The fossil record of spiders revisited: implications for calibrating trees and evidence for a major faunal turnover since the Mesozoic.

Studies in evolutionary biology and biogeography increasingly rely on the estimation of dated phylogenetic trees using molecular clocks. In turn, the calibration of such clocks is critically dependent on external evidence (i.e. fossils) anchoring the ages of particular nodes to known absolute ages. In recent years, a plethora of new fossil spiders, especially from the Mesozoic, have been described, while the number of studies presenting dated spider phylogenies based on fossil calibrations increased sharply. We critically evaluate 44 of these studies, which collectively employed 67 unique fossils in 180 calibrations. Approximately 54% of these calibrations are problematic, particularly regarding unsupported assignment of fossils to extant clades (44%) and crown (rather than stem) dating (9%). Most of these cases result from an assumed equivalence between taxonomic placement of fossils and their phylogenetic position. To overcome this limitation, we extensively review the literature on fossil spiders, with a special focus on putative synapomorphies and the phylogenetic placement of fossil species with regard to their importance for calibrating higher taxa (families and above) in the spider tree of life. We provide a curated list including 41 key fossils intended to be a basis for future estimations of dated spider phylogenies. In a second step, we use a revised set of 23 calibrations to estimate a new dated spider tree of life based on transcriptomic data. The revised placement of key fossils and the new calibrated tree are used to resolve a long-standing debate in spider evolution - we tested whether there has been a major turnover in the spider fauna between the Mesozoic and Cenozoic. At least 17 (out of 117) extant families have been recorded from the Cretaceous, implying that at least 41 spider lineages in the family level or above crossed the Cretaeous-Paleogene (K-Pg) boundary. The putative phylogenetic affinities of families known only from the Mesozoic suggest that at least seven Cretaceous families appear to have no close living relatives and might represent extinct lineages. There is no unambiguous fossil evidence of the retrolateral tibial apophysis clade (RTA-clade) in the Mesozoic, although molecular clock analyses estimated the major lineages within this clade to be at least ∼100 million years old. Our review of the fossil record supports a major turnover showing that the spider faunas in the Mesozoic and the Cenozoic are very distinct at high taxonomic levels, with the Mesozoic dominated by Palpimanoidea and Synspermiata, while the Cenozoic is dominated by Araneoidea and RTA-clade spiders.