The colonization of land by animals: molecular phylogeny and divergence times among arthropods

<p>Abstract</p> <p>Background</p> <p>The 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 Precam...

Full description

Bibliographic Details
Main Authors: Lyons-Weiler Maureen, Poling Laura L, Pisani Davide, Hedges S
Format: Article
Language:English
Published: BMC 2004-01-01
Series:BMC Biology
Online Access:http://www.biomedcentral.com/1741-7007/2/1
_version_ 1818688924005957632
author Lyons-Weiler Maureen
Poling Laura L
Pisani Davide
Hedges S
author_facet Lyons-Weiler Maureen
Poling Laura L
Pisani Davide
Hedges S
author_sort Lyons-Weiler Maureen
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>The 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.</p> <p>Results</p> <p>Significant 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.</p> <p>Conclusions</p> <p>The 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.</p>
first_indexed 2024-12-17T12:01:56Z
format Article
id doaj.art-a1e050bfa703467880695fb469602419
institution Directory Open Access Journal
issn 1741-7007
language English
last_indexed 2024-12-17T12:01:56Z
publishDate 2004-01-01
publisher BMC
record_format Article
series BMC Biology
spelling doaj.art-a1e050bfa703467880695fb4696024192022-12-21T21:49:47ZengBMCBMC Biology1741-70072004-01-0121110.1186/1741-7007-2-1The colonization of land by animals: molecular phylogeny and divergence times among arthropodsLyons-Weiler MaureenPoling Laura LPisani DavideHedges S<p>Abstract</p> <p>Background</p> <p>The 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.</p> <p>Results</p> <p>Significant 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.</p> <p>Conclusions</p> <p>The 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.</p>http://www.biomedcentral.com/1741-7007/2/1
spellingShingle Lyons-Weiler Maureen
Poling Laura L
Pisani Davide
Hedges S
The colonization of land by animals: molecular phylogeny and divergence times among arthropods
BMC Biology
title The colonization of land by animals: molecular phylogeny and divergence times among arthropods
title_full The colonization of land by animals: molecular phylogeny and divergence times among arthropods
title_fullStr The colonization of land by animals: molecular phylogeny and divergence times among arthropods
title_full_unstemmed The colonization of land by animals: molecular phylogeny and divergence times among arthropods
title_short The colonization of land by animals: molecular phylogeny and divergence times among arthropods
title_sort colonization of land by animals molecular phylogeny and divergence times among arthropods
url http://www.biomedcentral.com/1741-7007/2/1
work_keys_str_mv AT lyonsweilermaureen thecolonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT polinglaural thecolonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT pisanidavide thecolonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT hedgess thecolonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT lyonsweilermaureen colonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT polinglaural colonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT pisanidavide colonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods
AT hedgess colonizationoflandbyanimalsmolecularphylogenyanddivergencetimesamongarthropods