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Phylogenetic position of the Altaic fish genus Oreoleuciscus in Leuciscinae based on mitogenome sequences Junichi Imoto 1, Kenji Saitoh 2, Jun Adachi 3,

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Presentation on theme: "Phylogenetic position of the Altaic fish genus Oreoleuciscus in Leuciscinae based on mitogenome sequences Junichi Imoto 1, Kenji Saitoh 2, Jun Adachi 3,"— Presentation transcript:

1 Phylogenetic position of the Altaic fish genus Oreoleuciscus in Leuciscinae based on mitogenome sequences Junichi Imoto 1, Kenji Saitoh 2, Jun Adachi 3, Takeshi Sasaki 4, Yuri P. Kartavtsev 5, Satoru N. Chiba 1, Ryo O. Gotoh 1, Masaki Miya 5, Mutsumi Nishida 6 and Naoto Hanzawa 1 1 Grad Sch Sci Eng, Yamagata Univ, 2 Nat Res Inst Fish Sci, 3 Inst Stat Math, 4 Inst Marine Biol, 5 Nat Hist Mus Inst Chiba, 6 Ocean Res Inst, Univ Tokyo Phylogenetic position of the Altaic fish genus Oreoleuciscus in Leuciscinae based on mitogenome sequences

2 38 species 204 genera (FishBase) leuciscin : Eurasian plus North American Notemigonus cryleucas 48 species 319 genera (FishBase) phoxinin: North American and Far Eastern species Phylogeny based on morphology (Cavender and Coburn, 1992) Leuciscinae Widely distributed in Northern Hemisphere Morphologically similar (even among different genera) Important to consider the evolutional history of Leuciscinae Central Asia and Far East

3 The genus Oreoleuciscus (Warpachowskii, 1889) Endemic to inland lakes in western Mongolia and Tuva, the upper Ob River system within the Altai Mountain region of Siberia (Berg, 1962) Planktonic algae, insects, invertebrates and fishes Oreoleuciscus potanini Feeding habitat Distribution

4 Far Eastern European North American ML tree based on mt genome Phylogenetic position of Oreoleuciscus Oreoleucuscus potanini Closely related to Pseudaspius and Tribolodon ? (Howes, 1984, 1991) Tribolodon sachalinensis Tribolodon hakonensis Pseudaspius leptocephalus ? Tribolodon nakamurai

5 Far Eastern European North American ML tree based on mt genome Phylogenetic position of Oreoleuciscus Oreoleucuscus potanini Closely related to Phoxinus ? (Travers, 1989; Bogutskaya, 1990) Phoxinus phoxinus Phoxinus lagowskii Phoxinus perenurus ?

6 No molecular phylogenetic analyses for Oreoleuciscus species High degree of morphological variability that obscures differences among species Taxonomy of the genus Oreoleuciscus is controversial Paucity of specimens from key geographical areas Determine complete mitochondrial (mt) genome sequences of Oreoleuciscus Conduct phylogenetic analysis based on mt genome sequences Clarify the phylogenetic position of genus Oreoleuciscus and evolutional history of the Leuciscinae The purpose of this study

7 Mt genome analyses Long DNA sequences (Inoue et al., 2001a; Miya et al., 2003; Saitoh et al., 2006) Correct estimation of phylogeny at various taxonomic levels with strong statistical support 17 genera 31 species Outgroup 9 species (Cypridae 8, Cobitidae 1) MLRAxML v7.0.4 (Stamatakis, 2006) BayesMrBayes v3.1.2 (Ronquist & Huelsenbeck 2003) Determined mt genome sequences Genomic structure Common with vertebrates Exclude ND6, control region and gaps (14,826 bp) Mt genome of Oreoleuciscus potanini

8 Far Eastern European North American ML bootstrap / Bayesian posterior probabilities

9 Far Eastern European North American ML bootstrap / Bayesian posterior probabilities

10 Far Eastern European North American ML bootstrap / Bayesian posterior probabilities Oreoleuciscus potanini Phoxinus lagowskii Tribolodon nakamurai

11 L 100, U 120 L 112, U 145 L 85, U 95 U 363 Molecular Dating (Mya) Upper constraint : U Lower constraint : L Parametric Bayesian approach Multidistribute (Thorn & Kishino 2002) Cichlids

12 L 100, U 120 L 112, U 145 L 85, U 95 African South American Madagascar Indo/Sri Lanka Madagascar Cichlid Molecular Dating (Mya) Upper constraint : U Lower constraint : L (Azuma et al., 2008)

13 Leuciscinae / other subfamily Cyprinidae / Cobitidae Otocephala / Euteleostei MesozoicCenozoicPaleozoic Carboniferous TriassicJurassicCretaceous Tertiary Permian

14 phoxinin / leuciscin 84.8 Far Eastern phoxinin / P. phoxinus 78.5 Orieoleuciscus / Far Eastern Phoxinus 35.5 Tribolodon / Orieoleuciscus + Far Eastern Phoxinus 48.6 MesozoicCenozoic Cretaceous Pa.EoceneOli.MiocenePlio

15 The genus Oreoleuciscus is included in phoxinin (Cavender & Coburn 1992) rather than Tribodolon and Pseudaspius Oreoleuciscus formed a monophyletic clade with the Far Eastern phoxinins Conclusion Oreoleuciscus is closely related to the Far Eastern Phoxinus Tribolodon, Pseudaspius and the Far Eastern Phoxinus Tribolodon + Pseudaspius and Oreoleuciscus + Phoxinus were divided 49 Mya Oreoleuciscus and Phoxinus were divided 34 Mya

16 Thank you for your attention !!

17

18 The genus Oreoleuciscus (Warpachowskii, 1889) Endemic to inland lakes in western Mongolia and Tuva, the upper Ob River system within the Altai Mountain region of Siberia (Berg, 1962) The range of Oreoleuciscus demarcates a highly ranked biogeographical unit that has a very depauperate and distinct ichthyofauna. In the review of Eurasian cyprinid biogeography, Banarescu & Coad (1991) determined that the rank of this unit is equal to that of regions such as the entire Euro-Mediterranean or Central Asian regions. Oreoleucuscus potanini

19 Far Eastern European North American 1.81 ~ 4.37 Mya Tribolodon speciation The glacial period ~ Mya Radiation of Leuciscinae Rapid global cooling of Middle Miocene The sea level dropped The land area expansion, freshwater and brackish water area increased Environment habitable for Leuciscinae extended Enlarge their distribution and occurred speciation

20 Far Eastern European North American ML tree based on mt genome

21 Ancestral area of the Far Eastern Leuciscinae

22 The genus Oreoleuciscus (Warpachowskii, 1889) Endemic to inland lakes in western Mongolia and Tuva, the upper Ob River system within the Altai Mountain region of Siberia (Berg, 1962) The range of Oreoleuciscus demarcates a highly ranked biogeographical unit that has a very depauperate and distinct ichthyofauna. In the review of Eurasian cyprinid biogeography, Banarescu & Coad (1991) determined that the rank of this unit is equal to that of regions such as the entire Euro-Mediterranean or Central Asian regions.

23 中世代 第三紀 第四紀古世代 白亜紀ジュラ紀三畳紀ペルム紀 (Mya) ウグイ亜科と他の亜科 コイ科とドジョウ科 ニシン・骨鰾下区と 正新骨下区 化石記録よりも古い年代 コイ科魚類 最古の化石 Parabarbus sp. ca. 50 Mya

24 24 ユーラシアおよび北米に広く分布するコイ科ウグイ亜科魚類は、主にユーラシアに分布する leuciscin と、主に北米および極東 に分布する phoxinin の 2 つの系統に大別される。 ウグイ亜科魚類の系統地理学的考察を行うためには、 2 つの系統群が接する極東から中央ユーラシアにかけて分布するタクソン のサンプリングが必要と考えられ、発表者らは、アルタイ共和国においてサンプリングを行い、ウグイ亜科 Oreoleuciscus 属魚 類を採集した ( 千葉ら, 2008) 。 Oreoleuciscus 属魚類は中央アジア・オビ川上流のアルタイ山地、モンゴルの一部にのみ分布する非常に希少な魚類である。 Howes (1984, 1991) は、形態的特徴から Oreoleuciscus 属は Pseudaspius 属やウグイ属と共に aspinin の系統に含まれるとし た。 Howes (1984, 1991) ウグイ亜科を Abramin 、 Aspinin 、 Phoninin の 3 つに分類 しかし、 Oreoleuciscus 属は形態的に Phoxinus 属に近いという考えもあり (Travers, 1989; Bogutskaya, 1990) 、未だに系統 的位置は不明だが、これまで分子系統解析は全く行われていない。 そこで、我々は Oreoleuciscus potanini のミトコンドリアゲノムを決定して、他のウグイ亜科魚類とともに分子系統解析を行 った。 その結果、 Oreoleuciscus 属は極東産 Phoxinus 属の姉妹群となり、これらにウグイ属を加えたクレードは単系統群を形成し、 他の欧米産ウグイ亜科魚類各クレードからは大きく離れていた。 本研究の結果は、ウグイ亜科魚類の進化史を考察する上で重要なデータと考えられる。

25 中世代 第三紀 第四紀古世代 白亜紀ジュラ紀三畳紀ペルム紀 (Mya) コイ科とドジョウ科 ニシン・骨鰾下区と 正新骨下区 化石記録よりも古い年代 コイ科魚類 最古の化石 Parabarbus sp. ca. 50 Mya 分子を用いた年代推定とほぼ一致 (Inoue et al., 2005; Yamanoue et al., 2006; Azuma et al., 2008)

26 中世代新生代 白亜紀ジュラ紀 暁新生 始新生 漸新世 中新生 鮮新世 1000 (Mya) phoxinin / leuciscin 74.7 Far Eastern phoxinin / P. phoxinus 61.7 Orieoleuciscus / Far Eastern Phoxinus 21.2 Tribolodon / Orieoleuciscus + Far Eastern Phoxinus 39.2 イタリア モンゴル 最上川 請戸川

27 中世代新生代 白亜紀ジュラ紀 暁新生 始新生 漸新世 中新生 鮮新世 1000 (Mya) 7.5 ~ 21.2 Mya Tribolodon 属各種が種 分化 寒冷化・乾燥化 陸地が拡大、淡水域や汽水域などが増える ウグイ亜科魚類が生息できる環境が広がる新しい生息場所に分布を広げながら種分化 海水面の低下 イタリア モンゴル 最上川 請戸川

28 Closely related to Pseudaspius and Tribolodon ? (Howes, 1984, 1991) Closely related to Phoxinus ? (Travers, 1989; Bogutskaya, 1990) Tribolodon sachalinensis Tribolodon hakonensis Tribolodon brandtii Tribolodon nakamurai Phoxinus phoxinus Phoxinus lagowskii Phoxinus perenurus Pseudaspius leptocephalus High degree of morphological variability that obscures differences among species Taxonomy of the genus Oreoleuciscus is controversial Paucity of specimens from key geographical areas Phylogenetic position of Oreoleuciscus

29 Oreoleuciscus is thought to be allied to the Eurasian cyprinid genera Pseudaspius and Tribolodon which are within the aspinin lineage of the subfamily Leuciscinae (Howes, 1984, 1991). On the other hand, there is also the idea that Oreoleuciscus is rather closely related to the phoxinin lineage (Travers, 1989; Bogutskaya, 1990). Thus, taxonomy of the genus Oreoleuciscus is controversial, in part because of the paucity of specimens from key geographical areas, and in part because there is high degree of morphological variability that obscures differences among species.

30 Determine complete mitochondrial (mt) genome sequences of Leuciscinae species Purpose Conduct phylogenetic analysis based on mt genome sequences Clarify the phylogenetic position of genus Oreoleuciscus and evolutional history of the Leuciscinae

31 Determine complete mitochondrial (mt) genome sequences of Leuciscinae species Purpose Conduct phylogenetic analysis based on mt genome sequences Clarify the phylogenetic position of genus Oreoleuciscus and evolutional history of the Leuciscinae

32 38 species 204 genera (FishBase) leuciscin : Eurasian plus North American Notemigonus cryleucas 48 species 319 genera (FishBase) phoxinin: North American and Far Eastern species Phylogeny based on morphology (Cavender and Coburn, 1992) Leuciscinae

33 33

34 ウグイ亜科の分類 phoxinin と leuciscin 中央アジアが Point だけどサンプルが少ない ウグイ亜科の進化史を考えると重要 今回アルタイで Oreoleuciscus を採集 Oreoleuciscus はどこに入るか ?

35 T. sachalinensis T. hakonensis T. brandtii T. nakamurai Low level of morphological differentiation Their taxonomy had been contentious (1 ~ 5 species). Tribolodon (Ikeda, 1937; Nakamura, 1963,1969; Onodera & Honma, 1976; Kurawaka, 1977) Endemic in the Far East Far Eastern phoxinin Inhabit the upper reaches of rivers, lakes and coastal regions of the sea

36 The pharyngeal teeth of Pseudaspius and Tribolodon species are similar. Pseudaspius leptocephalus P. leptocephalusT. nakamuraiT. sachalinensis (Tomoda, 1998) Previous molecular phylogenetic studies (Kartavtsev et al., 2002; Sakai et al., 2002, 2006; Sasaki et al., 2007) Pseudaspius and Tribolodon species are closely related in the Far Eastern phoxinin branch.

37 Widely distributed in Northern Hemisphere (Nelson, 2006) Body size small Classified into a single genus “Phoxinus” 7 species live in the Far East Degree of morphological differentiation is lower than the other genera P. phoxinus P. lagowskii P. perenurus Phoxinus Previous molecular phylogenetic studies (Sasaki et al., 2007) Far Eastern Phoxinus species and P. phoxinus are polyphyletic Far Eastern phoxinin

38 Phylogenetic analysis based on cyt b gene

39 cyt b gene sequences 1140 bp Useful to estimate phylogenetic relationships in closely related species Large number of sequence are registered in databases. North American 27 species Far Eastern 30 species European 36 species Outgroup 9 species (Cypridae 8, Cobitidae 1) Neighbor Joining (NJ) Analysis 45 genera 93 species

40 NJ tree based on cyt b gene

41 Far Eastern phoxinin North American phoxinin European leuciscin & North American Notemigonus North American phoxinin Phoxinus phoxinus Relationship among clades Unclear NJ tree based on cyt b gene

42 Phylogenetic analysis based on mt genome

43 mt genome analysis Long DNA sequences (Inoue et al., 2001a; Miya et al., 2003; Saitoh et al., 2006) Determined mt genome sequences ca. 16,600 bp (circular) Genomic structure common with vertebrates Exclude ND6, control region and gaps (14,969 bp) mt genome of Leuciscinae species North American 10 species Far Eastern 13 species European 7 species Selected species from major clades in the cyt b-based tree 16 genera 30 species Outgroup 9 species (Cypridae 8, Cobitidae 1) Maximum likelihood (ML) Analysis (RAxML) Correct estimation of phylogeny at various taxonomic levels with strong statistical support

44 Far Eastern European North American ML tree based on mt genome

45 ML tree based on mt genome gene Far Eastern European North American ML tree based on mt genome

46 phoxinin leuciscin Far Eastern European North American This analysis supports the classification by Cavender and Coburn (1992) Divided into 2 clades; phoxinin & leuciscin

47 Far Eastern European North American The Far Eastern phoxinins Tribolodon, Pseudaspius, Phoxinus Monophyletic and greatly diverged from the other Leuciscinae clades

48 Far Eastern European North American Pseudaspius leptocephalus Tribolodon brandtii Tribolodon species and Pseudaspius leptocephalus A single genus ? Subclade with 100% statistical supports

49 Far Eastern European North American North American species Divided into some independent clades Notemigonus cryleucasEuropean leuciscin clade

50 Far Eastern European North American Far Eastern Phoxinus species, European P. phoxinus, North American P. eos P. eos P. lagowskii P. phoxinus Polyphyletic Some different genera ?

51 Far Eastern European North American mt genome tree Divergence time estimation L Mya North America isolation from Eurasia The oldest and reliable fossils of Cyprinidae (Cavender, 1991) Fossil record of Pseudorasbora (Liu and Su, 1962) U 54.8 L 49.0 Mya L 3.0 Mya Lower constraint : L Upper constraint : U Bayesian method; mcmctree (PAML 4; Yang and Rannala, 2006)

52 15.14 Mya Mya 8.82 Mya 4.37 Mya Mya Far Eastern European North American

53 Far Eastern European North American 1.81 ~ 4.37 Mya Tribolodon speciation The glacial period ~ Mya Radiation of Leuciscinae Rapid global cooling of Middle Miocene The sea level dropped The land area expansion, freshwater and brackish water area increased Environment habitable for Leuciscinae extended Enlarge their distribution and occurred speciation

54

55 (Miya and Nishida, 1999) Long PCR Cycle sequencing Same primers as for the nested PCR Nested PCR 162 Fish-versatile primers 55 cyprinid-specific primers Determination of whole mt genome sequences 4 combinations of Fish-versatile primers


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