Abstract

BackgroundThe earliest fossil evidence of terrestrial animal activity is from the Ordovician, ~450 million years ago (Ma). However, there are earlier animal fossils, and most molecular clocks suggest a deep origin of animal phyla in the Precambrian, leaving open the possibility that animals colonized land much earlier than the Ordovician. To further investigate the time of colonization of land by animals, we sequenced two nuclear genes, glyceraldehyde-3-phosphate dehydrogenase and enolase, in representative arthropods and conducted phylogenetic and molecular clock analyses of those and other available DNA and protein sequence data. To assess the robustness of animal molecular clocks, we estimated the deuterostome-arthropod divergence using the arthropod fossil record for calibration and tunicate instead of vertebrate sequences to represent Deuterostomia. Nine nuclear and 15 mitochondrial genes were used in phylogenetic analyses and 61 genes were used in molecular clock analyses.ResultsSignificant support was found for the unconventional pairing of myriapods (millipedes and centipedes) with chelicerates (spiders, scorpions, horseshoe crabs, etc.) using nuclear and mitochondrial genes. Our estimated time for the divergence of millipedes (Diplopoda) and centipedes (Chilopoda) was 442 ± 50 Ma, and the divergence of insects and crustaceans was estimated as 666 ± 58 Ma. Our results also agree with previous studies suggesting a deep divergence (~1100 – 900 Ma) for arthropods and deuterostomes, considerably predating the Cambrian Explosion seen in the animal fossil record.ConclusionsThe consistent support for a close relationship between myriapods and chelicerates, using mitochondrial and nuclear genes and different methods of analysis, suggests that this unexpected result is not an artefact of analysis. We propose the name Myriochelata for this group of animals, which includes many that immobilize prey with venom. Our molecular clock analyses using arthropod fossil calibrations support earlier studies using vertebrate calibrations in finding that deuterostomes and arthropods diverged hundreds of millions of years before the Cambrian explosion. However, our molecular time estimate for the divergence of millipedes and centipedes is close to the divergence time inferred from fossils. This suggests that arthropods may have adapted to the terrestrial environment relatively late in their evolutionary history.

Highlights

  • The earliest fossil evidence of terrestrial animal activity is from the Ordovician, ~450 million years ago (Ma)

  • Support for Pancrustacea was significant in most analyses of nuclear genes and the Bayesian analysis of nuclear + mitochondrial genes

  • We have found strong statistical support for the unconventional grouping of myriapods and chelicerates, a taxon that we name Myriochelata

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Summary

Introduction

The earliest fossil evidence of terrestrial animal activity is from the Ordovician, ~450 million years ago (Ma). The earliest undisputed fossils of terrestrial plants, animals, and fungi are all from the early Palaeozoic (Ordovician and Silurian; 495 – 417 million years ago, Ma) [5,6,7,8,9]. The earliest animal fossils are known from ~600 Ma [10,11,12] and the earliest representatives of the "plant lineage", such as green algae [13] and red algae [14], from even earlier (1000 – 750 Ma and 1200 Ma, respectively) This raises the possibility that land was colonized by multicellular eukaryotes prior to the Ordovician. A previous molecular clock analysis addressed the question of land colonization by plants and fungi, resulting in early time estimates of about 700 and 1000 Ma, respectively [15]. Molecular clock analyses have not addressed the colonization of land by animals

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