A double-edged sword: evolutionary novelty along deep-time diversity oscillation in an iconic group of predatory insects (Neuroptera: Mantispoidea)
Creators: name: Li, Hongyu
name: Zhuo, De
name: Wang, Bo
name: Nakamine, Hiroshi
name: Yamamoto, Shûhei
name: Zhang, Weiwei
name: Jepson, James
name: Ohl, Michael
name: Tin Nyunt, Thet
name: Aspöck, Ulrike
name: Aspöck, Horst
name: Engel, Michael S.
name: Benton, Michael
name: Donoghue, Philip
name: Liu, Xingyue
Publisher: name: Zenodo
Year: 2024
Subjects: evolutionary novelty
Macroevolution
Diversification
raptorial foreleg
fossil
insect
Mantispoidea

description: 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.
description: Funding provided by: National Natural Science Foundation of ChinaROR ID: https://ror.org/01h0zpd94Award Number: No. 31972871
Funding provided by: National Natural Science Foundation of ChinaROR ID: https://ror.org/01h0zpd94Award Number: No. 32130012
Funding provided by: National Natural Science Foundation of ChinaROR ID: https://ror.org/01h0zpd94Award Number: No. 32370484
Funding provided by: China Agricultural UniversityROR ID: https://ror.org/04v3ywz14Award Number: 
Funding provided by: Institute of ZoologyROR ID: https://ror.org/05skxkv18Award Number: 
Funding provided by: Ministry of Education of the People's Republic of ChinaROR ID: https://ror.org/01mv9t934Award Number: 
Funding provided by: Japan Society for the Promotion of ScienceROR ID: https://ror.org/00hhkn466Award Number: No. JP20J00159