Estimating the Drivers of Diversification of Stoneflies Through Time and the Limits of Their Fossil Record

Abstract

Deciphering the timing of lineage diversification and extinction has greatly benefited in the last decade from methodological developments in fossil-based analyses. If these advances are increasingly used to study the past dynamics of vertebrates, other taxa such as insects remain relatively neglected. Our understanding of how insect clades waxed and waned or of the impact of major paleoenvironmental changes during their periods of diversification and extinction (mass extinction) are rarely investigated. Here, we compile and analyze the fossil record of Plecoptera (1,742 vetted occurrences) to investigate their genus-level diversification and diversity dynamics using a Bayesian process-based model that incorporates temporal preservation biases. We found that the Permian-Triassic mass extinction has drastically impacted Plecoptera, while the Cretaceous Terrestrial Revolution corresponds with a turnover of plecopteran fauna. We also unveiled three major gaps in the plecopteran fossil record: the Carboniferous-Permian transition, the late Early Cretaceous, and the late Cenomanian to Bartonian, which will need to be further investigated. Based on the life history of extant Plecoptera, we investigate the correlations between their past dynamic and a series of biotic (Red Queen hypothesis) and abiotic (Court Jester hypothesis) factors. These analyses highlight the major role of continental fragmentation in the evolutionary history of stoneflies, which is in line with phylogeny-based biogeographic analyses showing how vicariance drove their diversification. Our study advocates analyzing the fossil record with caution, while attempting to unveil the diversification and extinction periods plus the likely triggers of these past dynamics of diversification.

Multiple drivers and lineage-specific insect extinctions during the Permo–Triassic

“…The largest extinctions of insect families may have rather occurred at the end of the Triassic period, with the demise of insect families belonging to ancient orders (i.e. that began to radiate during the Carboniferous and/or Permian like Caloneurodea, Permopsocida, Mecoptera and Plecoptera), as evidenced by species of these groups recorded during the Triassic but not thereafter 7 , 26 , 43 .…”

“…We found that drops in atmospheric O 2 may have slowed down insect diversification during both the Permian and the Triassic. Finally, continental fragmentation is considered a major driver of diversification for some insect lineages, promoting allopatric speciation but also deeply altering previous ecosystems 26 , 68 . This process was very active during the Permo–Triassic with the initiation of the Pangea fragmentation into Laurasia and Gondwana 69 .…”

“…To test correlations of insect diversification with environmental changes, we examined the link between a series of environmental variables and origination/extinction rates over a period encompassing the GEE, the LPME and the CPE but also for each extinction event. We focused on the role of nine variables, also called proxies, which have been demonstrated or assumed to be linked to extinctions and changes in insect diversity 26 , 67 .…”

“…The continental fragmentation, as approximated by plate tectonic change over time, has recently been proposed as a driver of Plecoptera dynamics 26 . Because the period studied encompasses a major geological event, the fragmentation of the supercontinent Pangea, we investigated the effect of continental fragmentation on insect diversification dynamics.…”

“…The deep-time dynamic of insect diversification (i.e. variations in origination and extinction rates) has supposedly been affected by abiotic factors such as global temperature or continental fragmentation 7,23,[26][27][28][29][30] . However, their role throughout the Permo-Triassic crises, as well as that of biotic factors such as interactions (diversity dependence) between ecological groups, have never been investigated.…”