Recalibration of the insect evolutionary time scale using Monte San Giorgio fossils suggests survival of key lineages through the End-Permian Extinction

Abstract

Insects are a highly diverse group of organisms and constitute more than half of all known animal species. They have evolved an extraordinary range of traits, from flight and complete metamorphosis to complex polyphenisms and advanced eusociality. Although the rich insect fossil record has helped to chart the appearance of many phenotypic innovations, data are scarce for a number of key periods. One such period is that following the End-Permian Extinction, recognized as the most catastrophic of all extinction events. We recently discovered several 240-million-year-old insect fossils in the Mount San Giorgio Lagerstätte (Switzerland-Italy) that are remarkable for their state of preservation (including internal organs and soft tissues), and because they extend the records of their respective taxa by up to 200 million years. By using these fossils as calibrations in a phylogenomic dating analysis, we present a revised time scale for insect evolution. Our date estimates for several major lineages, including the hyperdiverse crown groups of Lepidoptera, Hemiptera: Heteroptera and Diptera, are substantially older than their currently accepted post-Permian origins. We found that major evolutionary innovations, including flight and metamorphosis, appeared considerably earlier than previously thought. These results have numerous implications for understanding the evolution of insects and their resilience in the face of extreme events such as the End-Permian Extinction.

Keywords: divergence times; fossil calibration; molecular dating; phylogenomics; relaxed molecular clock.

Figure 1.

Macro photographs of the MSG fossil insects. (a) Gigamachilis triassicus (Archaeognatha: Machilidae). (b) Tintorina meridensis (Ephemeroptera: Tintorinidae). (c) Archetingis ladinica (Hemiptera: Tingidae). (d) Praedodromeus sangiorgiensis (Coleoptera: Trachipachidae). (e) Completely phosphatized stonefly nymph (Plecoptera), with a total length of 9.38 mm. (f) Phosphatized webspinner (Embioptera) of 18.3 mm in length, preserved in ventral view; fore basitarsi swollen, three segmented tarsi, hindlegs with enlarged femora; muscles and tendons are visible within the legs. (g) Coleoptera Polyphaga (not Staphyliniformia) of 2.9 mm in length preserved in dorsal/lateral view. (h) Phosphatized holometabolous larva (MCSN8531) of approximately 4 cm in length (not complete), not assigned to an order. (i) Phosphatized specimens with grasshopper-like body plan; within the abdomen, at its end, a group of tubules is visible, possibly identifiable as the Malpighian tubules; in (j) a magnification of these structures, scale bar, 200 µm. Details of image acquisition are reported in electronic supplementary material, text S1. (Online version in colour.)

Figure 2.

Comparison of age estimates for 13 key nodes obtained from three analyses employing different fossil calibration priors. For each lineage, vertical bars show the 95% credibility intervals of the age estimates; circles denote median values, and the red triangle corresponds to the age of MSG fossils. The purple dashed line corresponds to the Permo-Triassic boundary. The main comparisons are between the results of Analysis 1 (grey bars, replicating the calibration scheme used by Misof et al. [12]), Analysis 3 (yellow bars, replicating the calibration scheme used to produce fig. 1B in Tong et al. [32]) and Analysis 4 (red bars, based on the addition of the MSG fossil calibrations). We also include estimates for some nodes obtained by Wheat & Wahlberg [33] (purple bars), Ronquist et al. [34] (green bars) and Wahlberg et al. [35] (blue bars); for some of these, squares denote estimated mean values. The periods and epochs from the International Chronostratigraphic Chart v 2019/05 [36] are shown on the left. Hexa, Hexapoda; Ecto, Ectognatha; Pter, Pterygota; Holo, Holometabola; Arch, Archaeognatha; Poly, Polyneoptera incl. Zoraptera; Zora+Derm, Zoraptera + Dermaptera; Phth, Phthiraptera; Orth, Orthoptera; Hemi: Hete, Hemiptera: Heteroptera; Hymenopt, Hymenoptera; Lepidopt, Lepidoptera; Dipt, Diptera; Mississip., Mississippian; N, Neogene; Pennsylv., Pennsylvanian; Q , Quaternary; Silur, Silurian; Terreneuv., Terreneuvian. (Online version in colour.)

Figure 3.

Time-calibrated phylogenetic tree of insect evolutionary relationships. Tips show the names of taxa at ordinal and sub-ordinal levels. Bars on nodes correspond to the 95% credibility intervals of node-age estimates, with red indicating the nodes for which the median age is pushed back by more than 50 Myr. Green stars indicate the nodes calibrated with MSG fossils; yellow circles indicate nodes calibrated with other fossils. Two key evolutionary innovations in insects (wings and complete metamorphosis) are shown at the relevant nodes. Red triangles indicate Hexapoda and Insecta. Below the tree the following are shown: (i) bars with periods and epochs from the International Chronostratigraphic Chart v. 2019/05 [36]; (ii) scale axis of the tree expressed in millions of years; (iii) origin of plant groups; (iv) bar with warmer (red) and cooler (blue/dark blue) periods [37]; and (v) plot of O₂ concentration versus time according to [38]. Abbreviations as in figure 2. (Online version in colour.)