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Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be resolved? N.I. Abramson Zooological Institute, Russian Academy of Sciences

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Page 1: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Supraspecies phylogenetic relationships in the subfamily

Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be resolved?

N.I. AbramsonZooological Institute, Russian Academy of Sciences

Page 2: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Overview of the talk• What are arvicolids and why they present an

excellent model to test evolutionary and phylogenetic hypotheses and approaches to phylogeny recovery

• Brief historical background• Material and methods• Unexpected results of molecular research in

phylogeny reconstruction • Mitochondrial versus nuclear genes Could hard

polytomies be resolved?• Molecular data in paleontological context

Page 3: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Subfamily Arvicolinae(voles and lemmings)

Page 4: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Arvicolinae as a modelone of the most young and species rich

groups of Muroidea (over 100 known species).

widely distributed in all landscape types in the temperate and arctic zones of the Northern Hemisphere

unprecedented paleontological record, rapid evolution rate, and continuous diversification

morphological, cytogenetic, biochemical and molecular data sets available

Page 5: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

BRIEF HISTORICAL BACKGROUND

Page 6: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

BRIEF HISTORICAL BACKGROUND

Page 7: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

BRIEF HISTORICAL BACKGROUND

Journal of Mammalian Evolution, Vol. 6, No. 3, 1999MtDNA Evidence for Repeated Pulses of Speciation

Within Arvicoline and Murid Rodents Chris J. Conroy and Joseph A. Cook1

Mitochondrial phylogeny of Arvicolinae usingcomprehensive taxonomic sampling yields new insightsELENA V. BUZAN, BORIS KRYSTUFEK, BERND HÄNFLING2 andWILLIAM F. HUTCHINSON

The evolutionary radiation of Arvicolinae rodents (voles andlemmings): relative contribution of nuclear and mitochondrial DNAPhylogenies

Thomas Galewski et al.

Page 8: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Objective

To separate the phyletic lineages that diverged during the basal (first) radiation wave from the groups arising at the later steps of the evolution of Arvicolinae

Page 9: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Material and methods

•21 vole species belonging to 14 (out of 28) genera of eight (out of ten) tribes•Vole tribes Ellobiusini and Lagurini, which were not examined before, and whose phylogenetic positions are questionable•Akodon (Sigmodontinae), Peromyscus (Neotominae), andCricetulus (Cricetinae), used as an outgroup

The sample includes:

Molecular markers: •GHR , 10 exon, 921 bp;• LCAT, 612 bp: exons 2-5; introns, 330 bp

Phylogenetic analysis:•MP for both the concatenated matrix and the two separate genes•ML for exons for both genes•Bayesian analysis•Relaxed molecular clock, using the Bayesian algorithm of the Multidivtime package( BRCA1, RAG1,IRBP,and cmyc)

Page 10: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Results

III II wave

II wave

III wave

Page 11: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Results

Chronogram of radiation in the subfamily Arvicolinae. The divergence time corresponds to the mean a posteriori estimate of the age. Gray bars show the confidence intervals of the nodes.

My

od

ini

Lagurini

Ellobiusini

Arv

ico

lini

Page 12: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Mitochondrial versus nuclear genes

Cyt b

Buzan et al., 2008

Page 13: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Possible evolutionary scenario

Page 14: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Morphological and paleontological evidence

Page 15: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Molecular data in paleontological context

The first radiation wave Our results suggest that basal subfamily radiation occurred in the late Miocene, which is in accordance with paleontological data indicating that the most primitive undoubted members of the group appeared about 7.0 million years ago in Pon tic deposits of eastern Europe

The second radiation wave. This step corresponds to the divergence of the ancestors of modern Myodini. The divergence time corresponds to the Late Miocene–Early Pliocene according to molecular data. Our findings indicate that Myodini diverged from the common branch of Arvicolinae after the first (basal) radiation wave but before Lagurini/Ellobiusini/Arvicolini radiation. The distribution of modern species and paleontological findings indicate that the group originates from East Asia and that level and highland forests were its initial habitats.

The third radiation wave of Arvicolinae includes the divergence of Lagurini/Ellobiusini/Arvicolini. The divergence dates back to the Early Pliocene according to our results. This means that Palearctic voles of a pro-Mimomys organization level might be a common ancestor of the group. Lagurini and Arvicolini developed along the main evolutionarily pathway of the subfamily, gradually adapting to eating vegetative parts of grasses and colonizing predominantly meadow (Arvicolini) and steppe (Lagurini) landscapes. Ellobiusini provide a remarkable example of rapid evolutionary changes associated with the adaptation to subterranean life; in particular, they preserved the primitive molar structure, while their cranium and limbs were changed. Rapid adaptive evolution explains why it is difficult to infer the phylogennetic position of Ellobiusini from classical morphological data

Page 16: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be

Aknowledgements This work is coauthored by Vladimir

Lebedev, Anna Bannikova and Alexei Tesakov

A.S. Smorktcheva provide invaluable material on yellow steppe vole

A.Kostygov, E.Rodchenkova, T.Petrova & S.Bodrov assist in the laboratory

Financial support was provided by RFFI grant 09-04-01330 and Programs of Fundamental Research RAS: “Biosphere Origin and Evolution” and “Biodiversity”

Page 17: Supraspecies phylogenetic relationships in the subfamily Arvicolinae (voles and lemmings): nuclear versus mitochondrial genes. Could hard polytomies be