Hemiptera, the fifth most diverse insect order, are characterized by their high diversity in deep time, with 145 known extinct families. However, the precise timing of the origin of Hemiptera lineages has remained uncertain. Traditional approaches, molecular clock analyses and fossil calibrations, have overlooked much of this extinct diversity by failing to incorporate key fossil data. Furthermore, no estimates have been proposed for the timing of the extinction of Hemiptera’s fossil lineages. In this study, we use the recently developed Bayesian Brownian Bridge model, which estimates the timing of lineage origin and extinction through fossil-based Bayesian modelling, to provide a temporal framework for the rise and fall of 310 major hemipteran lineages. Our results support an early Pennsylvanian origin of Hemiptera, and indicate that the major hemipteran lineages originated between the late Carboniferous and Late Permian (Pennsylvanian-Lopingian). Additionally, our analyses reveal a radiation of Hemiptera during the Permian (Guadalupian), followed by multiple extinctions of ancient hemipteran lineages from the Permo-Triassic boundary to the mid-Triassic. A second major radiation occurred during the Cretaceous, coinciding with numerous extinctions of relic and newly emerging Cretaceous lineages, highlighting a faunal turnover. Our study provides a holistic fossil-based picture of the evolutionary history of Hemiptera.

The superorder Archaeorthoptera (or total group of the extant Orthoptera) was exceedingly diverse during the Late Carboniferous and Permian. Most of the species described to date are comparatively remote relatives of Orthoptera (Archaeorthoptera nec. Panorthoptera). The Panorthoptera are a clade including species more closely related to crown Orthoptera, sharing with them synapomorphies in their wing venation, viz. division of the anterior-most branch CuPa of CuP into two branches; fusion of the anterior branch CuPaα of CuPa with CuA (or M+CuA). The Orthoptera sensu stricto are then characterized by the posterior branch of CuPa (CuPaβ) generally simple, and by the broadened (‘saltatorial’) metafemora (Béthoux & Nel, 2002). The Panorthoptera are quite rare in the early Late Carboniferous (Béthoux et al., 2012; Gu et al., 2014, 2017). Thus, any new fossil attributable to this clade is welcome to clarify the history of its diversification.

Extant ice-crawlers (Notoptera: Grylloblattidae) are wingless, ground-dwelling, relict, polyneopteran insects that live in Holarctic cold environments. Their closest living relatives are the similarly apterous bush-crawlers (Notoptera: Mantophasmatodea) from southern Africa, forming together a disjunct bipolar distribution. Meanwhile, numerous winged fossil insects have been assigned to Grylloblattodea, though the lack of defining synapomorphies has complicated efforts to clarify the evolutionary relationships between these fossils and modern wingless ice-crawlers. Here, we report a well preserved winged ice-crawler, Zygogrylloblatta longipalpa gen. et sp. nov., from the Albian/Cenomanian of northern Myanmar ( ca 99 Ma). Zygogrylloblatta has the typical forewing venation of Mesozoic ‘stem-Grylloblattodea’, but also exhibits a unique unambiguous synapomorphy of extant Grylloblattidae in male genitalia (coxae IX with apical styli), making it the only fossil accurately related to crown-group Grylloblattidae. In contrast to ground-dwelling habits of extant ice-crawlers, Zygogrylloblatta has well developed wings, arolia and true foot pads, supporting a specialized arboreal lifestyle during the mid-Cretaceous. We demonstrate that Grylloblattidae diverged from some winged, arboreal ancestors prior to the mid-Cretaceous, bridging the gap between ancient stem-group and extant Grylloblattidae. Our results reveal previously unknown ecological and morphological diversity in early ice-crawlers and highlight the significance of transitional fossils in tracing the origin of this enigmatic insect lineage.