Julie Pisano , Fabien L. Condamine, Vladimir Lebedev, Anna Bannikova, Jean-Pierre Quéré, Gregory I. Shenbrot, Johan R. Michaux*, Marie Pagès*

Original Article submitted in Journal of Biogeography Muroidea (≈1,300-1,500 spp.) • Superfamily most closely related to the large and species-rich superfamily Muroidea • Most studies focus on Muroidea Dipodoidea(≈51 spp.)

DIPODIDAE (7 spp.) Euchoreutinae (1 sp.) Allactaginae (16 sp.) (9 spp.)

ZAPODIDAE (5 SPP .) Jumping mice Syn. Zapodinae

SMINTHIDAE (13 SPP .) Syn. Sicistinae Birch mice

(Holden & Musser, 2005; Lebedev et al ., 2012) Holarctic • Disjoint distribution patterns (e.g . Zapodidae) • Many species found in different remote arid habitats

SMINTHIDAE ZAPODIDAE Dipodoidea are particularly relevant for testing biogeographic scenarios • Subalpine meadows, • Riparian or wooded • Deserts, semi-deserts boreal and alpine areas andBUT marshlands and steppes forests; also in steppes within coniferous Lackand of asemi-deserts suitable phylogeneticforests framework is still impeding the inference of their biogeographic history ‹ Europe, Russia and ‹ North America and ‹ North Africa & Eurasia Central and Eastern China Asia ZHANG ET AL . (2012): • Middle Eocene: Diversification of modern Dipodoidea (i.e. crown; ≈42.7 Ma) • Warming period spanning from Late Oligocene through Early Miocene: Diversification of Sminthidae (≈16.8 Ma) • Global cooling following the mid-Miocene climatic optimum: Diversification of Zapodidae (≈13.2 Ma) and Dipodidae (≈27 Ma) WU ET AL . (2012): • Early Oligocene: Origin of modern Dipodoidea ( i.e. crown; ≈32.4 Ma)

Sinosminthus (Asia) FOSSIL RECORD Heosminthus (Asia) Simimys (North America) Elymys (North America) 1st occurrence of Dipodoidea in NA

Middle Late Early Late Early Middle Late Plio Pl Ho Eocene Eocene Oligocene Oligocene Miocene Miocene Miocene

48.6 Ma 37.2 Ma 33.9 Ma 28.4 Ma 23 Ma 16 Ma 11.6 Ma 5.3 Ma 2.6 Ma Present Based on the most complete species-level phylogeny (34/51 spp.), we reconstructed the temporal and biogeographic origins of the group with

1. Estimates of divergence times using a Bayesian relaxed molecular clock calibrated with fossils;

2. Inferences of biogeographic and evolutionary history using the dispersal-extinction- cladogenesis model • 34/51 species of Dipodoidea – 15/16 genera • Markers: Cyt b, IRBP, GHR, RAG1, BRCA1 (Single missing genus: Salpingotulus ) • Combined matrices: • Densely sampled matrix • Species-level matrix • 12 outgroup species (Muroidea, Sciuridae, Aplodontiidae) V PartitionFinder 1.1.1: – Selected to recovered specific Appropriate subset partitions nodes in the phylogeny allowing the use of fossils as calibration Appropriate substitution models of sequence evolution points to constrain nodes

1. PhyML 3.0 & MrBayes 3.2.2: on each gene independently V Congruence between markers 2. raxmlGUI 1.31 and MrBayes 3.2.2: V Analyses on combined datasets 3. ASSESSMENT OF THE TREE TOPOLOGY : (solved questions unresovled in Lebedev et al. (2012)) • Bayes factors Hypotheses (1 st part): The single species of Euchoreutinae with a. Allactaginae b. Dipodinae Hypothesis (2 nd part): c. Monophyly of • Bayesian relaxed clock • Clock model: Uncorrelated log-normal relaxed clock • Tree model: Yule / birth-death speciation process

• Soft bounds: - Log-normal distributions : - 2.5% quartile = Minimum age of the geological interval where the fossil was found - 97.5% quartile = 54 Ma, i.e. geological interval where Erlianomys, the oldest known fossil of Myodonta, was found

• Omission one by one each of the FC in turn to identify putative inconsistencies Douglasciurus Apodemus jeanteti / Progonomys Sicista primus jeffersoni A.dominans

FC1 FC2 FC3 FC4 In total: 10 dating analyses • 9 areas delineated using: o Palaeogeographical criteria o Revised distributions of extant dipodoid spp.

• Dispersal rates added according to o Palaeogeographical reconstructions of Earth 3 types of matrices of dispersal rates: • Time slice boundaries fit with - Nulle hypothesis M0: o Pulses of species diversification all dispersal rates = 1 o Past key environmental events - Alternative hypotheses: - M1: 0 to 1 5 Time-Slices: TS1: 0-5.3 Ma = IV ‰Pliocene - M2: 0 to 0.5 TS2: 5.3-16 Ma = late ‰ middle Miocene TS3: 16-23 Ma = Early Miocene TS4: 23-34 Ma = Oligocene TS5: 34-56 Ma = Eocene • BFs confirm: V Paraphyly of Allactaga species V Sister grouping between E. naso and the MOST COMPLETE MOLECULAR clade including Allactaginae and PHYLOGENY OF DIPODOIDEA TO Dipodinae DATE V Congruence with previous studies V Answered unresolved V The superfamilyquestions Dipodoideaof Lebedev et al . V The families(2012)Sminthidae, Zapodidae, Dipodidae V The subfamilies Cardiocraniinae, Dipodinae, Allactaginae

17 Rare genomic changes: • Indels of 3 or multiple of 3 nucleotides V Strengthened the obtained topology by confirming several monophylies A l l F C N o F C 1 N o F C 2 N o F C 3 N o F C 4 Node identification Yule BD Yule BD Yule BD Yule BD Yule BD 64.85 64.15 63.97 64.65 64.4 64.11 64.84 (60.7 (56.1 (56.6 64.8 (60.6 (60.5 64.46 (60.4 64.18 1 Crown of (60- 5- 8- 4- (60.6 5- 6- (60.6 6- (60.6- Rodentia 71,72 71.75 75.22 76.01 9- 71.53 70.79 9- 70.87 71.37 ) ) ) ) 71.8) ) ) 71.1) ) ) 37.9 37.91 37.5 37.39 37.88 37.79 37.68 37.48 37.52 FC1 – (35.4 (35.5 (32.8 (33.1 (35.4 (35.4 37.65 (35.4 (35.3 (35.4 • 3 All analysesDouglasciuru gave similar9- results1- whatever4- 1- 8- 6- (35.4- 8- 4- 2- s jeffersoni 42.09 41.94 43.97 44.43 41.97 41.81 41.38 41.56 41.43 41.72 ) ) ) ) ) ) ) ) ) ) the calibration strategy12.95 used during12.95 the12.81 12.78 12.94 12.91 12.8 FC2 – (12.1 (12.1 (11.2 (11.3 (12.1 (12.1 12.86 12.87 (12.0 12.82 9 cross-validationProgonomys procedure2- 3- 2- 1- 2- 1- (12.1- (12.1 7- (12.1- (Crown of 14.38 14.33 15.02 15.18 14.34 14.29 14.14 2- 14.15 14.25 Murinae) ) ) ) ) ) ) ) 14.2) ) ) • Fossil calibrationF C 3 – Constraints: ✓ Apodemus 7.37 7.37 7.29 7.27 7.36 7.35 7.32 7.33 7.29 7.29 12 jeanteti & (6.9- (6.9- (6.39- (6.44- (6.9- (6.89- (6.88- (6.9- (6.87- (6.89- Apodemus 8.18) 8.16) 8.55) 8.64) 8.16) 8.13) 8.05) 8.08) 8.05) 8.11) dominans 17.9 17.9 17.71 17.66 17.89 17.85 17.78 17.79 17.7 FC4 – Sicista 16.76 (16.7 (15.5 (15.6 (16.7 (16.7 (16.7 (16.7 (16.6 17.72 14 primus - 7- 1- 3- 5- 4- 2- 5- 9- (16.7 (Crown of 19.87 19.81 20.76 20.98 19.82 19.75 19.54 19.63 19.56 3- Sminthidae) ) ) ) ) ) ) ) ) ) 19.7) 58.51 58.51 57.72 58.47 58.34 58.11 58.16 57.85 Split (54.7 (54.8 57.89 (51.1 (54.7 (54.7 (54.6 (54.7 (54.5 57.91 6 Dipodoidea / 8- 2- (50.7- 1- 6- 3- 5- 7- 5- (54.6 Muroidea 64.97 64.74 67.88 68.59 64.79 64.55 63.88 64.16 63.95 8- ) ) ) ) ) ) ) ) ) 64.4) 41.18 41.18 40.74 40.62 41.05 40.9 40.93 40.76 (38.5 (38.5 (35.6 (35.9 41.15 (38.5 (38.4 (38.5 40.71 (38.4 13 Radiation of 5- 8- 8- 7- (38.5 2- 6- 4- (38.3 8- Dipodoidea 45.72 45.56 47.77 48.27 4- 45.43 44.95 45.15 9-45) 45.32 ) ) ) ) 45.6) ) ) ) ) 34.99 34.99 34.62 34.52 34.96 34.78 34.6 (32.7 (32,7 (30.3 (30.5 (32.7 34.89 34.75 (32.7 (32.6 34.63 21 Divergence 6- 8- 2- 6- 5- (32.7 (32.6 5- 2- (32.7- Zapodidae 38.85 38.72 40.59 41.02 38.75 3- 8- 38.37 38.24 38.51 ) ) ) ) ) 38.6) 38.2) ) ) ) 27.18 27.19 26.89 26.82 27.1 27 27.02 26.88 26.91 Divergence (25.4 (25.4 (16.4 (23.7 27.16 (25.4 (25.3 (25.4 (25.3 (25.4 26 Cardiocranii 5- 7- 4- 4- (25.4 3- 9- 4- 5- 1- nae 30.18 30.08 22.01 31.87 4- 29.99 29.68 29.81 29.71 29.92 ) ) ) ) 30.1) ) ) ) ) ) 22.52 22.28 22.21 22.5 22.45 22.36 22.38 22.26 22.29 Divergence 22.51 (21.0 (19.5 (19.6 (21.0 (21.0 (21.0 (21.0 (20.9 (21.0 28 Euchoreutina (21.0 9- 1- 7- 7- 6- 3- 8- 9- 4- e 8-25) 24.91 26.12 26.39 24.93 24.84 24.58 24.69 24.61 24.78 ) ) ) ) ) ) ) ) ) Late Paleocene (≈57.72 Ma): SPLIT BETWEEN DIPODOIDEA AND MUROIDEA

Middle Eocene (≈ 40.62 Ma): RADIATION OF MODERN DIPODOIDEA in Central Asia and Himalaya Tibetan plateau (Area ‘DG’)

V Congruent with the fossil record V Congruent with environmental changes: 40 Ma: India collided with Asia

Uplift episodes of Himalaya (Known to have induced vicariant events in many groups; e.g. warblers, glyptosternoid fishes) Early Oligocene (≈ 34.52 Ma): S PLIT BETWEEN ZAPODIDAE AND DIPODIDAE in Central Asia Global temperature Ó & Antarctic ice-sheet expanded rapidly

In Palearctic: development of open grasslands

Great worldwide mammalian faunal turn-over (i.e. the Mongolian remodelling in Asia): Eocene perissodactyl-dominant faunas replaced by /lagomorph-dominant faunas ≈20.24 Ma: in Central Asia during early Miocene

Diversification of Altitude of Zapodidae likely Aridification of Himalaya-Tibetan triggered by these Central Asia plateau Ì environmental changes Expansion of the range from East Russia to Present: Restricted to Himalaya-Tibetan Himalaya-Tibetan plateau plateau (Area ‘G’) (Area ‘CDG’) Between early (≈20.24 Between ≈14 to 3.5 Ma: Suggesting a middle Ma) and middle BLB covered by a Miocene colonisation of Miocene (≈13.01 Ma): continuous boreal North America Colonisation of North coniferous forest belt America

✓✓✓ Congruent with the fossil record : Megasminthus, middle Miocene, North America ‰ Oldest known North American fossil of Zapodidae ≈16.11 Ma: in Central Asia at the early-middle Miocene boundary Mid-Miocene climatic Year-round aridity Most intense optimum: and formation of orogenic phase of Period of considerable deserts and Himalaya warming grasslands

Likely to have favour the diversification of Dipodinae Between 5.33 and 5.96 Late Miocene (≈5.97 Ma, the Messinian Promoted faunal Ma): Diversification of Salinity Crisis: exchanges between Africa spp. in Central Dessication of the and adjacent regions Asia (and colonisation Mediterranean sea of Africa)

✓✓✓ Congruent with the fossil record : e.g. colonisation of Africa by Mus around 6.6 – 4 Ma

J. blanfordi

J. jaculus J. orientalis Late Miocene (≈8.66 Ma): Coincide with the replacement of Diversification of the MRCA of woodland-adapted by more- and Dipus in Central Asia open habitat representatives

Late Miocene: Global cooling promoted Favoured the diversification of these grasslands & arid habitats in Europe and species adapted to open and arid habitats. Central Asia Stylodipus andrewsi

S. telum S. sungorus V Paraphyly of Allactaga V Phylogenetic position of Euchoreutinae • Inference of a V Especially thanks to the exhaustive sampling of Zapodidae and Dipodinae ‰ Detailed biogeographic scenarios of these two groups

V Geological and climatic upheavals of Central Asia V AND ESPECIALLY the uplift of the Himalaya-Tibetan plateau ‰ Induced aridification process ‰ Promoted the development of new habitats ( e.g. deserts and grasslands) Thanks for your attention !