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Underground evolution: new roots for the old tree of lumbricid earthworms.

ABSTRACT: Earthworms belonging to the family Lumbricidae are extremely abundant in terrestrial temperate regions. They affect soil properties and nutrient cycling, thus shaping plant community composition and aboveground food webs. Some lumbricids are also model organisms in ecology and toxicology. Despite the intense research efforts dedicated to lumbricids over the last 130years, the evolutionary relationships and taxonomic classification of these organisms are still subject to great debate. Resolution of their systematics is hampered by the structural simplicity of the earthworm body plan and the existence of cryptic species. We sampled 160 earthworm specimens belonging to 84 lumbricid species (28 genera) and 22 Lumbricoidea outgroups, sequenced two nuclear genes, four mitochondrial genes and seven mitochondrial tRNAs and examined 22 morphological characters. We then applied a combination of phylogenetic methods to generate the first robust genus-level phylogeny of the Lumbricidae. Our results show that the current Lumbricidae classification and the underlying hypotheses of character evolution must be revised. Our chronogram suggests that lumbricids emerged in the Lower Cretaceous in the holarctic region and that their diversification has been driven by tectonic processes (e.g. Laurasia split) and geographical isolation. Our chronogram and character reconstruction analysis reveal that spermathecae number does not follow a gradual pattern of reduction and that parthenogenesis arose from sexual relatives multiple times in the group; the same analysis also indicates that both epigeic and anecic earthworms evolved from endogeic ancestors. These findings emphasize the strong and multiple changes to which morphological and ecological characters are subjected, challenging the hypothesis of character stasis in Lumbricidae.

SUBMITTER: Dominguez J

PROVIDER: S-EPMC4766815 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Underground evolution: new roots for the old tree of lumbricid earthworms.

Domínguez Jorge J Aira Manuel M Breinholt Jesse W JW Stojanovic Mirjana M James Samuel W SW James Samuel W SW Pérez-Losada Marcos M

Molecular phylogenetics and evolution 20141115

Earthworms belonging to the family Lumbricidae are extremely abundant in terrestrial temperate regions. They affect soil properties and nutrient cycling, thus shaping plant community composition and aboveground food webs. Some lumbricids are also model organisms in ecology and toxicology. Despite the intense research efforts dedicated to lumbricids over the last 130years, the evolutionary relationships and taxonomic classification of these organisms are still subject to great debate. Resolution ...[more]

PMID: 25463017

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Project description:Aim:Lumbricid earthworms are invasive across northern North America, causing notable changes in forest ecosystems. During their range expansion they encountered harsher climatic conditions compared to their native ranges in evolutionary short time. This study investigated if (1) dispersal barriers, (2) climatic selection, or (3) anthropogenic activities, such as fishing bait disposal, structure the dispersal of free-living earthworm populations. Location:North America, forest habitats along former Wisconsinan glaciation line. Taxon:Lumbricus terrestris, L. rubellus. Methods:Lumbricus terrestris and L. rubellus co-occur in the same habitats but differ in ecology and use Conservation approach for goblin species were sampled in five transects ranging from the east to the west coast of northern North America, including major dispersal barriers, three different climate zones, and bait shops near sampling locations. Genetic diversity and structure were compared between the two species, and the presence of free-living bait shop genotypes was assessed using four markers (COI, 16S rDNA, 12S rDNA, H3). Results:Populations of both species were genetically diverse with some geographic structure, which was more pronounced in L. terrestris than in L. rubellus. Common haplotypes were present in all regions, but locally restricted haplotypes also occurred. Further, two distinct genetic clades of L. terrestris co-occurred only in the two most distant transects (Alberta and Minnesota). Genotypes identical to bait individuals were omnipresent in field populations of L. terrestris. Main conclusions:Genetic diversity was high in both species, and invasive populations represented a genetic subset of European earthworms. Geographic and climatic dispersal barriers affected the less mobile species, L. rubellus, resulting in differences in genetic structure between the two species. Our results indicate common long-distance dispersal vectors and specific vectors affecting only L. terrestris. The roles of climate and anthropogenic activities are discussed, providing additional explanations of dispersal and new insights into establishment of invasive earthworms.

Project description:Uniformly pigmented Eisenia andrei (Ea) and striped E. fetida (Ef) lumbricid earthworms are hermaphrodites capable of self-fertilization, cross-fertilization, and asymmetrical hybridization. The latter was detected by genotyping of F1 and F2 progeny of the controlled Ea+Ef pairs by species-specific sequences of maternal mitochondrial COI genes and maternal/paternal nuclear S28 rRNA genes. Among F1offspring there were self-fertilized Ea (aAA), Ef (fFF), and cross-fertilized fertile Ea-derived hybrids (aAF); the latter mated with Ea and gave new generation of Ea and hybrids, while mated with Ef gave Ea, Ef, Ea-derived hybrids and sterile Ef-derived hybrids (fFA). Coelomic fluid of Ea exhibits unique fluorescence spectra called here the M-fluorescence considered as a molecular biomarker of this species. Since similar fluorescence was detected also in some Ef (hypothetical hybrids?), the aim of present investigations was to identify the M-positive earthworms among families genotyped previously. It was assumed that factor/s responsible for metabolic pathways leading to production of undefined yet M-fluorophore might be encoded/controlled by alleles of hypothetical nuclear gene of Eisenia sp. segregating independently from species-specific S28 rRNA nuclear genes, where 'MM' or 'Mm' alleles determine M-positivity while 'mm' alleles determine M-negative phenotypes. Spectra of M-fluorescence were detected in all 10 Ea (aAAMM) and 19 Ea-derived hybrids (aAFMm), three of four Ef-derived hybrids (fFAMm) and one 'atypical' Ef (fFFMm) among 13 Ef earthworms. Among progeny of 'atypical' M-positive Ef (fFFMm) reappeared 'typical' M-negative Ef (fFFmm), confirming such hypothesis. Alternatively, the M-fluorescence might be dependent on unknown gene products of vertically-transmitted Ea-specific symbiotic bacteria sexually transferred to the Ef partner. Hypotheses of intrinsic and external origin of M-fluorescence might complement each other. The presence/absence of M-fluorophore does not correspond with body pigmentation patterns; Ef-characteristic banding appeared in posterior parts of hybrids body. In conclusion, Ea/Ef hybridization may serve for further studies on bi-directional gene flow.

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Underground evolution: new roots for the old tree of lumbricid earthworms.

Publications

Underground evolution: new roots for the old tree of lumbricid earthworms.

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