A Double-edged Sword: Evolutionary Novelty along Deep-time Diversity Oscillation in An Iconic Group of Predatory Insects (Neuroptera: Mantispoidea)

Abstract

Evolutionary novelties are commonly identified as drivers of lineage diversification, with key innovations potentially triggering adaptive radiation. Nevertheless, testing hypotheses on the role of evolutionary novelties in promoting diversification through deep time has proven challenging. Here we unravel the role of the raptorial appendages, with evolutionary novelties for predation, in the macroevolution of a predatory insect lineage, the Superfamily Mantispoidea (mantidflies, beaded lacewings, thorny lacewings, and dipteromantispids), based on a new dated phylogeny and quantitative evolutionary analyses on modern and fossil species. We demonstrate a single origin of the raptorial foreleg and its associated novelties as key innovations triggering an early radiation of raptorial mantispoids from the Late Triassic to the Early Jurassic. Subsequently, the evolution of the raptorial foreleg influenced the diversification in different modes among lineages. At times, it might have limited the morphological diversity of other body parts and lead to lineage constraint by intensifying competition and lowering environmental resilience, e.g., in thorny lacewings, whose extant diversity is meagre. Conversely, in mantidflies, reduced emphasis on foreleg novelties and increased plasticity in other body parts may lead to better adaptation to predator-prey interactions and environmental shifts, thus maintaining a stable or accelerated level of diversification. We also reveal how major environmental change and lineage interactions interplayed with raptorial novelties in shaping the significant oscillations of mantispoid diversification over deep time, especially the abrupt shift near the mid-Cretaceous. However, by excluding a substantial portion of samples from the mid-Cretaceous of Myanmar, these shifts of some evolutionary parameters, such as morphological disparity, body size, and diversification rates, became inconspicuous and might be overestimated due to sampling bias. Our results uncover the intricate evolutionary patterns and profound significance of raptorial specializations, providing new insights into the role of novelties in forming evolutionary trajectories, both for the better and worse. [evolutionary novelty; macroevolution; diversification; raptorial foreleg; fossil; insect; Mantispoidea]