New Cretaceous crickets of the subfamilies Nemobiinae and Podoscirtinae (Orthoptera, Grylloidea: Trigonidiidae, Oecanthidae) attest the antiquity of these clades

Abstract Fossils are more and more used in phylogenetic evolutionary studies either for clade calibration, or as terminals in a dataset including morphological characters. The strength of these methodological advances relies however on the quality and completeness of the fossil record. For crickets (Insecta, Orthoptera, Gryllidea), few ancient (pre-Cenozoic) well-preserved fossils are known, except for isolated wings often classified in purely fossil groups and a few fossils found in Cretaceous amber. Here, we present two remarkable fossils from mid-Cretaceous amber of France, that were imaged using X-ray synchrotron microtomography and exhibit an exquisite preservation allowing description with a precision similar to that of extant taxa. Palaeonemobius occidentalis Laurent and Desutter-Grandcolas, gen. nov., sp. nov. and Picogryllus carentonensis Josse and Desutter-Grandcolas, gen. nov., sp. nov. are the oldest representatives of the Nemobiinae and Podoscirtinae subfamilies of the Trigonidiidae and Oecanthidae families respectively. P. carentonensis Josse and Desutter-Grandcolas, gen. nov., sp. nov. is also the smallest adult male with a full stridulatory apparatus ever documented in crickets (body length 3.3 mm), and the first taxon of the cricket clade for which male genitalia can be partly described. We discuss the significance of Cretaceous fossils of crickets for future evolutionary studies of this clade.

[1]  Li-Bin Ma,et al.  The Oldest Representatives of Tree Crickets (Orthoptera: Gryllidae; Oecanthinae) from Northern Myanmar , 2022, Insects.

[2]  Zhe-Yuan Yu,et al.  A new genus with a new species of cricket from mid-Cretaceous Burmese Kachin amber (Orthoptera: Trigonidiidae) , 2022, Cretaceous Research.

[3]  He Wang,et al.  Chunxiania fania: a new genus and species of mole cricket (Orthoptera: Ensifera: Gryllotalpidae) from mid-Cretaceous Kachin amber , 2022, Cretaceous Research.

[4]  M. Tan,et al.  Phylogeny, systematics and evolution of calling songs of the Lebinthini crickets (Orthoptera, Grylloidea, Eneopterinae), with description of two new genera , 2021, Systematic Entomology.

[5]  Sylvain Hugel,et al.  Updated diagnoses for the cricket family Trigonidiidae (Insecta: Orthoptera: Grylloidea) and its subfamilies (Trigonidiinae, Nemobiinae), with a review of the fossil record , 2021 .

[6]  A. V. Gorochov.  The Oldest Representative of the Superfamily Hagloidea (Orthoptera) from the Upper Permian of Russia, with Remarks on Katydid-Like Forms from the Paleozoic , 2021, Paleontological journal.

[7]  F. Legendre,et al.  Including fossils in phylogeny: a glimpse into the evolution of the superfamily Evanioidea (Hymenoptera: Apocrita) under tip-dating and the fossilized birth–death process , 2021, Zoological Journal of the Linnean Society.

[8]  A. Nel.  Impact of the choices of calibration points for molecular dating: a case study of Ensifera , 2021, Palaeoentomology.

[9]  Sylvain Hugel,et al.  New intertidal crickets from Comoros and Mascarene islands (Orthoptera: Trigonidiidae: Nemobiinae: Burcini). , 2021, Zootaxa.

[10]  Zhu-Qing He,et al.  A new species of Parapteronemobius from Zhejiang, China (Orthoptera: Trigonidiidae: Nemobiinae). , 2021, Zootaxa.

[11]  P. Grandcolas,et al.  Revising dating estimates and the antiquity of eusociality in termites using the fossilized birth–death process , 2021, Systematic Entomology.

[12]  L. Desutter‐Grandcolas,et al.  Colonization of different biomes drove the diversification of the Neotropical Eidmanacris crickets (Insecta: Orthoptera: Grylloidea: Phalangopsidae) , 2021, PloS one.

[13]  Zhu-Qing He,et al.  The first phylogenetic study of sword-tail crickets from China inferred from COI, 18S and 28S genes, with the establishment of two new genera and description of one new species (Orthoptera: Grylloidea: Trigonidiidae). , 2020, Zootaxa.

[14]  J. Hyvönen,et al.  Defying death: incorporating fossils into the phylogeny of the complex thalloid liverworts (Marchantiidae, Marchantiophyta) confirms high order clades but reveals discrepancies in family‐level relationships , 2020, Cladistics : the international journal of the Willi Hennig Society.

[15]  Haichun Zhang,et al.  The first ground cricket (Orthoptera: Trigonidiidae: Nemobiinae) from mid-Cretaceous Burmese amber , 2020 .

[16]  H. Letsch,et al.  Phylogenomic analysis sheds light on the evolutionary pathways towards acoustic communication in Orthoptera , 2020, Nature Communications.

[17]  He Wang,et al.  A new mole cricket (Orthoptera: Gryllotalpidae) from mid-Cretaceous Burmese amber , 2020 .

[18]  Pei Guo,et al.  A pilot phylogeny study of Nemobiinae inferred from 18S, 28s and COI genes, with descriptions of two new genera and a new species from Hainan, China (Orthoptera: Grylloidea: Trigonidiidae). , 2020, Zootaxa.

[19]  P. Grandcolas,et al.  To be or not to be: postcubital vein in insects revealed by microtomography , 2020, Systematic Entomology.

[20]  Y. Su,et al.  A New Genus of Crickets (Orthoptera: Gryllidae) in Mid-Cretaceous Myanmar Amber , 2020 .

[21]  Haichun Zhang,et al.  The earliest Gryllotalpinae (Insecta, Orthoptera, Gryllotalpidae) from mid-Cretaceous Burmese amber , 2020 .

[22]  Yuan Huang,et al.  Evolutionary rates of and selective constraints on the mitochondrial genomes of Orthoptera insects with different wing types. , 2020, Molecular phylogenetics and evolution.

[23]  D. Batten,et al.  Early Cenomanian palynofloras and inferred resiniferous forests and vegetation types in Charentes (southwestern France) , 2019, Cretaceous Research.

[24]  A. Minelli,et al.  No limits: Breaking constraints in insect miniaturization. , 2019, Arthropod structure & development.

[25]  G. Kergoat,et al.  Biogeographic patterns and diversification dynamics of the genus Cardiodactylus Saussure (Orthoptera, Grylloidea, Eneopterinae) in Southeast Asia. , 2018, Molecular phylogenetics and evolution.

[26]  P. Grandcolas,et al.  3-D imaging reveals four extraordinary cases of convergent evolution of acoustic communication in crickets and allies (Insecta) , 2017, Scientific Reports.

[27]  G. Kergoat,et al.  In and out of the Neotropics: historical biogeography of Eneopterinae crickets , 2017 .

[28]  Benedict D. Chivers,et al.  Functional morphology of tegmina-based stridulation in the relict species Cyphoderris monstrosa (Orthoptera: Ensifera: Prophalangopsidae) , 2017, Journal of Experimental Biology.

[29]  Sylvain Hugel,et al.  Insect mimicry of plants dates back to the Permian , 2016, Nature Communications.

[30]  P. Grandcolas,et al.  Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis , 2016, Cladistics : the international journal of the Willi Hennig Society.

[31]  M. Whiting,et al.  300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling , 2015, Cladistics : the international journal of the Willi Hennig Society.

[32]  L. Desutter‐Grandcolas.  Phalangopsidae crickets from Tropical Africa (Orthoptera, Grylloidea), with descriptions of new taxa and an identification key for African genera. , 2015, Zootaxa.

[33]  A. Polilov,et al.  Small is beautiful: features of the smallest insects and limits to miniaturization. , 2015, Annual review of entomology.

[34]  J. Huelsenbeck,et al.  The fossilized birth–death process for coherent calibration of divergence-time estimates , 2013, Proceedings of the National Academy of Sciences.

[35]  C. Labandeira,et al.  Eocene Orthoptera from Green River Formation of Wyoming (USA) , 2012 .

[36]  D. Robert,et al.  Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females , 2012, Proceedings of the National Academy of Sciences.

[37]  A. V. Gorochov.  New and little known orthopteroid insects (Polyneoptera) from fossil resins: Communication 3 , 2010 .

[38]  A. Nel,et al.  An enigmatic diapriid wasp (Insecta, Hymenoptera) from French Cretaceous amber , 2009 .

[39]  P. Tafforeau,et al.  The oldest representative of the Trichomyiinae (Diptera : Psychodidae) from the Lower Cenomanian French amber studied with phase-contrast synchrotron X-ray imaging , 2008 .

[40]  P. Vršanský.  Mesozoic relative of the common synanthropic German cockroach (Blattodea) , 2008 .

[41]  Peter Cloetens,et al.  Phase Contrast X-Ray Synchrotron Imaging: Opening Access to Fossil Inclusions in Opaque Amber , 2008, Microscopy and Microanalysis.

[42]  A. Nel,et al.  SCHIZOPTERID BUGS (INSECTA: HETEROPTERA) IN MID‐CRETACEOUS AMBERS FROM FRANCE and MYANMAR (BURMA) , 2007 .

[43]  Tamra C. Mendelson,et al.  Sexual behaviour: Rapid speciation in an arthropod , 2005, Nature.

[44]  L. Desutter‐Grandcolas.  Phylogeny and the evolution of acoustic communication in extant Ensifera (Insecta, Orthoptera) , 2003 .

[45]  James M. Clark,et al.  PROBLEMS DUE TO MISSING DATA IN PHYLOGENETIC ANALYSES INCLUDING FOSSILS: A CRITICAL REVIEW , 2003 .

[46]  O. Béthoux,et al.  Venation pattern and revision of Orthoptera sensu nov. and sister groups. Phylogeny of Palaeozoic and Mesozoic Orthoptera sensu nov. , 2002 .

[47]  Ann V. Hedrick,et al.  Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions , 2002 .

[48]  A. Nel,et al.  A new genus and species of fossil mole cricket in the Lower Cretaceous amber of Charente-Maritime, SW France (Insecta: Orthoptera: Gryllotalpidae) , 2002 .

[49]  D. Néraudeau,et al.  Un nouveau gisement à ambre insectifère et à végétaux (Albien terminal probable) : Archingeay (Charente-Maritime, France) , 2002 .

[50]  H. C. Bennet-Clark,et al.  Size and scale effects as constraints in insect sound communication , 1998 .

[51]  D. Gwynne.  Phylogeny of the Ensifera (Orthoptera): A Hypothesis Supporting Multiple Origins of Acoustical Signalling, Complex Spermatophores and Maternal Care in Crickets, Katydids, and Weta , 1995 .

[52]  D. Otte.  Evolution of Cricket Songs , 1992 .

[53]  W. Bailey.  Acoustic Behaviour of Insects: An Evolutionary Perspective , 1990 .

[54]  Martins Neto,et al.  Sistemática dos Ensifera insecta, (Orthopteroida) da Formação Santana (Cretáceo inferior do nordeste do Brasil) , 1990 .

[55]  F. E. Zeuner.  Fossil Orthoptera Ensifera , 1940, Nature.

[56]  S. Hervé,et al.  Paleocene of Menat Formation, France, reveals an extraordinary diversity of orthopterans and the last known survivor of a Mesozoic Elcanidae , 2020 .

[57]  G. Pollack,et al.  Insect Hearing , 2016, Springer Handbook of Auditory Research.

[58]  O. Béthoux.  Grylloptera - a unique origin of the stridulatory fi le in katydids, crickets, and their kin (Archaeorthoptera) , 2012, Arthropod Systematics & Phylogeny.

[59]  G. Edgecombe.  Palaeomorphology: fossils and the inference of cladistic relationships , 2010 .

[60]  S. Heads.  The first fossil spider cricket (Orthoptera: Gryllidae: Phalangopsinae): 20 million years of troglobiomorphosis or exaptation in the dark? , 2010 .

[61]  D. Jolly,et al.  Apport de données palynologiques à la reconstruction paléoenvironnementale de l’Albo-Cénomanien des Charentes (Sud-Ouest de la France) , 2005 .

[62]  E. Masure,et al.  Analyse palynologique de l’argile lignitifère à ambre de l’Albien terminal d’Archingeay (Charente-Maritime, France) , 2005 .

[63]  R. Jackson,et al.  The Evolution of Mating Systems in Insects and Arachnids: Jumping spider mating strategies: sex among cannibals in and out of webs , 1997 .

[64]  D. Otte.  Orthoptera species file , 1994 .

[65]  L. Chopard.  Some Crickets from South America (Grylloidea and Tridactyloidea) , 1956 .

[66]  W. Koenig,et al.  The Evolution of Mating Systems in Insects and Arachnids , 2022 .