A double-edged sword: evolutionary novelty along deep-time diversity oscillation in an iconic group of predatory insects (Neuroptera: Mantispoidea)

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 led to lineage
constraint by intensifying competition and lowering environmental
resilience, e.g., in thorny lacewings, whose extant diversity is meager.
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 interplay 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.