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Ancient phylogenetic divergence of the enigmatic African rodent Zenkerella and the origin of anomalurid gliding.

ABSTRACT: The "scaly-tailed squirrels" of the rodent family Anomaluridae have a long evolutionary history in Africa, and are now represented by two gliding genera (Anomalurus and Idiurus) and a rare and obscure genus (Zenkerella) that has never been observed alive by mammalogists. Zenkerella shows no anatomical adaptations for gliding, but has traditionally been grouped with the glider Idiurus on the basis of craniodental similarities, implying that either the Zenkerella lineage lost its gliding adaptations, or that Anomalurus and Idiurus evolved theirs independently. Here we present the first nuclear and mitochondrial DNA sequences of Zenkerella, based on recently recovered whole-body specimens from Bioko Island (Equatorial Guinea), which show unambiguously that Zenkerella is the sister taxon of Anomalurus and Idiurus. These data indicate that gliding likely evolved only once within Anomaluridae, and that there were no subsequent evolutionary reversals. We combine this new molecular evidence with morphological data from living and extinct anomaluromorph rodents and estimate that the lineage leading to Zenkerella has been evolving independently in Africa since the early Eocene, approximately 49 million years ago. Recently discovered fossils further attest to the antiquity of the lineage leading to Zenkerella, which can now be recognized as a classic example of a "living fossil," about which we know remarkably little. The osteological markers of gliding are estimated to have evolved along the stem lineage of the Anomalurus-Idiurus clade by the early Oligocene, potentially indicating that this adaptation evolved in response to climatic perturbations at the Eocene-Oligocene boundary (?34 million years ago).

SUBMITTER: Heritage S

PROVIDER: S-EPMC4991859 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Ancient phylogenetic divergence of the enigmatic African rodent Zenkerella and the origin of anomalurid gliding.

Heritage Steven S Fernández David D Sallam Hesham M HM Cronin Drew T DT Esara Echube José Manuel JM Seiffert Erik R ER

PeerJ 20160816

The "scaly-tailed squirrels" of the rodent family Anomaluridae have a long evolutionary history in Africa, and are now represented by two gliding genera (Anomalurus and Idiurus) and a rare and obscure genus (Zenkerella) that has never been observed alive by mammalogists. Zenkerella shows no anatomical adaptations for gliding, but has traditionally been grouped with the glider Idiurus on the basis of craniodental similarities, implying that either the Zenkerella lineage lost its gliding adaptatio ...[more]

PMID: 27602286

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Project description:Numerous ancient whole-genome duplications (WGD) have occurred during eukaryote evolution. In vertebrates, duplicated developmental genes and their functional divergence have had important consequences for morphological evolution. Although two vertebrate WGD events (1R/2R) occurred over 525 Ma, we have focused on the more recent 3R or TGD (teleost genome duplication) event which occurred approximately 350 Ma in a common ancestor of over 26,000 species of teleost fishes. Through a combination of whole genome and bacterial artificial chromosome clone sequencing we characterized all Hox gene clusters of Pantodon buchholzi, a member of the early branching teleost subdivision Osteoglossomorpha. We find 45 Hox genes organized in only five clusters indicating that Pantodon has suffered more Hox cluster loss than other known species. Despite strong evidence for homology of the five Pantodon clusters to the four canonical pre-TGD vertebrate clusters (one HoxA, two HoxB, one HoxC, and one HoxD), we were unable to confidently resolve 1:1 orthology relationships between four of the Pantodon clusters and the eight post-TGD clusters of other teleosts. Phylogenetic analysis revealed that many Pantodon genes segregate outside the conventional "a" and "b" post-TGD orthology groups, that extensive topological incongruence exists between genes physically linked on a single cluster, and that signal divergence causes ambivalence in assigning 1:1 orthology in concatenated Hox cluster analyses. Out of several possible explanations for this phenomenon we favor a model which keeps with the prevailing view of a single TGD prior to teleost radiation, but which also considers the timing of diploidization after duplication, relative to speciation events. We suggest that although the duplicated hoxa clusters diploidized prior to divergence of osteoglossomorphs, the duplicated hoxb, hoxc, and hoxd clusters concluded diploidization independently in osteoglossomorphs and other teleosts. We use the term "tetralogy" to describe the homology relationship which exists between duplicated sequences which originate through a shared WGD, but which diploidize into distinct paralogs from a common allelic pool independently in two lineages following speciation.

Dataset Information

Ancient phylogenetic divergence of the enigmatic African rodent Zenkerella and the origin of anomalurid gliding.

Publications

Ancient phylogenetic divergence of the enigmatic African rodent Zenkerella and the origin of anomalurid gliding.

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