Gene content evolution in the arthropods

doi:10.1186/s13059-019-1925-7

. 2020 Jan 23;21(1):15.

doi: 10.1186/s13059-019-1925-7.

Gene content evolution in the arthropods

Gregg W C Thomas¹, Elias Dohmen^{2

3

4}, Daniel S T Hughes^{5

6}, Shwetha C Murali^{5

7}, Monica Poelchau⁸, Karl Glastad^{9

10}, Clare A Anstead¹¹, Nadia A Ayoub¹², Phillip Batterham¹³, Michelle Bellair^{5

14}, Greta J Binford¹⁵, Hsu Chao⁵, Yolanda H Chen¹⁶, Christopher Childers⁸, Huyen Dinh⁵, Harsha Vardhan Doddapaneni⁵, Jian J Duan¹⁷, Shannon Dugan⁵, Lauren A Esposito¹⁸, Markus Friedrich¹⁹, Jessica Garb²⁰, Robin B Gasser¹¹, Michael A D Goodisman⁹, Dawn E Gundersen-Rindal²¹, Yi Han⁵, Alfred M Handler²², Masatsugu Hatakeyama²³, Lars Hering²⁴, Wayne B Hunter²⁵, Panagiotis Ioannidis^{26

27}, Joy C Jayaseelan⁵, Divya Kalra⁵, Abderrahman Khila²⁸, Pasi K Korhonen¹¹, Carol Eunmi Lee²⁹, Sandra L Lee⁵, Yiyuan Li³⁰, Amelia R I Lindsey^{31

32}, Georg Mayer²⁴, Alistair P McGregor³³, Duane D McKenna³⁴, Bernhard Misof³⁵, Mala Munidasa⁵, Monica Munoz-Torres^{36

37}, Donna M Muzny⁵, Oliver Niehuis³⁸, Nkechinyere Osuji-Lacy⁵, Subba R Palli³⁹, Kristen A Panfilio⁴⁰, Matthias Pechmann⁴¹, Trent Perry¹³, Ralph S Peters⁴², Helen C Poynton⁴³, Nikola-Michael Prpic^{44

45}, Jiaxin Qu⁵, Dorith Rotenberg⁴⁶, Coby Schal⁴⁷, Sean D Schoville⁴⁸, Erin D Scully⁴⁹, Evette Skinner⁵, Daniel B Sloan⁵⁰, Richard Stouthamer³¹, Michael R Strand⁵¹, Nikolaus U Szucsich⁵², Asela Wijeratne^{34

53}, Neil D Young¹¹, Eduardo E Zattara⁵⁴, Joshua B Benoit⁵⁵, Evgeny M Zdobnov²⁶, Michael E Pfrender³⁰, Kevin J Hackett⁵⁶, John H Werren⁵⁷, Kim C Worley⁵, Richard A Gibbs⁵, Ariel D Chipman⁵⁸, Robert M Waterhouse⁵⁹, Erich Bornberg-Bauer^{2

3

60}, Matthew W Hahn¹, Stephen Richards^{61

62}

Affiliations

¹ Department of Biology and Department of Computer Science, Indiana University, Bloomington, IN, USA.
² Institute for Evolution and Biodiversity, University of Münsterss, 48149, Münster, Germany.
³ Institute for Bioinformatics and Chemoinformatics, University of Hamburg, Hamburg, Germany.
⁴ Westphalian University of Applied Sciences, 45665, Recklinghausen, Germany.
⁵ Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
⁶ Present Address: Institute for Genomic Medicine, Columbia University, New York, NY, 10032, USA.
⁷ Present Address: Howard Hughes Medical Institute, Department of Genome Sciences, University of Washington, Seattle, WA, 98195, USA.
⁸ National Agricultural Library, USDA, Beltsville, MD, 20705, USA.
⁹ School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
¹⁰ Present Address: Penn Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, 19104, USA.
¹¹ Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia.
¹² Department of Biology, Washington and Lee University, 204 West Washington Street, Lexington, VA, 24450, USA.
¹³ School of BioSciences Science Faculty, The University of Melbourne, Melbourne, VIC, 3010, Australia.
¹⁴ Present Address: CooperGenomics, Houston, TX, USA.
¹⁵ Department of Biology, Lewis & Clark College, Portland, OR, 97219, USA.
¹⁶ Department of Plant and Soil Sciences, University of Vermont, Burlington, USA.
¹⁷ Beneficial Insects Introduction Research Unit, United States Department of Agriculture, Agricultural Research Service, Newark, DE, USA.
¹⁸ Institute for Biodiversity Science and Sustainability, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA, 94118, USA.
¹⁹ Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
²⁰ Department of Biological Sciences, University of Massachusetts Lowell, 198 Riverside Street, Lowell, MA, 01854, USA.
²¹ USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory, Beltsville, MD, USA.
²² USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology, 1700 S.W. 23rd Drive, Gainesville, FL, 32608, USA.
²³ Division of Insect Sciences, National Institute of Agrobiological Sciences, Owashi, Tsukuba, 305-8634, Japan.
²⁴ Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany.
²⁵ USDA ARS, U. S. Horticultural Research Laboratory, Ft. Pierce, FL, 34945, USA.
²⁶ Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.
²⁷ Present Address: Foundation for Research and Technology Hellas, Institute of Molecular Biology and Biotechnology, Vassilika Vouton, 70013, Heraklion, Greece.
²⁸ Université de Lyon, Institut de Génomique Fonctionnelle de Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, 46 allée d'Italie, 69364, Lyon, France.
²⁹ Department of Integrative Biology, University of Wisconsin, Madison, WI, 53706, USA.
³⁰ Department of Biological Sciences, University of Notre Dame, 109B Galvin Life Sciences, Notre Dame, IN, 46556, USA.
³¹ Department of Entomology, University of California Riverside, Riverside, CA, USA.
³² Present Address: Department of Biology, Indiana University, Bloomington, IN, USA.
³³ Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
³⁴ Department of Biological Sciences, University of Memphis, 3700 Walker Ave, Memphis, TN, 38152, USA.
³⁵ Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Bonn, Germany.
³⁶ Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, USA.
³⁷ Present Address: Phoenix Bioinformatics, 39221 Paseo Padre Parkway, Ste. J., Fremont, CA, 94538, USA.
³⁸ Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert Ludwig University of Freiburg, 79104, Freiburg (Brsg.), Germany.
³⁹ Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA.
⁴⁰ School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK.
⁴¹ Cologne Biocenter, Zoological Institute, Department of Developmental Biology, University of Cologne, 50674, Cologne, Germany.
⁴² Centre of Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander Koenig, Bonn, Germany.
⁴³ School for the Environment, University of Massachusetts Boston, Boston, MA, 02125, USA.
⁴⁴ Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, Georg-August-Universität Göttingen, Göttingen, Germany.
⁴⁵ Göttingen Center for Molecular Biosciences (GZMB), Georg-August-Universität Göttingen, Göttingen, Germany.
⁴⁶ Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27606, USA.
⁴⁷ Department of Entomology and W.M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, 27695, USA.
⁴⁸ Department of Entomology, University of Wisconsin-Madison, Madison, USA.
⁴⁹ Stored Product Insect and Engineering Research Unit, USDA-ARS Center for Grain and Animal Health Research, Manhattan, KS, 66502, USA.
⁵⁰ Department of Biology, Colorado State University, Ft. Collins, CO, USA.
⁵¹ Department of Entomology, University of Georgia, Athens, GA, USA.
⁵² Present Address: Arkansas Biosciences Institute, Arkansas State University, Jonesboro, AR, USA.
⁵³ Natural History Museum Vienna, Burgring 7, 1010, Vienna, Austria.
⁵⁴ INIBIOMA, Univ. Nacional del Comahue - CONICET, Bariloche, Argentina.
⁵⁵ Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
⁵⁶ Crop Production and Protection, U.S. Department of Agriculture-Agricultural Research Service, Beltsville, MD, 20705, USA.
⁵⁷ Department of Biology, University of Rochester, Rochester, NY, 14627, USA.
⁵⁸ Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel.
⁵⁹ Department of Ecology & Evolution and Swiss Institute of Bioinformatics, University of Lausanne, 1015, Lausanne, Switzerland.
⁶⁰ Department Protein Evolution, Max Planck Institute for Developmental Biology, Tübingen, Germany.
⁶¹ Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. srichards@ucdavis.edu.
⁶² Present Address: UC Davis Genome Center, University of California, Davis, CA, 95616, USA. srichards@ucdavis.edu.

PMID: 31969194
PMCID: PMC6977273
DOI: 10.1186/s13059-019-1925-7

Gene content evolution in the arthropods

Gregg W C Thomas et al. Genome Biol. 2020.

. 2020 Jan 23;21(1):15.

doi: 10.1186/s13059-019-1925-7.

Authors

Affiliations

¹ Department of Biology and Department of Computer Science, Indiana University, Bloomington, IN, USA.
² Institute for Evolution and Biodiversity, University of Münsterss, 48149, Münster, Germany.
³ Institute for Bioinformatics and Chemoinformatics, University of Hamburg, Hamburg, Germany.
⁴ Westphalian University of Applied Sciences, 45665, Recklinghausen, Germany.
⁵ Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
⁶ Present Address: Institute for Genomic Medicine, Columbia University, New York, NY, 10032, USA.
⁷ Present Address: Howard Hughes Medical Institute, Department of Genome Sciences, University of Washington, Seattle, WA, 98195, USA.
⁸ National Agricultural Library, USDA, Beltsville, MD, 20705, USA.
⁹ School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
¹⁰ Present Address: Penn Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, 19104, USA.
¹¹ Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia.
¹² Department of Biology, Washington and Lee University, 204 West Washington Street, Lexington, VA, 24450, USA.
¹³ School of BioSciences Science Faculty, The University of Melbourne, Melbourne, VIC, 3010, Australia.
¹⁴ Present Address: CooperGenomics, Houston, TX, USA.
¹⁵ Department of Biology, Lewis & Clark College, Portland, OR, 97219, USA.
¹⁶ Department of Plant and Soil Sciences, University of Vermont, Burlington, USA.
¹⁷ Beneficial Insects Introduction Research Unit, United States Department of Agriculture, Agricultural Research Service, Newark, DE, USA.
¹⁸ Institute for Biodiversity Science and Sustainability, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA, 94118, USA.
¹⁹ Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.
²⁰ Department of Biological Sciences, University of Massachusetts Lowell, 198 Riverside Street, Lowell, MA, 01854, USA.
²¹ USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory, Beltsville, MD, USA.
²² USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology, 1700 S.W. 23rd Drive, Gainesville, FL, 32608, USA.
²³ Division of Insect Sciences, National Institute of Agrobiological Sciences, Owashi, Tsukuba, 305-8634, Japan.
²⁴ Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany.
²⁵ USDA ARS, U. S. Horticultural Research Laboratory, Ft. Pierce, FL, 34945, USA.
²⁶ Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.
²⁷ Present Address: Foundation for Research and Technology Hellas, Institute of Molecular Biology and Biotechnology, Vassilika Vouton, 70013, Heraklion, Greece.
²⁸ Université de Lyon, Institut de Génomique Fonctionnelle de Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, 46 allée d'Italie, 69364, Lyon, France.
²⁹ Department of Integrative Biology, University of Wisconsin, Madison, WI, 53706, USA.
³⁰ Department of Biological Sciences, University of Notre Dame, 109B Galvin Life Sciences, Notre Dame, IN, 46556, USA.
³¹ Department of Entomology, University of California Riverside, Riverside, CA, USA.
³² Present Address: Department of Biology, Indiana University, Bloomington, IN, USA.
³³ Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.
³⁴ Department of Biological Sciences, University of Memphis, 3700 Walker Ave, Memphis, TN, 38152, USA.
³⁵ Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Bonn, Germany.
³⁶ Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, USA.
³⁷ Present Address: Phoenix Bioinformatics, 39221 Paseo Padre Parkway, Ste. J., Fremont, CA, 94538, USA.
³⁸ Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert Ludwig University of Freiburg, 79104, Freiburg (Brsg.), Germany.
³⁹ Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA.
⁴⁰ School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK.
⁴¹ Cologne Biocenter, Zoological Institute, Department of Developmental Biology, University of Cologne, 50674, Cologne, Germany.
⁴² Centre of Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander Koenig, Bonn, Germany.
⁴³ School for the Environment, University of Massachusetts Boston, Boston, MA, 02125, USA.
⁴⁴ Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, Georg-August-Universität Göttingen, Göttingen, Germany.
⁴⁵ Göttingen Center for Molecular Biosciences (GZMB), Georg-August-Universität Göttingen, Göttingen, Germany.
⁴⁶ Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27606, USA.
⁴⁷ Department of Entomology and W.M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, 27695, USA.
⁴⁸ Department of Entomology, University of Wisconsin-Madison, Madison, USA.
⁴⁹ Stored Product Insect and Engineering Research Unit, USDA-ARS Center for Grain and Animal Health Research, Manhattan, KS, 66502, USA.
⁵⁰ Department of Biology, Colorado State University, Ft. Collins, CO, USA.
⁵¹ Department of Entomology, University of Georgia, Athens, GA, USA.
⁵² Present Address: Arkansas Biosciences Institute, Arkansas State University, Jonesboro, AR, USA.
⁵³ Natural History Museum Vienna, Burgring 7, 1010, Vienna, Austria.
⁵⁴ INIBIOMA, Univ. Nacional del Comahue - CONICET, Bariloche, Argentina.
⁵⁵ Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.
⁵⁶ Crop Production and Protection, U.S. Department of Agriculture-Agricultural Research Service, Beltsville, MD, 20705, USA.
⁵⁷ Department of Biology, University of Rochester, Rochester, NY, 14627, USA.
⁵⁸ Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel.
⁵⁹ Department of Ecology & Evolution and Swiss Institute of Bioinformatics, University of Lausanne, 1015, Lausanne, Switzerland.
⁶⁰ Department Protein Evolution, Max Planck Institute for Developmental Biology, Tübingen, Germany.
⁶¹ Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. srichards@ucdavis.edu.
⁶² Present Address: UC Davis Genome Center, University of California, Davis, CA, 95616, USA. srichards@ucdavis.edu.

PMID: 31969194
PMCID: PMC6977273
DOI: 10.1186/s13059-019-1925-7

Abstract

Background: Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.

Results: Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.

Conclusions: These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

Keywords: Arthropods; DNA methylation; Evolution; Gene content; Genome assembly; Genomics; Protein domains.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

**Fig. 1**
OrthoDB orthology delineation for the i5K pilot species. The bars show Metazoa-level orthologs for the 76 selected arthropods and three outgroup species (of 13 outgroup species used for orthology analysis) partitioned according to their presence and copy number, sorted from the largest total gene counts to the smallest. The 28 i5K species generated in this study with a total of 533,636 gene models are indicated in bold green font. A total of 38,195 orthologous protein groups were annotated among the total 76 genomes

**Fig. 2**
Arthropod phylogeny inferred from 569 to 4097 single-copy protein-coding genes among the six multi-species orders, crustaceans, and non-spider chelicerates (Additional file 1: Table S13) and 150 single-copy genes for the orders represented by a single species and the deeper nodes. Divergence times estimated with non-parametric rate smoothing and fossil calibrations at 22 nodes (Additional file 1: Table S14). Species in bold are those sequenced within the framework of the i5K pilot project. All nodes, except those indicated with red shapes, have bootstrap support of 100 inferred by ASTRAL. Nodes of particular interest are labeled in orange and referred to in the text. Larger fonts indicate multi-species orders enabling CAFE 3.0 likelihood analyses (see “Methods”). Nodes leading to major taxonomic groups have been labeled with their node number and the number of genes inferred at that point. See Additional file 2: Figure S16 and Additional file 1: Table S12 for full node labels

**Fig. 3**
Summary of major results from gene family, protein domain, and methylation analyses. a We identify 147 gene families emerging during the evolution of insects, including several which may play an important role in insect development and adaptation. b Contrastingly, we find only ten emergent gene families during the evolution of holometabolous insects, indicating many gene families were already present during this transition. c Among all lineage nodes, we find that the node leading to Lepidoptera has the most emergent gene families. d We find that rates of gene gain and loss are highly correlated with rates of protein domain rearrangement. Leafcutter ants have experienced high rates of both types of change. e *Blattella germanica* has experienced the highest number of rapid gene family changes, possibly indicating its ability to rapidly adapt to new environments. f We observe signals of CpG methylation in all Araneae (spiders) genomes investigated (species shown: the brown recluse spider, *Loxosceles reclusa*) and the genome of the bark scorpion, *Centruroides exilicauda*. The two peaks show different CG counts in different gene features, with depletion of CG sequences in the left peak due to methylated C’s mutating to T. This suggests epigenetic control of a significant number of spider genes. Additional plots for all species in this study are shown in Additional file 2: Figure S5

**Fig. 4**
Rate of genomic change along the arthropod phylogeny: a frequency of amino acid substitutions per site, b gene gains/losses, and c domain changes. All rates are averaged per My and color-indicated as branches of the phylogenetic tree. Species names are shown on the right; specific subclades are highlighted by colors according to the taxonomic groups noted in Fig. 2

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References

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1. Medved V, Marden JH, Fescemyer HW, Der JP, Liu J, Mahfooz N, Popadic A. Origin and diversification of wings: insights from a neopteran insect. Proc Natl Acad Sci U S A. 2015;112:15946–15951. doi: 10.1073/pnas.1509517112. - DOI - PMC - PubMed
1. Nel A, Roques P, Nel P, Prokin AA, Bourgoin T, Prokop J, Szwedo J, Azar D, Desutter-Grandcolas L, Wappler T, et al. The earliest known holometabolous insects. Nature. 2013;503:257–261. doi: 10.1038/nature12629. - DOI - PubMed

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[1] Lozano-Fernandez J, Carton R, Tanner AR, Puttick MN, Blaxter M, Vinther J, Olesen J, Giribet G, Edgecombe GD, Pisani D. A molecular palaeobiological exploration of arthropod terrestrialization. Philos Trans R Soc B. 2016;371:20160133. doi: 10.1098/rstb.2015.0133. - DOI - PMC - PubMed

[2] Lozano-Fernandez J, Carton R, Tanner AR, Puttick MN, Blaxter M, Vinther J, Olesen J, Giribet G, Edgecombe GD, Pisani D. A molecular palaeobiological exploration of arthropod terrestrialization. Philos Trans R Soc B. 2016;371:20160133. doi: 10.1098/rstb.2015.0133. - DOI - PMC - PubMed

[3] Glenner H, Thomsen PF, Hebsgaard MB, Sorensen MV, Willerslev E. Evolution. The origin of insects. Science. 2006;314:1883–1884. doi: 10.1126/science.1129844. - DOI - PubMed

[4] Glenner H, Thomsen PF, Hebsgaard MB, Sorensen MV, Willerslev E. Evolution. The origin of insects. Science. 2006;314:1883–1884. doi: 10.1126/science.1129844. - DOI - PubMed

[5] Haug JT, Haug C, Garwood RJ. Evolution of insect wings and development - new details from Palaeozoic nymphs. Biol Rev Camb Philos Soc. 2015;91:53–69. doi: 10.1111/brv.12159. - DOI - PubMed

[6] Haug JT, Haug C, Garwood RJ. Evolution of insect wings and development - new details from Palaeozoic nymphs. Biol Rev Camb Philos Soc. 2015;91:53–69. doi: 10.1111/brv.12159. - DOI - PubMed

[7] Medved V, Marden JH, Fescemyer HW, Der JP, Liu J, Mahfooz N, Popadic A. Origin and diversification of wings: insights from a neopteran insect. Proc Natl Acad Sci U S A. 2015;112:15946–15951. doi: 10.1073/pnas.1509517112. - DOI - PMC - PubMed

[8] Medved V, Marden JH, Fescemyer HW, Der JP, Liu J, Mahfooz N, Popadic A. Origin and diversification of wings: insights from a neopteran insect. Proc Natl Acad Sci U S A. 2015;112:15946–15951. doi: 10.1073/pnas.1509517112. - DOI - PMC - PubMed

[9] Nel A, Roques P, Nel P, Prokin AA, Bourgoin T, Prokop J, Szwedo J, Azar D, Desutter-Grandcolas L, Wappler T, et al. The earliest known holometabolous insects. Nature. 2013;503:257–261. doi: 10.1038/nature12629. - DOI - PubMed

[10] Nel A, Roques P, Nel P, Prokin AA, Bourgoin T, Prokop J, Szwedo J, Azar D, Desutter-Grandcolas L, Wappler T, et al. The earliest known holometabolous insects. Nature. 2013;503:257–261. doi: 10.1038/nature12629. - DOI - PubMed

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Gene content evolution in the arthropods

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Gene content evolution in the arthropods

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