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Morphological Evolution from Aquatic to Terrestrial in the Genus Oreolalax (Amphibia, Anura, Megophryidae)

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Morphological Evolution from Aquatic to Terrestrial in the Genus Oreolalax (Amphibia, Anura, Megophryidae) Available online at www.sciencedirect.com Progress in Natural Science 19 (2009) 1403–1408 www.elsevier.com/locate/pnsc Short communication Morphological evolution from aquatic to terrestrial in the genus Oreolalax (Amphibia, Anura, Megophryidae) Gang Wei a,b,c, Bin Wang c, Ning Xu b, Zizhong Li a, Jianping Jiang c,* a Institute of Entomology, Guizhou University, Guiyang 550025, China b Centre of Ecology, Guiyang College, Guiyang 550005, China c Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China Received 18 January 2009; received in revised form 23 February 2009; accepted 23 February 2009 Abstract A phylogeny of 17 species in the genus Oreolalax is reconstructed based on 21 morphological characters from adult specimens, skel- eton specimens, tadpoles and eggs. Four species groups are recognized, of which the O. rugosus species group is the most primitive, the O. weigoldi species group is the second, the O. omeimontis species group is the third and the O. pingii species group is the most recently diversified. Based on the evolutional tendency of the morphological characters on the phylogenetic tree, it is proposed that the evolution of tympanum, tympanic annulus, columella, spoon-like cartilage and the web between toes reflect the habit changes from aquatic to ter- restrial. Thus, Oreolalax is regarded as one important representative genus to study further the evolution of morphological characters from aquatic to terrestrial. Ó 2009 National Natural Science Foundation of China and Chinese Academy of Sciences. Published by Elsevier Limited and Science in China Press. All rights reserved. Keywords: Aquatic; Terrestrial; Morphology; Evolution; Oreolalax 1. Introduction evolution, geographic distribution and differentiation of high-altitude pelobatid toads (=Megophryidae) in Asia [5]. It is well known that amphibians are transitional verte- Megophryid genus Oreolalax Myers and Leviton, 1962, just brates from aquatic to terrestrial. There are more than occurred in this area and mainly distributed in the middle- 6000 species in the class Amphibia in the world [1]. However, southern part of the Hengduan Mountains and adjacent in this group with so high a biodiversity, the evolutionary areas, restrained by the Qinghai-Tibet Plateau in the west tendency of morphological characters from aquatic animals [6]. Therefore, genus Oreolalax could be used as an example to terrestrial animals based on phylogeny remains unclear. evolving from aquatic to terrestrial in vertebrates around the The southern part of the Qinghai-Tibet Plateau was ocean Hengduan Mountains. The validity of Oreolalax was reeval- during the Paleocene Epoch [2]. The Indian block colliding uated by Fei et al. [7] and has widely been accepted [1,6,8– with Eurasia led to a large-scale Qinghai-Tibet Plateau as 10], which has only 17 species and could be classified into well as adjacent areas (including the Hengduan Mountains) four species groups: the O. rugosus species group, the O. wei- [3]. The historically stable environment of the Hengduan goldi species group, the O. omeimontis species group and the Mountains was in high favor for maintaining biodiversity O. pingii species group [6]. This study aims to reconstruct [4]. The Hengduan Mountains might be the centre of origin, phylogeny within the genus based on morphological charac- ters, study relationships between morphological transfor- * Corresponding author. Tel.: +86 13668280192. mation and environment change and further investigate E-mail address: [email protected] (J. Jiang). the origin and differentiation centre of the genus. 1002-0071/$ - see front matter Ó 2009 National Natural Science Foundation of China and Chinese Academy of Sciences. Published by Elsevier Limited and Science in China Press. All rights reserved. doi:10.1016/j.pnsc.2009.02.010 1404 G. Wei et al. / Progress in Natural Science 19 (2009) 1403–1408 2. Materials and methods Table 2 Morphological characters of the genus Oreolalax. 2.1. Specimens Character number Character state 01 23 Our analyses included 1307 morphological specimens of 1. Spoon-like cartilage Absent Present 17 species and 50 skeleton specimens of 16 species within 2. Columella Short Long Oreolalax (Table 1), of which information of O. weigoldi 3. Post-otic projection of Absent Present was obtained from the description of Ohler and Dubois squamosal [11]. In addition, 44 morphological specimens and 5 skele- 4. Linea musculinae Absent Present 5. Spinal patches on the Not Apparent ton specimens of two species of genus Scutiger were lower arm apparent selected as the outgroup in our analyses, as Scutiger is a sis- 6. Ratio of spinal patches Large Small (<0.3) ter to Oreolalax based on the results of Delorme and width on the chest to the (>0.4) Dubois [12] and our work (unpublished) on the phylogeny chest width of Megophryidae. All specimens were deposited in the 7. Density of spines on the Small Large (<5 chest (>10 granules/ Chengdu Institute of Biology (CIB), the Chinese Academy granules/ mm2) of Science (CAS). mm2) 8. Spines on both sides of Absent Present 2.2. Cladistic analysis the belly 9. Tympanum Absent Concealment Apparent 10. Ratio of tympanic Tympanic Small (<0.2) large According to the criteria of Ye et al. [13], plesiomorphy annulus to eye diameter annulus (>0.3) (0) or apomorphy (1), or autopomorphic character (2 or 3) absent was determined for the 21 morphological characters used 11. Opening of eustachian Small Large in this study (Table 2). tube The morphological data matrix of the 17 species with 12. Color pattern on belly Present Absent 13. Web between toes Present Absent their character state (Table 3) was used in this phylogenetic 14. Spines in lip margins Present Absent analysis using PAUP version 4.10b [14]. All characters 15. Ratio of the length of Short Long (>0.6) were ordered and equally weighted. The MP tree was fore arm and hand to (<0.6) reconstructed by a heuristic search with 1000 randomly- body length added-sequence replicates. Tree-bisection-reconnection 16. Ratio of tibia length to Short Long (>0.45) body length (<0.45) branches were swapped, and only one parsimonious tree 17. Spines on the back Present Absent was held each time. The clade robustness in the MP tree 18. Color pattern on back Absent Present was assessed by the bootstrap analysis: 1000 replicates, 19. Spines on the metatarsal Absent Present 100 randomly added samples and one tree held at each 20. Labial tooth formula of <4 row 4 row 5 or 6 >6 step. tadpole row row 21. Egg pigment Present Absent Table 1 Specimen information. 3. Results Species Location Specimens Skeleton Others (China number number We obtained one maximum parsimonious tree for the Province) genus Oreolalax from the parsimony analysis based on 21 Oreolalax popei Sichuan #25$2 #5$1 Eggs, tadpoles morphological characters. The parameters of this tree were O. omeimontis Sichuan #3$3 #1 Eggs, tadpoles O. major Sichuan #4$2 #1 Eggs, tadpoles as follows: tree length = 60, consistency index (CI) = O. liangbeiensis Sichuan #50$88 #4 Eggs, tadpoles 0.4167 and retention index (RI) = 0.6569. O. pingii Sichuan #168$137 #4 Eggs, tadpoles The maximum parsimonious tree showed that O. shmidti O. schmidti Sichuan #68$4 #4 Eggs, tadpoles was a sister to O. puxiongensis supported by synapomor- O. puxiongensis Sichuan #236$18 #4 Eggs, tadpoles phies 12 (color pattern on belly absent), 13 (web between O. lichuanensis Hubei #71$3 #4 Eggs, tadpoles O. rhodostigmatus Guizhou, #3$2 #1 Eggs, tadpoles toes absent) and 20 (labial tooth formula of tadpole >4 Hubei row). Oreolalax omeimontis was a sister to O. lichuanensis O. chuanbeiensis Sichuan #25$2 #4 Eggs, tadpoles supported by synapomorphies 16 (ratio of tibia length to O. rugosus Sichuan #43$46 #3$1 Eggs, tadpoles body length >0.45) and 20 (labial tooth formula of tadpole O. jingdongensis Yunan #32$2 #4 Eggs, tadpoles >4 row). Oreolalax pingii was a sister to node 15 supported O. granulosus Yunan #13$2 #4 Eggs, tadpoles O. weigoldi Sichuan #1 Eggs by synapomorphies 5 (spinal patches on the lower arm O. multipunctatus Sichuan #2 #1 Eggs, tadpoles apparent), 17 (spines on the back absent) and 21 (egg pig- O. nanjiangensis Sichuan #11$8 #2 Tadpoles ment absent). Node 13 was supported by synapomorphies Scutiger sikimmensis Tibet #5$1 #3 Eggs, tadpoles 2 (columella long), 3 (post-otic projection of squamosal S. nyingchiensis Tibet #35$3 #2 Eggs, tadpole present), 4 (linea musculinae present) and 9 (tympanum G. Wei et al. / Progress in Natural Science 19 (2009) 1403–1408 1405 Table 3 Morphological data matrix for phylogenetic analysis of the genus Oreolalax. Species Character code 123456789101112131415161718192021 O. omeimontis 11111000121010011102 1 O. popei 11100110120010111102 0 O. liangbeiensis 11100000110100011101 0 O. chuanbeiensis 11100000110000010101 0 O. major 11100001121000010101 1 O. lichuanensis 11111110121000011112 1 O. rugosus 00000100000000010101 0 O. xiangchengensis 00100000000100011001 0 O. pingii 11111000121110001101 1 O. schmidti 11110000121111000102 1 O. puxiongensis 11110000121110000112 0 O. granulosus 00000000000000010101 0 O. jingdongensis 01000010000000011101 0 O. nanjiangensis 111000101211110101029a O. multipunctatus 10990000121111011102 1 O. weigoldi 99990001199101110009 1 O. rhodostigmatas 11100000221011001103 1 S. nyingchiensis 00000000000100000001 0 S. sikkimensis 01000000000010000000 0 a “9” means the character state unknown. concealment). Oreolalax multipunctatus was a sister to O. The node consisting of O. xiangchengensis, O. jingdongensis, rhodostigmatas supported by synapomorphies 16 (ratio of O. rugosus and O. granulosus was a sister to the clade tibia length to body length long >0.45), 17 (spines on the consisting of O. chuanbeiensis, O. liangbeiensis, O. major back absent) and 21 (egg pigment absent). Oreolalax nanji- and O. weigoldi supported by synapomorphy 16 (ratio of angensis was a sister to node 12 supported by synapomor- tibia length to body length long). phies 13 (web between toes absent) and 14 (spines in lip margins absent). Node 10 was supported by synapomorphy 4. Discussion 11 (opening of the eustachian tube is large).
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