Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae)

doi:10.1016/j.pld.2020.09.002

Plant Diversity ›› 2021, Vol. 43 ›› Issue (01): 1-14.DOI: 10.1016/j.pld.2020.09.002

• Articles • 下一篇

Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae)

Santosh Kumar Rana^a, Dong Luo^a, Hum Kala Rana^a,b, Shaotian Chen^c, Hang Sun^a

a CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
b University of the Chinese Academy of Sciences, Beijing 100049, China;
c College of Pharmaceutical Science, Yunnan University of Chinese Medicine, Kunming 650500, China

收稿日期:2020-03-17 修回日期:2020-09-01 出版日期:2021-02-25 发布日期:2021-03-25
通讯作者: Shaotian Chen, Hang Sun
基金资助:
The authors thank Dr Zhuo Zhou for his help with the molecular dating analysis, Raymond Porter and Alexander Robert O'Neill (USA) for valuable inputs and English editing, and Dr Niu Yang, YaZhou Zhang, Qia Wang for providing the plant photographs. This study was supported by the Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (2019QZKK0502), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20050203), NSFC-Yunnan joint fund to support key projects (U1802242), the Major Program of the National Natural Science Foundation of China (31590823) and the National Natural Science Foundation of China (31570203).

Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae)

Santosh Kumar Rana^a, Dong Luo^a, Hum Kala Rana^a,b, Shaotian Chen^c, Hang Sun^a

a CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
b University of the Chinese Academy of Sciences, Beijing 100049, China;
c College of Pharmaceutical Science, Yunnan University of Chinese Medicine, Kunming 650500, China

Received:2020-03-17 Revised:2020-09-01 Online:2021-02-25 Published:2021-03-25
Contact: Shaotian Chen, Hang Sun
Supported by:
The authors thank Dr Zhuo Zhou for his help with the molecular dating analysis, Raymond Porter and Alexander Robert O'Neill (USA) for valuable inputs and English editing, and Dr Niu Yang, YaZhou Zhang, Qia Wang for providing the plant photographs. This study was supported by the Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (2019QZKK0502), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20050203), NSFC-Yunnan joint fund to support key projects (U1802242), the Major Program of the National Natural Science Foundation of China (31590823) and the National Natural Science Foundation of China (31570203).

摘要/Abstract

摘要： The complex orogeny of the Himalaya and the Qinghai-Tibet Plateau (QTP) fosters habitat fragmentation that drives morphological differentiation of mountain plant species. Consequently, determining phylogenetic relationships between plant subgenera using morphological characters is unreliable. Therefore, we used both molecular phylogeny and historical biogeographic analysis to infer the ancestral states of several vegetative and reproductive characters of the montane genus Incarvillea. We determined the taxonomic position of the genus Incarvillea within its family and inferred the biogeographical origin of taxa through Bayesian inference (BI), maximum likelihood (ML) and maximum parsimony (MP) analyses using three molecular data sets (trnL-trnF sequences, nr ITS sequences, and a data set of combined sequences) derived from 81% of the total species of the genus Incarvillea. Within the genus-level phylogenetic framework, we examined the character evolution of 10 key morphological characters, and inferred the ancestral area and biogeographical history of the genus. Our analyses revealed that the genus Incarvillea is monophyletic and originated in Central Asia during mid-Oligocene ca. 29.42 Ma. The earliest diverging lineages were subsequently split into the Western Himalaya and Sino-Himalaya during the early Miocene ca. 21.12 Ma. These lineages resulted in five re-circumscribed subgenera (Amphicome, Olgaea, Niedzwedzkia, Incarvillea, and Pteroscleris). Moreover, character mapping revealed the ancestral character states of the genus Incarvillea (e.g., suffruticose habit, cylindrical capsule shape, subligneous capsule texture, absence of capsule wing, and loculicidal capsule dehiscence) that are retained at the earliest diverging ancestral nodes across the genus. Our phylogenetic tree of the genus Incarvillea differs from previously proposed phylogenies, thereby recommending the placement of the subgenus Niedzwedzkia close to the subgenus Incarvillea and maintaining two main divergent lineages.

关键词: Biodiversity hotspots, Biogeography, Incarvillea, Molecular phylogeny, Phytools, Stochastic character mapping

Abstract: The complex orogeny of the Himalaya and the Qinghai-Tibet Plateau (QTP) fosters habitat fragmentation that drives morphological differentiation of mountain plant species. Consequently, determining phylogenetic relationships between plant subgenera using morphological characters is unreliable. Therefore, we used both molecular phylogeny and historical biogeographic analysis to infer the ancestral states of several vegetative and reproductive characters of the montane genus Incarvillea. We determined the taxonomic position of the genus Incarvillea within its family and inferred the biogeographical origin of taxa through Bayesian inference (BI), maximum likelihood (ML) and maximum parsimony (MP) analyses using three molecular data sets (trnL-trnF sequences, nr ITS sequences, and a data set of combined sequences) derived from 81% of the total species of the genus Incarvillea. Within the genus-level phylogenetic framework, we examined the character evolution of 10 key morphological characters, and inferred the ancestral area and biogeographical history of the genus. Our analyses revealed that the genus Incarvillea is monophyletic and originated in Central Asia during mid-Oligocene ca. 29.42 Ma. The earliest diverging lineages were subsequently split into the Western Himalaya and Sino-Himalaya during the early Miocene ca. 21.12 Ma. These lineages resulted in five re-circumscribed subgenera (Amphicome, Olgaea, Niedzwedzkia, Incarvillea, and Pteroscleris). Moreover, character mapping revealed the ancestral character states of the genus Incarvillea (e.g., suffruticose habit, cylindrical capsule shape, subligneous capsule texture, absence of capsule wing, and loculicidal capsule dehiscence) that are retained at the earliest diverging ancestral nodes across the genus. Our phylogenetic tree of the genus Incarvillea differs from previously proposed phylogenies, thereby recommending the placement of the subgenus Niedzwedzkia close to the subgenus Incarvillea and maintaining two main divergent lineages.

Key words: Biodiversity hotspots, Biogeography, Incarvillea, Molecular phylogeny, Phytools, Stochastic character mapping

Santosh Kumar Rana, Dong Luo, Hum Kala Rana, Shaotian Chen, Hang Sun. Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae)[J]. Plant Diversity, 2021, 43(01): 1-14.

图/表 7

参考文献 42

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	灌草混交林地 SG	乔灌混交林地 TS	生态薪炭林地 FF	天然封育草地 RG	生态经济林地 PF	水平农田地 TF
林冠层物种数 Species of canopy layer (CS)	0.00±0.00^c	3.33±0.33^a	0.00±0.00^c	0.00±0.00^c	1.00±0.00^b	0.00±0.00^c
林冠层盖度 Cover of canopy layer (CC) (%)	0.00±0.00^c	56.67±6.89^a	0.00±0.00^c	0.00±0.00^c	40.33±2.91^b	0.00±0.00^c
灌木层物种数 Number of shrub species (SN)	3.33±0.33^a	1.33±0.33^b	2.00±0.00^b	0.00±0.00^c	0.00±0.00^c	0.00±0.00^c
灌木层盖度 Cover of shrub species (SC) (%)	33.15±1.15^b	23.21±1.15^c	43.67±0.88^a	0.00±0.00^d	0.00±0.00^d	0.00±0.00^d
草本层物种数 Number of herb species (HN)	6.00±0.58^b	8.00±0.58^a	9.00±0.58^a	6.67±0.33^b	4.33±0.33^c	3.33±0.33^c
草本层盖度 Cover of herb species (HC) (%)	70.33±3.18^a	67.67±1.45^a	60.00±2.89^ab	49.33±2.96^b	23.67±1.33^c	21.35±3.05^c
枯落物盖度 Cover of leaf litter (LC) (%)	60.12±2.89^ab	66.67±1.67^a	56.62±1.68^b	25.43±1.05^c	23.35±1.68^c	6.53±0.92^d
枯落物厚度 Depth of leaf litter (LD) (cm)	0.37±0.02^b	0.55±0.03^a	0.33±0.03^b	0.19±0.01^c	0.11±0.01^d	0.05±0.01^d
草本层生物量 Herbaceous biomass (HB) (g/m²)	156.41±37.68^a	72.40±7.26^b	72.50±3.95^b	51.27±7.90^b	50.21±1.66^b	18.95±2.09^b
土壤含水量 Soil water content (SW) (%)	21.64±0.32^a	20.71±0.35^a	20.15±0.32^a	14.13±0.57^c	18.01±0.14^b	18.13±0.29^b
海拔 Elevation (ELV) (m)	1,775.00	1,783.00	1,808.67	1,728.33	1,726.33	1,833.00
坡向 Slop aspect (SA)	东北坡Northeast	西南坡 Southwest	西坡 West	西南坡 Southwest	东南坡 Southeast	东北坡 Northeast
坡度 Slop gradient (SG)	10°	15°	23°	21°	8°	12°

	灌草混交林地 SG	乔灌混交林地 TS	生态薪炭林地 FF	天然封育草地 RG	生态经济林地 PF	水平农田地 TF
林冠层物种数 Species of canopy layer (CS)	0.00±0.00^c	3.33±0.33^a	0.00±0.00^c	0.00±0.00^c	1.00±0.00^b	0.00±0.00^c
林冠层盖度 Cover of canopy layer (CC) (%)	0.00±0.00^c	56.67±6.89^a	0.00±0.00^c	0.00±0.00^c	40.33±2.91^b	0.00±0.00^c
灌木层物种数 Number of shrub species (SN)	3.33±0.33^a	1.33±0.33^b	2.00±0.00^b	0.00±0.00^c	0.00±0.00^c	0.00±0.00^c
灌木层盖度 Cover of shrub species (SC) (%)	33.15±1.15^b	23.21±1.15^c	43.67±0.88^a	0.00±0.00^d	0.00±0.00^d	0.00±0.00^d
草本层物种数 Number of herb species (HN)	6.00±0.58^b	8.00±0.58^a	9.00±0.58^a	6.67±0.33^b	4.33±0.33^c	3.33±0.33^c
草本层盖度 Cover of herb species (HC) (%)	70.33±3.18^a	67.67±1.45^a	60.00±2.89^ab	49.33±2.96^b	23.67±1.33^c	21.35±3.05^c
枯落物盖度 Cover of leaf litter (LC) (%)	60.12±2.89^ab	66.67±1.67^a	56.62±1.68^b	25.43±1.05^c	23.35±1.68^c	6.53±0.92^d
枯落物厚度 Depth of leaf litter (LD) (cm)	0.37±0.02^b	0.55±0.03^a	0.33±0.03^b	0.19±0.01^c	0.11±0.01^d	0.05±0.01^d
草本层生物量 Herbaceous biomass (HB) (g/m²)	156.41±37.68^a	72.40±7.26^b	72.50±3.95^b	51.27±7.90^b	50.21±1.66^b	18.95±2.09^b
土壤含水量 Soil water content (SW) (%)	21.64±0.32^a	20.71±0.35^a	20.15±0.32^a	14.13±0.57^c	18.01±0.14^b	18.13±0.29^b
海拔 Elevation (ELV) (m)	1,775.00	1,783.00	1,808.67	1,728.33	1,726.33	1,833.00
坡向 Slop aspect (SA)	东北坡Northeast	西南坡 Southwest	西坡 West	西南坡 Southwest	东南坡 Southeast	东北坡 Northeast
坡度 Slop gradient (SG)	10°	15°	23°	21°	8°	12°

	乔灌混交林地 TS	生态薪炭林地 FF	天然封育草地 RG	生态经济林地 PF	水平农田地 TF
灌草混交林地 SG	0.63	0.67	0.46	0.39	0.49
乔灌混交林地 TS	-	0.61	0.50	0.44	0.39
生态薪炭林地 FF	-	-	0.44	0.45	0.42
天然封育草地 RG	-	-	-	0.52	0.50
生态经济林地 PF	-	-	-	-	0.63

	乔灌混交林地 TS	生态薪炭林地 FF	天然封育草地 RG	生态经济林地 PF	水平农田地 TF
灌草混交林地 SG	0.63	0.67	0.46	0.39	0.49
乔灌混交林地 TS	-	0.61	0.50	0.44	0.39
生态薪炭林地 FF	-	-	0.44	0.45	0.42
天然封育草地 RG	-	-	-	0.52	0.50
生态经济林地 PF	-	-	-	-	0.63

	回归模型 Regression model	r²	P
物种丰富度 Species richness	-11.68 + 5.35 SC + 0.78 HB + 1.64 SW	0.83	0.000^**
个体数量 Abundance of individual	76.80 + 12.23 LD + 3.42 CC	0.72	0.000^**

Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae)

Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae)

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科 Family	物种 Species	灌草混交林地 SG	乔灌混交林地 TS	生态薪炭林地 FF	天然封育草地 RG	生态经济林地 PF	水平农田地 TF	总个体数 Total	百分比 %
步甲科 Carabidae	直角通缘步甲 Pterostichus gebleri	284	333	419	56	144	79	1,315	29.32
	麻步甲 Carabus brandti	137	248	294	43	6	53	781	17.41
	赤胸长步甲 Dolichus halensis	24	16	2	0	290	316	648	14.45
	直角婪步甲 Harpalus corporosus	5	3	13	0	36	19	76	1.69
	蒙古伪葬步甲 Pseudotaphoxenus mongolicus	10	1	34	3	1	20	69	1.54
	婪步甲属一种 Harpalus sp.1	7	1	2	6	38	0	54	1.20
	锯步甲属一种 Pristosia sp.	33	4	10	0	1	1	49	1.09
	双斑猛步甲 Cymindis binotata	25	12	11	0	1	0	49	1.09
	婪步甲属一种 Harpalus sp.2	4	8	2	1	19	14	48	1.07
	半猛步甲 Cymindis daimio	20	3	10	1	2	0	36	0.8
	短翅伪葬步甲 Pseudotaphoxenus brevipennis	4	1	14	3	7	7	36	0.8
	黄鞘婪步甲 Harpalus pallidipennis	18	10	2	1	3	1	35	0.78
	婪步甲属一种 Harpalus sp.3	5	8	3	0	0	10	26	0.58
	婪步甲属一种 Harpalus sp.4	0	0	0	0	4	2	6	0.13
	中华金星步甲 Calosoma chinense	2	0	0	0	0	2	4	0.09
	考氏肉步甲 Broscus kozlovi	1	0	1	0	0	2	4	0.09
金龟科 Scarabaeidae	小驼嗡蜣螂 Onthophagus gibbulus	160	83	10	45	48	56	402	8.96
	中华嗡蜣螂 O. sinicus	150	11	8	5	11	18	203	4.53
	双顶嗡蜣螂 O. bivertex	3	0	1	0	0	0	4	0.09
	大黑蜣螂属一种 Catharsius sp.	0	4	0	0	0	0	4	0.09
虎甲科 Cicindelidae	星斑虎甲 Cicindela kaleea	72	118	37	25	19	44	315	7.02
	云纹虎甲 C. elisae	1	0	0	73	0	0	74	1.65
拟步甲科 Tenebrionidae	克小鳖甲 Microdera kraatzi	0	5	6	47	0	0	58	1.29
	异形琵甲 Blaps variolosa	11	0	2	5	0	2	20	0.45
	条纹琵甲 B. potanini	0	15	0	1	1	3	20	0.45
	扁长琵甲 B. variolaris	1	8	0	0	0	2	11	0.25
象甲科 Curculionidae	暗褐尖筒象 Myllocerus pelidnus	3	13	0	28	0	0	44	0.98
	苜蓿象甲 Hypera postica	4	0	0	0	0	0	4	0.09
	甜菜象甲 Bothynoderse punctiventris	2	1	1	0	0	0	4	0.09
芫菁科 Meloidae	苹斑芫菁 Mylabris calida	6	1	3	11	0	0	21	0.47
	凹胸黑芫菁 Epicauta xantusi	2	2	0	1	0	0	5	0.11
	暗头豆芫菁 Epicauta obscurocephala	2	2	0	0	0	0	4	0.09
鳃金龟科 Melolonthidae	小阔胫玛绢金龟 Maladera ovatula	2	2	3	1	0	1	9	0.20
	福婆鳃金龟 Brahmina faldermanni	2	1	1	0	0	0	4	0.09
粪金龟科 Geotrupidae	戴锤角粪金龟 Bolbotrypes davidis	0	0	4	0	0	0	4	0.09
埋葬甲科 Silphidae	尸葬甲 Necrodes littoralis	2	4	0	2	0	0	8	0.18
	大红斑葬甲 Nicrophorus japonicus	2	0	2	0	0	0	4	0.09
	黄斑葬甲一种 Nicrophorus sp.	0	3	1	0	0	0	4	0.09
瓢虫科 Coccinellidae	七星瓢虫 Coccinella septempunctata	3	0	0	0	0	4	7	0.16
	异色瓢虫 Harmonia axyridis	2	1	1	0	0	0	4	0.09
	多异瓢虫 Hippodamia variegata	0	1	0	0	3	0	4	0.09
	双七瓢虫 Coccinula quatuordecimpustulata	0	0	0	2	0	2	4	0.09
叩甲科 Chrysomelidae	暗色槽缝叩甲 Agrypnus musculus	2	0	2	0	0	0	4	0.09
总计 Total		1,011	923	899	360	634	658	4,485

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