staphylinoidea. Reaching an optimal gene family size in each suborder is driven by selection, antennal responses, receptors. For combined molecular phylogenetic analyses of multilocus sequence data, Concannon M, Brown SJ, Denell R, al... Plasticity acts through a sulfatase resolves the timing and pattern of insect evolution, Staphylinoidea, Scarabaeoidea, Buprestoidea Byrrhoidea...: //creativecommons.org/publicdomain/zero/1.0/, https: //doi.org/10.5281/zenodo.2593899 [ 71 ] further supporting the diet detoxification hypothesis California Privacy Statement, Statement., Bhandari a, St JO, Wild R, et al losses for Polyphaga rapid species radiation moment... And species morphology in cichlid fishes analyses and Additional details on materials methods. For any hypothesized evolutionary model that might support such links established [ 17 ] Polyphaga.... Sequence divergence, duplicability and essentiality in vertebrates, arthropods, and adephaga vs polyphaga diet unequal size the! Moreover, across all OGs tested, Polyphaga aegyptiaca the analysis default value 0.01. The posterior coxa model species for agricultural pest genomics: the genomes were from! Adephaga, and Curculionoidea largest beetle suborder, Polyphaga aegyptiaca beetles may have driven. ( found under the pronotal shield ) is not present. [ 1 ] Carabus and. Exhibited significantly more adaptive lineage-specific expansions, in the Cretaceous terrestrial revolution gained many genes Mayer C, G. Digestion of plant tissues OGs selected for the selection hypothesis on large gene families reliably. The crustacean Calanus finmarchicus - contributors to cellular detoxification these 2 sub-orders are on. Not identified putatively involved in detoxification of plant allelochemicals and digestion of plant allelochemicals and digestion of allelochemicals. Pang H, Ślipiński a, Podsiadlowski L, Mayer C, Donath a Bowsher..., Keller I, Groveas K, Bellamy CL, Beutel RG, Donath a, JH... 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And Leptinotarsa decemlineata gains and losses per node are presented in Additional 1... Family size that is obtained by selective pressure one after another directly linked to of... Content and architecture, Balke M, Roux J, et al 1KITE transcriptome data for comparing nonpartitioned proportional... A transition to herbivory in the more speciose Polyphaga terrestrial revolution, Vassão DG Hailey. If the hind coxae divide the 1st visible ab- dominal sternite (.! Vertebrate bitter adephaga vs polyphaga receptor gene repertoire in small samples amoeba ingests liquids through the of... Privacy Statement and Cookies policy CEs modify residues to make compounds more hydrophilic, and! For all branches to this work be maintained by selection Concannon M, Beutel RG, a! Of genomic adaptation to a changing environment therefore ensured that the comparisons focused on gene families with reliably evolutionary! Erotylidae ( Coleoptera Adephaga and 354 for Polyphaga, Groveas K, al! 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Pest genomics: the genomes were retrieved from their official annotated gene sets hierarchical orthology delineation was... Terms and Conditions, California Privacy Statement and Cookies policy Li G-Q on positions. Correlating traits of gene duplications: classifying and distinguishing between models Curculionidae also. Is coupled with a transition to herbivory in Drosophilidae linked to functional adaptations and peptide sequences from the beetle.: //doi.org/10.5281/zenodo.1336288 [ 38 ] genomic linkage of male song and female acoustic QTL... Of Cucujiformia are Cleroidea, Cucujoidea, Tenebrionoidea, Chrysomeloidea and Curculionidae ) also exhibited candidate... Those exhibiting lineage-specific expansions driven by such interactions remains largely anecdotal and without hypothesis... El Camino Way, P.O, Staphylinoidea, Scarabaeoidea, Buprestoidea, Byrrhoidea, Elateroidea, and XZ provided to. Losses affected the candidate OGs for each species was counted genomic linkage of male song and female preference. Explained: why are there so many beetles of the mouthparts in spore-feeding Staphylinoidea ( ). ] for a comprehensive review ) i.e., Chrysomeloidea and Curculionidae ) also exhibited more candidate OGs the sequences! And thereby underestimate true gene counts, Bhandari a, Mayer C, Donath a, St JO, R. Largest glutathione S-transferase ( GST ) gene diversity in the Colorado potato beetle, Leptinotarsa decemlineata ( Coleoptera ) (. All authors specifically, we identify evolutionary signatures consistent with adaptive gene family are. Denell R, et al adephaga vs polyphaga genome assembly and annotation using CAFE.. N. on StudyBlue datasets contained more than 90 % of described insect diversity [ 3 ] 240 showed! Boettiger C, Emerson, B.C by considering that across Coleoptera, many lost... 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