小檗科鬼臼亚科多样性格局的演化历史和成因

doi:10.17520/biods.2023100

生物多样性 ›› 2023, Vol. 31 ›› Issue (7): 23100. DOI: 10.17520/biods.2023100

• 研究报告: 植物多样性 • 上一篇下一篇

小檗科鬼臼亚科多样性格局的演化历史和成因

陈馥艳¹^,², 游旨价¹^,^*(), 张秋月¹, 黄健¹, 星耀武¹^,^*()

1.中国科学院西双版纳热带植物园热带森林生态学重点实验室, 云南勐腊 666303
2.中国科学院大学, 北京 100049

收稿日期:2023-04-03 接受日期:2023-07-17 出版日期:2023-07-20 发布日期:2023-07-22
通讯作者: * E-mail: youzhijia@xtbg.ac.cn;ywxing@xtbg.org.cn
作者简介:ywxing@xtbg.org.cn
* E-mail: youzhijia@xtbg.ac.cn;
基金资助:
国家自然科学基金(32225005)

The diversification history of Podophylloideae (Berberidaceae) and its underlying drivers

Fuyan Chen¹^,², Chih-Chieh Yu¹^,^*(), Qiuyue Zhang¹, Jian Huang¹, Yaowu Xing¹^,^*()

1. CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303
2. University of Chinese Academy of Sciences, Beijing 100049

Received:2023-04-03 Accepted:2023-07-17 Online:2023-07-20 Published:2023-07-22
Contact: * E-mail: youzhijia@xtbg.ac.cn;ywxing@xtbg.org.cn

摘要/Abstract

摘要：

探究生物多样性在类群和空间不均一性的形成机制对于认识多样性的形成和演化规律具有重要意义, 也是生物学研究的热点之一。鬼臼亚科属于小檗科, 包含10属约89种, 属间物种数量差异巨大。本研究利用比较系统发育学的研究方法, 重建了鬼臼亚科的系统发育关系、分化时间和多样化历史, 并探讨了生物和非生物因素对净多样化速率的影响。研究结果表明鬼臼亚科起源于92.75 Myr, 净多样化速率在约23 Myr开始明显提升, 最显著的净多样化速率转变发生在21 Myr附近的淫羊藿属(Epimedium)分支上。基于性状的演化速率分析显示, 具有蜜距和分布在东亚亚热带的类群具有较高的净多样化速率, 但淫羊藿属特定的距长对其物种的净多样化速率没有影响; 果实类型、假种皮和气生茎的有无对类群间净多样化速率无影响。本研究表明功能性状的演化和中新世以来东亚地区季风气候的加强导致了鬼臼亚科内部多样性的分布不均。

关键词: 鬼臼亚科, 物种净多样化速率, 蜜距, 淫羊藿属, 东亚亚热带

Abstract

Aims: In this study, our objective is to test the hypothesis that species-rich group possess higher net diversification rates. We focus on the subfamily Podophylloideae in Berberidaceae as our study system. Additionally, we aim to investigate the combined effects of biotic and abiotic factors on diversification rates.

Methods: We reconstructed the phylogeny of Podophylloideae by using 77 chloroplast CDS genes and employing both maximum likelihood and Bayesian inference methods. To estimate divergence time, we used one second calibration and two fossil calibrations. Net diversification rates through time were estimated using BAMM. Additionally, we employed Hidden State Speciation and Extinction analysis (HiSSE) and Quantitative State Speciation and Extinction analysis (QuaSSE) to estimate the effect of four functional traits on diversification rates.

Results: Molecular dating, based on 77 chloroplast CDS genes, showed that Podophylloideae originated approximately 92.75 Myr (95% HPD, 86.84‒95.84 Myr) with a crown age of 85 Myr (95% HPD, 73.19‒94.94 Myr). The net diversification rate began to increase around 23 Myr ago, and the most significant rate shift accrued approximately 21 Myr along the Epimedium stem branch. The analysis of state-dependent diversification rate indicated that taxa with nectar spur in subtropical East Asia possessed a higher net diversification rate. However, the specific spur length in Epimedium did not have a significant effect on net diversification rate. Furthermore, fruit type, the presence of aril, or the presence of aerial stems did not exert any significant effect on net diversification rate.

Conclusions: Our results suggest that the variation in net diversification rates is driven by the presence of nectar spur and the intensification of the East Asian monsoon since the Miocene, which has shaped the discrepancy in species diversity in Podophylloideae.

Key words: Podophylloideae, net diversification rate, nectar spur, Epimedium, subtropical East Asia

陈馥艳, 游旨价, 张秋月, 黄健, 星耀武 (2023) 小檗科鬼臼亚科多样性格局的演化历史和成因. 生物多样性, 31, 23100. DOI: 10.17520/biods.2023100.

Fuyan Chen, Chih-Chieh Yu, Qiuyue Zhang, Jian Huang, Yaowu Xing (2023) The diversification history of Podophylloideae (Berberidaceae) and its underlying drivers. Biodiversity Science, 31, 23100. DOI: 10.17520/biods.2023100.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2023100

https://www.biodiversity-science.net/CN/Y2023/V31/I7/23100

图/表 8

图1 鬼臼亚科不同属的分布及花的形态多样性。(A)裸花草属, Walter Siegmund摄, CC BY-SA 3.0; (B)折瓣花属, Walter Siegmund摄, CC BY-SA 3.0; (C)北美桃儿七属, Wasrts摄, CC BY-SA 4.0; (D)山荷叶属, 游旨价摄; (E)二叶鲜黄连属, Krzysztof Ziarnek摄, CC BY-SA 4.0; (F)山槐叶属, Ori Fragman-Sapir摄, CC BY-SA 3.0; (G)桃儿七属, 游旨价摄; (H)鬼臼属, Cathy DeWitt摄, CC BY 4.0; (I)淫羊藿属, 游旨价摄; (J)鲜黄连属, Krzysztof Ziarnek摄, CC BY-SA 4.0。地图来自 https://vemaps.com。

Fig. 1 Distribution and flower morphological diversity of each genus in Podophylloideae. (A) Achlys, photo by Walter Siegmund/CC BY-SA 3.0; (B) Vancouveria, photo by Walter Siegmund/CC BY-SA 3.0; (C) Podophyllum, photo by Wasrts/CC BY-SA 4.0; (D) Diphylleia, photo by Chih-Chieh Yu; (E) Jeffersonia, photo by Krzysztof Ziarnek /CC BY-SA 4.0; (F) Bongardia, photo by Ori Fragman-Sapir/CC BY-SA 3.0; (G) Sinopodophyllum, photo by Chih-Chieh Yu; (H) Dysosma, photo by Cathy DeWitt/CC BY 4.0; (I)Epimedium, photo by Chih-Chieh Yu; (J) Plagiorhegma, photo by Krzysztof Ziarnek /CC BY-SA 4.0. The map is taken from https://vemaps.com.

表1 本研究新采集的淫羊藿属信息及上传至GenBank的序列号

Table 1 Sampling information of newly sequenced Epimedium in this study

物种 Species	采集地点 Sampling site	序列号 Accession no.
天全淫羊藿 E. flavum	中国四川省天全县二郎山 Erlang Mountain, Tianquan County, Sichuan, China (29.87° N, 102.31° E)	OQ674756
短茎淫羊藿 E. brachyrrhizum	中国贵州省岑巩县地郎 Dilang, Cengong County, Guizhou, China (27.32° N, 108.61° E)	OQ674753
黔岭淫羊藿 E. leptorrhizum	中国重庆市黔江区仰头山森林公园 Yangtoushan Forest Park, Qianjiang District, Chongqing, China (29.56° N, 108.79° E)	OQ674758
紫距淫羊藿 E. epsteinii	中国湖南省桑植县八大公山自然保护区 Badagong Mountain National Nature Reserve, Sangzhi County, Hunan, China (29.78° N, 110.09° E)	OQ674754
箭叶淫羊藿 E. sagittatum	中国重庆市忠县刺竹沟 Cizhugou, Zhong County, Chongqing, China (30.10° N, 108.03° E)	OQ674759
E. pubigerum	英国邱园(栽培) Kew Gardens, the United Kingdom (cultivated)	OQ674751
E. perralderianum	英国邱园(栽培) Kew Gardens, the United Kingdom (cultivated)	OQ674757
E. alpinum	英国邱园(栽培) Kew Gardens, the United Kingdom (cultivated)	OQ674755
E. diphyllum	英国邱园(栽培) Kew Gardens, the United Kingdom (cultivated)	OQ674750
E. grandiflorum var. thunbergianum	日本岩手县八幡平市 Hachimantai, Iwate Prefecture, Japan (39.95° N, 140.88° E)	OQ674752

表2 隐藏状态物种形成和灭绝分析使用的模型

Table 2 Selected models in Hidden State Speciation and Extinction analysis

模型 Model	性状状态 Trait state	成种速率 Speciation rate (λ)	灭绝速率 Extinction rate (μ)	转化率 Turnover rate (q)
CID	0, 1	λ₀ = λ₁	μ₀ = μ₁	q₀₁ ≠ q₁₀
BiSSE	0, 1	λ₀ ≠ λ₁	μ₀ ≠ μ₁	q₀₁ ≠ q₁₀
CID-2	0A, 1A, 0B, 1B	λ_0A = λ_1A, λ_0B = λ_1B	μ_0A = μ_1A, μ_0B = μ_1B	q_0A→1A = q_1A→0A, q_0B→1B = q_1B→0B
CID-4	0A, 1A, 0B, 1B, 0C, 1C, 0D, 1D	λ_0A = λ_1A, λ_0B = λ_1B, λ_0C = λ_1C, λ_0D = λ_1D	μ_0A = μ_1A, μ_0B = μ_1B, μ_0C = μ_1C, μ_0D = μ_1D	q_0A→1A = q_1A→0A, q_0B→1B = q_1B→0B, q_0C→1C = q_1C→0C, q_0D→1D = q_1D→0D
HiSSE FULL	0A, 1A, 0B, 1B, 0C, 1C, 0D, 1D	λ_0A ≠ λ_1A, λ_0B ≠ λ_1B, λ_0C ≠ λ_1C, λ_0D ≠ λ_1D	μ_0A ≠ μ_1A, μ_0B ≠ μ_1B, μ_0C ≠ μ_1C, μ_0D ≠ μ_1D	q_0A→1A ≠ q_1A→0A, q_0B→1B ≠ q_1B→0B, q_0C→1C ≠ q_1C→0C, q_0D→1D ≠ q_1D→0D

图2 鬼臼亚科系统关系(中文名称见附录1)。(a)和(b)分别为基于最大似然法和贝叶斯方法推断的拓扑结构, 节点处标出了小于100的自展值和小于1.00的后验概率。

Fig. 2 Phylogeny of Podophylloideae (See Chinese name in Appendix 1). (a) and (b) are topology of Maximum likelihood (ML) and Bayesian inference (BI). Bootstrap (BS) value from ML less than 100 and posterior probability (PP) from BI less than 1.00 are labeled on the nodes.

图3 鬼臼亚科的多样化历史。(a)鬼臼亚科分化时间树(节点处蓝色条带代表95%置信区间内的年龄范围), 以及用于HiSSE分析的4个形态性状和1个生境信息分布。其中, A表示有无蜜距(粉色为是, 灰色为否), B表示是否分布于东亚亚热带(绿色为是, 灰色为否), C表示果实类型(灰蓝色为干果, 灰色为浆果), D表示是否有假种皮(浅蓝色为是, 灰色为否), E表示是否有气生茎(深蓝色为是, 灰色为否)。(b)基于BAMM分析的鬼臼亚科的净多样化速率。(c)基于BAMM分析的淫羊藿属距长演化速率。(d)净多样化速率在系统树的分布。中文名称见附录1。

Fig. 3 Diversification history of Podophylloideae. (a) Dated phylogeny of Podophylloideae (horizontal bars at nodes indicate 95% credible intervals of the divergence time estimate), and 4 morphological characters and 1 habitat information used in HiSSE analysis. The colored squares labeled A?E corresponding to each species represents with or without spur (pink or grey), in or out of subtropical East Asia (green or grey), dry or fleshy fruit (bice or grey), with or without aril (light blue or grey), with or without aerial stem (dark blue or grey). (b) Diversification rate of Podophylloideae estimated by BAMM. (c) Rate of spur length evolution in Epimedium estimated by BAMM. (d) Diversification rate distribution on phylogenetic tree. See Chinese name in Appendix 1.

表3 HiSSE分析模型检测和各性状状态速率结果

Table 3 Model test and rates inferred from HiSSE analysis

性状 Trait	模型 Model	AIC	AICc	ΔAICc
有距 vs. 无距 With vs. without spur	CID	532.30	532.88	25.81
	BiSSE	505.82	507.07
	CID-2	522.09	533.02	25.95
	CID-4	510.59	513.40	6.33
	FULL	512.36	513.24	6.17
东亚亚热带 vs. 非东亚亚热带 In vs. out of subtropical East Asia	CID	531.12	531.70	27.54
	BiSSE	502.91	504.16
	CID-2	512.13	513.01	8.85
	CID-4	511.13	513.94	9.78
	FULL	521.24	532.16	28.00
果实类型 Fruit type	CID	495.95	496.53	20.94
	BiSSE	494.72	495.97	20.38
	CID-2	474.71	475.59
	CID-4	490.38	493.20	17.60
	FULL	502.27	513.20	37.61
有假种皮 vs. 无假种皮 With vs. without aril	CID	498.36	498.94	17.81
	BiSSE	496.64	497.89	16.76
	CID-2	480.25	481.13
	CID-4	508.39	511.20	30.07
	FULL	511.63	522.55	41.42
有气生茎 vs. 无气生茎 With vs. without aerial stem	CID	509.46	510.04	21.00
	BiSSE	487.79	489.04
	CID-2	490.63	491.51	2.47
	CID-4	491.49	494.31	5.47
	FULL	506.46	517.39	28.35

图4 基于二态性状进行多样化速率推断的HiSSE分析结果。(a)?(e)依次为对于是否有距, 是否分布在东亚亚热带, 是否有假种皮, 是否有气生茎和果实类型等性状状态下, HiSSE所推断最优模型下的分化、成种和灭绝速率。

Fig. 4 Result of Hidden State Speciation and Extinction analysis. (a)?(e) illustrate net diversification rate, speciation rate and extinction rate under the best models of the following 5 binary-state traits: the existence of spur, subtropical East Asian distribution, the existence of aril, the existence of aerial stem and fruit type.

图5 基于定量性状进行多样化速率推断的QuaSSE分析结果: 距长-净多样化速率的分布, 最优模型为modal。图例从左到右分别显示单峰模型、逻辑斯蒂模型和线性模型, 上边一行有漂移率, 下边一行没有漂移率。

Fig. 5 Quantitative state-dependent diversification rate estimation based on QuaSSE analysis. Pattern of spur length- diversification rate, Modal is the best model. The legends showed, from left to right, the Modal, Sigmoid, and Linear models, with drift rates in the top row and no drift rates in the bottom row.

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小檗科鬼臼亚科多样性格局的演化历史和成因

The diversification history of Podophylloideae (Berberidaceae) and its underlying drivers

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