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Earthworm genomes, genes and proteins: the (re)discovery of Darwin's worms.

Stürzenbaum SR, Andre J, Kille P, Morgan AJ - Proc. Biol. Sci. (2009)

Bottom Line: Mistaken though he was in advocating systemic 'gemmules' as agents of inheritance, Darwin was perceptive in seeking to underpin his core vision with concrete factors that both determine the nature of a trait in one generation and convey it to subsequent generations.We predict that the current understanding will deepen with the announcement of a draft earthworm genome in Darwin's bicentenary year, 2009.Subsequently, the earthworm may be elevated from the status of a soil sentinel to that elusive entity, an ecologically relevant genetic model organism.

View Article: PubMed Central - PubMed

Affiliation: School of Biomedical & Health Sciences, King's College London, London SE1 9NH, UK. stephen.sturzenbaum@kcl.ac.uk

ABSTRACT
Small incremental biological change, winnowed by natural selection over geological time scales to produce large consequences, was Darwin's singular insight that revolutionized the life sciences. His publications after 1859, including the 'earthworm book', were all written to amplify and support the evolutionary theory presented in the Origin. Darwin was unable to provide a physical basis for the inheritance of favoured traits because of the absence of genetic knowledge that much later led to the 'modern synthesis'. Mistaken though he was in advocating systemic 'gemmules' as agents of inheritance, Darwin was perceptive in seeking to underpin his core vision with concrete factors that both determine the nature of a trait in one generation and convey it to subsequent generations. This brief review evaluates the molecular genetic literature on earthworms published during the last decade, and casts light on the specific aspects of earthworm evolutionary biology that more or less engaged Darwin: (i) biogeography, (ii) species diversity, (iii) local adaptations and (iv) sensitivity. We predict that the current understanding will deepen with the announcement of a draft earthworm genome in Darwin's bicentenary year, 2009. Subsequently, the earthworm may be elevated from the status of a soil sentinel to that elusive entity, an ecologically relevant genetic model organism.

Show MeSH

Related in: MedlinePlus

Phylogenetic analysis of species diversity within a range of Annelida. Representative COI sequences were selected from GenBank to illustrate maximal diversity with four annelid species: T. tubifex (EF179544.1, EF179543.1 and AF534866.1); Metaphire glareosa (AY960803.1, AY962167.1, AY962168.1, AY962169.1, AY962178.1 and AY962179.1); Dendrobaena octaedra (EU035478.1, EU035481.1, EU035484.1, EU035487.1, EU035488.1, EU035492.1 and DQ092895.1); and Diplocardia caroliniana (EF156651.1, EF156658.1, EF156659.1 and EF156661.1). The tree was constructed using the distance-based neighbour-joining algorithm, based upon p distance.
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fig3: Phylogenetic analysis of species diversity within a range of Annelida. Representative COI sequences were selected from GenBank to illustrate maximal diversity with four annelid species: T. tubifex (EF179544.1, EF179543.1 and AF534866.1); Metaphire glareosa (AY960803.1, AY962167.1, AY962168.1, AY962169.1, AY962178.1 and AY962179.1); Dendrobaena octaedra (EU035478.1, EU035481.1, EU035484.1, EU035487.1, EU035488.1, EU035492.1 and DQ092895.1); and Diplocardia caroliniana (EF156651.1, EF156658.1, EF156659.1 and EF156661.1). The tree was constructed using the distance-based neighbour-joining algorithm, based upon p distance.

Mentions: Classical taxonomy is based on the examination and comparisons of morphological structures. The body plan of oligochaete worms, largely devoid of prominent external appendages other than the secondary sexual structures decorating the evolutionary innovation of metameric segmentation, limits the scope of morphological taxonomy. Application of enzyme electrophoresis in the 1980s and 1990s increased the information in many topics of earthworm research, such as in taxonomy (Øien & Stenersen 1984), allozyme diversity in amphigonic and polyploid strains (e.g. Cobolli Sbordoni et al. 1987), diversity and regional adaption of clone pools in parthenogenetic species (Terhivuo & Saura 1990, 1993) and temporal variability of clones in parthenogens (Jaenike & Selander 1985). The advent of molecular genotyping tools for earthworms (Chang et al. in press) has begun to reveal hitherto unsuspected degrees of ‘intraspecific’ genetic diversity that represent potential cases of cryptic speciation, defined as morphologically similar but genetically distinct sibling species (Rocha-Olivares et al. 2004). An analysis of mitochondrial cytochrome oxidase subunit I (COI) sequences of the small number of contrasting oligochaete ‘species’ deposited in genetic databases (National Center for Biotechnology Information, GenBank, DNA Data Bank of Japan) demonstrates multiple genetically differentiated lineages within each species cluster (figure 3). It is possible that the Oligochaeta are particularly prone to sympatric speciation. For example, Sturmbauer et al. (1999) identified that the mitochondrial 16S rDNA of the freshwater worm Tubifex tubifex could be differentiated into five major lineages (separated by genetic distances of up to 13%), providing strong evidence for the presence of cryptic speciation. Likewise, COI genotyping on the representatives of the British earthworm fauna indicate that at least four of the eight species contain two to three distinct lineages that may diverge by over 12 per cent (King et al. 2008). Another notion supporting the fact that earthworms are genetically heterogeneous is that both the amphigonic and polyploid strains can exist within a species as shown by surveys on chromosomal status of populations (Casellato 1987). The origin of this diversity is not known, but the convergent postglacial invasion of multiple genotypes from geographically isolated refugia of southern Europe has been offered as a plausible explanation (King et al. 2008). Whatever factors gave rise to the genetic diversity of earthworms, the ecological and evolutionary implications of its existence are wide-ranging. In short, Darwin was correct in saying that earthworms are closely similar to each other, but he would have been stunned at how modern molecular techniques are able to distinguish between the many different species (belonging to a large number of different genera) and provide a compelling case for including leeches and branchiobdellids within the Oligochaeta (Jamieson et al. 2002).


Earthworm genomes, genes and proteins: the (re)discovery of Darwin's worms.

Stürzenbaum SR, Andre J, Kille P, Morgan AJ - Proc. Biol. Sci. (2009)

Phylogenetic analysis of species diversity within a range of Annelida. Representative COI sequences were selected from GenBank to illustrate maximal diversity with four annelid species: T. tubifex (EF179544.1, EF179543.1 and AF534866.1); Metaphire glareosa (AY960803.1, AY962167.1, AY962168.1, AY962169.1, AY962178.1 and AY962179.1); Dendrobaena octaedra (EU035478.1, EU035481.1, EU035484.1, EU035487.1, EU035488.1, EU035492.1 and DQ092895.1); and Diplocardia caroliniana (EF156651.1, EF156658.1, EF156659.1 and EF156661.1). The tree was constructed using the distance-based neighbour-joining algorithm, based upon p distance.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2664377&req=5

fig3: Phylogenetic analysis of species diversity within a range of Annelida. Representative COI sequences were selected from GenBank to illustrate maximal diversity with four annelid species: T. tubifex (EF179544.1, EF179543.1 and AF534866.1); Metaphire glareosa (AY960803.1, AY962167.1, AY962168.1, AY962169.1, AY962178.1 and AY962179.1); Dendrobaena octaedra (EU035478.1, EU035481.1, EU035484.1, EU035487.1, EU035488.1, EU035492.1 and DQ092895.1); and Diplocardia caroliniana (EF156651.1, EF156658.1, EF156659.1 and EF156661.1). The tree was constructed using the distance-based neighbour-joining algorithm, based upon p distance.
Mentions: Classical taxonomy is based on the examination and comparisons of morphological structures. The body plan of oligochaete worms, largely devoid of prominent external appendages other than the secondary sexual structures decorating the evolutionary innovation of metameric segmentation, limits the scope of morphological taxonomy. Application of enzyme electrophoresis in the 1980s and 1990s increased the information in many topics of earthworm research, such as in taxonomy (Øien & Stenersen 1984), allozyme diversity in amphigonic and polyploid strains (e.g. Cobolli Sbordoni et al. 1987), diversity and regional adaption of clone pools in parthenogenetic species (Terhivuo & Saura 1990, 1993) and temporal variability of clones in parthenogens (Jaenike & Selander 1985). The advent of molecular genotyping tools for earthworms (Chang et al. in press) has begun to reveal hitherto unsuspected degrees of ‘intraspecific’ genetic diversity that represent potential cases of cryptic speciation, defined as morphologically similar but genetically distinct sibling species (Rocha-Olivares et al. 2004). An analysis of mitochondrial cytochrome oxidase subunit I (COI) sequences of the small number of contrasting oligochaete ‘species’ deposited in genetic databases (National Center for Biotechnology Information, GenBank, DNA Data Bank of Japan) demonstrates multiple genetically differentiated lineages within each species cluster (figure 3). It is possible that the Oligochaeta are particularly prone to sympatric speciation. For example, Sturmbauer et al. (1999) identified that the mitochondrial 16S rDNA of the freshwater worm Tubifex tubifex could be differentiated into five major lineages (separated by genetic distances of up to 13%), providing strong evidence for the presence of cryptic speciation. Likewise, COI genotyping on the representatives of the British earthworm fauna indicate that at least four of the eight species contain two to three distinct lineages that may diverge by over 12 per cent (King et al. 2008). Another notion supporting the fact that earthworms are genetically heterogeneous is that both the amphigonic and polyploid strains can exist within a species as shown by surveys on chromosomal status of populations (Casellato 1987). The origin of this diversity is not known, but the convergent postglacial invasion of multiple genotypes from geographically isolated refugia of southern Europe has been offered as a plausible explanation (King et al. 2008). Whatever factors gave rise to the genetic diversity of earthworms, the ecological and evolutionary implications of its existence are wide-ranging. In short, Darwin was correct in saying that earthworms are closely similar to each other, but he would have been stunned at how modern molecular techniques are able to distinguish between the many different species (belonging to a large number of different genera) and provide a compelling case for including leeches and branchiobdellids within the Oligochaeta (Jamieson et al. 2002).

Bottom Line: Mistaken though he was in advocating systemic 'gemmules' as agents of inheritance, Darwin was perceptive in seeking to underpin his core vision with concrete factors that both determine the nature of a trait in one generation and convey it to subsequent generations.We predict that the current understanding will deepen with the announcement of a draft earthworm genome in Darwin's bicentenary year, 2009.Subsequently, the earthworm may be elevated from the status of a soil sentinel to that elusive entity, an ecologically relevant genetic model organism.

View Article: PubMed Central - PubMed

Affiliation: School of Biomedical & Health Sciences, King's College London, London SE1 9NH, UK. stephen.sturzenbaum@kcl.ac.uk

ABSTRACT
Small incremental biological change, winnowed by natural selection over geological time scales to produce large consequences, was Darwin's singular insight that revolutionized the life sciences. His publications after 1859, including the 'earthworm book', were all written to amplify and support the evolutionary theory presented in the Origin. Darwin was unable to provide a physical basis for the inheritance of favoured traits because of the absence of genetic knowledge that much later led to the 'modern synthesis'. Mistaken though he was in advocating systemic 'gemmules' as agents of inheritance, Darwin was perceptive in seeking to underpin his core vision with concrete factors that both determine the nature of a trait in one generation and convey it to subsequent generations. This brief review evaluates the molecular genetic literature on earthworms published during the last decade, and casts light on the specific aspects of earthworm evolutionary biology that more or less engaged Darwin: (i) biogeography, (ii) species diversity, (iii) local adaptations and (iv) sensitivity. We predict that the current understanding will deepen with the announcement of a draft earthworm genome in Darwin's bicentenary year, 2009. Subsequently, the earthworm may be elevated from the status of a soil sentinel to that elusive entity, an ecologically relevant genetic model organism.

Show MeSH
Related in: MedlinePlus