Reproductive isolation in sympatric Salvia species sharing a sole pollinator

doi:10.17520/biods.2017039

Abstract

Abstract:

Reproductive isolation (RI) is one of the key factors for speciation and diversity maintenance, however, there are differences in formation stage, means, and strength of RI for different species. To assess the effects and the significance of reproductive isolation in Salvia species, we compared flowering, pollination, and reproduction characteristics of Salvia liguliloba and S. bowleyana, which grow sympatrically and have overlapping flowering periods in the Tianmu Mountain, Zhejiang. Furthermore, artificial hybridization between the two species were conducted to estimate and understand their genetic compatibility and reproductive isolation. Results indicated that the two Salvia species considerably differed in their flower morphological structures, inflorescence organization, and the number of flowers produced per inflorescence. Bombus trifasciatus is the sole pollinator for these two species during the overlapping flowering period. However, different visitation behavior and floral structure (P < 0.05) leads to obviously different pollination patterns between the two species. Pollen is deposited on distinctly separate areas of the pollinator’s body in a manner precluding contact with any heterospecific Salvia stigmata. Under natural condition, the two species are equally successful in reproduction (natural seed set > 87%). Artificial pollination and hybridization experiments between these two species showed that they have a higher genetic compatibility. The cross seed sets are 77.8 ± 10.7% and 78.7 ± 11.2% when the two species are reciprocally cross parents. Our research suggests that for the two Salvia species lacking genetic incompatibility systems and relying on pollinators for outcrossing, there are differences in floral structures and pollen placement sites. The mechanical isolation (a form of pre-pollination RI) prevents heterospecific pollen interference and natural hybridization of the two different species that grow sympatrically and have overlapping flowering periods, and also maintains species diversity and the constancy of species heredity.

Key words: mechanical isolation, genetic compatibility, species diversity, natural hybridization, Bombus trifasciatus

Yukun Wei, Yanbo Huang, Guibin Li. Reproductive isolation in sympatric Salvia species sharing a sole pollinator[J]. Biodiv Sci, 2017, 25(6): 608-614.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2017039

https://www.biodiversity-science.net/EN/Y2017/V25/I6/608

Figures/Tables 5

References 21

[1]	Baack E, Melo MC, Rieseberg LH, Ortiz-Barrientos D (2015) The origins of reproductive isolation in plants. New Phytologist, 207, 968-984.
[2]	Claßen-Bockhoff R, Speck T, Tweraser E, Wester P, Thimm S, Reith M (2004) The staminal lever mechanism in Salvia L. (Lamiaceae): a key innovation for adaptive radiation? Organisms Diversity & Evolution, 4, 189-205.
[3]	Claßen-Bockhoff R, Wester P, Tweraser E (2003) The staminal lever mechanism in Salvia L. (Lamiaceae): a review. Plant Biology, 5, 33-41.
[4]	Epling C (1947) Natural hybridization of Salvia apiana and S. mellifera. Evolution, 1, 69-78.
[5]	Hopkins R (2013) Reinforcement in plants. New Phytologist, 197, 1095-1103.
[6]	Huang S, Shi X (2013) Floral isolation in Pedicularis: how do congeners with shared pollinators minimize reproductive interference? New Phytologist, 199, 858-865.
[7]	Huang YB, Wei YK, Ge BJ, Wang Q (2014) Research progress in pollination biology of genus Salvia (Lamiaceae) and their pollination mechanisms in East Asia (China). Acta Ecologica Sinica, 34, 2282-2289. (in Chinese with English abstract)
	[黄艳波, 魏宇昆, 葛斌杰, 王琦 (2014) 鼠尾草属东亚分支的传粉模式. 生态学报, 34, 2282-2289.]
[8]	Huang YB, Wei YK, Wang Q, Xiao YE, Ye XY (2015) Floral morphology and pollination mechanism of Salvia liguliloba, a narrow endemic species with degraded lever-like stamens. Chinese Journal of Plant Ecology, 39, 753-761. (in Chinese with English abstract)
	[黄艳波, 魏宇昆, 王琦, 肖月娥, 叶喜阳 (2015) 舌瓣鼠尾草退化杠杆雄蕊的相关花部特征及传粉机制. 植物生态学报, 39, 753-761.]
[9]	Huang Z, Liu H, Huang S (2015) Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body. Journal of Plant Ecology, 8, 109-115.
[10]	Kipling R, Warren J (2013) How generalists coexist: the role of floral phenotype and spatial factors in the pollination systems of two Ranunculus species. Journal of Plant Ecology, 7, 480-489.
[11]	Ma YP, Xie WJ, Sun WB, Marczewski T (2016a) Strong reproductive isolation despite occasional hybridization between a widely distributed and a narrow endemic Rhododendron species. Scientific Reports, 6, 19146.
[12]	Ma YP, Zhou RC, Milne R (2016b) Pollinator-mediated isolation may be an underestimated factor in promoting homoploid hybrid speciation. Frontiers in Plant Science, 7, 1183.
[13]	Melo MC, Grealy A, Brittain B, Walter GM, Ortiz-Barrientos D (2014) Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel. New Phytologist, 203, 323-334.
[14]	Meyn O, Emboden WA (1987) Parameters and consequences of introgression in Salvia apiana × S. mellifera (Lamiaceae). Systematic Botany, 12, 390-399.
[15]	Pauw A (2013) Can pollination niches facilitate plant coexistence? Trends in Ecology & Evolution, 28, 30-37.
[16]	Pedron M, Buzatto CR, Singer RB, Batista JAN, Moser A (2012) Pollination biology of four sympatric species of Habenaria (Orchidaceae: Orchidinae) from southern Brazil. Botanical Journal of the Linnean Society, 170, 141-156.
[17]	Ruchisansakun S, Tangtorwongsakul P, Cozien RJ, Smets EF, Niet TVD (2016) Floral specialization for different pollinators and divergent use of the same pollinator among co-occuring Impatiens species (Balsaminaceae) from Southeast Asia. Botanical Journal of the Linnean Society, 181, 651-666.
[18]	Wei YK, Wang Q, Huang YB (2015) Species diversity and distribution of Salvia (Lamiaceae). Biodiversity Science, 23, 3-10. (in Chinese with English abstract)
	[魏宇昆, 王琦, 黄艳波 (2015) 唇形科鼠尾草属的物种多样性与分布. 生物多样性, 23, 3-10.]
[19]	Wester P, Claßen-Bockhoff R (2007) Floral diversity and pollen transfer mechanisms in bird-pollinated Salvia species. Annals of Botany, 100, 401-421.
[20]	Widmer A, Lexer C, Cozzolino S (2009) Evolution of reproductive isolation in plants. Heredity, 102, 31-38.
[21]	Yang FC (1992) Comprehensive Investigation Report on Natural Resource of Tianmu Mountain Nature Reserve. Zhejiang Science and Technology Press, Hangzhou. (in Chinese)
	[杨逢春 (1992) 天目山自然保护区自然资源综合考察报告. 浙江科学技术出版社, 杭州.]

	花冠长 Corolla length	花冠宽 Corolla width	花冠高 Corolla height	冠筒长 Tube length	冠口高 Entrance height	冠筒口高 Tube entrance height	冠筒口宽 Tube entrance width	花丝长 Filament length	药隔长 Connective length	雌蕊长 Pistil length
舌瓣鼠尾草 S. liguliloba	23.7 ± 0.74^a	5.31 ± 0.34^a	7.30 ± 0.67^b	19.5 ± 0.8^a	4.87 ± 0.61^b	4.87 ± 0.61^a	4.41 ± 0.52^a	2.39 ± 0.14^b	5.19 ± 0.33^b	23.7 ± 0.43^b
南丹参 S. bowleyana	22.8 ± 1.10^b	4.47 ± 0.26^b	16.6 ± 0.94^a	12.4 ± 0.76^b	11.2 ± 0.80^a	4.47 ± 0.28^a	3.21 ± 0.23^b	4.30 ± 0.26^a	14.3 ± 0.68^a	26.1 ± 1.85^a
P	0.0407	0.000	0.000	0.000	0.000	0.0585	0.000	0.000	0.000	0.0011

	花冠长 Corolla length	花冠宽 Corolla width	花冠高 Corolla height	冠筒长 Tube length	冠口高 Entrance height	冠筒口高 Tube entrance height	冠筒口宽 Tube entrance width	花丝长 Filament length	药隔长 Connective length	雌蕊长 Pistil length
舌瓣鼠尾草 S. liguliloba	23.7 ± 0.74^a	5.31 ± 0.34^a	7.30 ± 0.67^b	19.5 ± 0.8^a	4.87 ± 0.61^b	4.87 ± 0.61^a	4.41 ± 0.52^a	2.39 ± 0.14^b	5.19 ± 0.33^b	23.7 ± 0.43^b
南丹参 S. bowleyana	22.8 ± 1.10^b	4.47 ± 0.26^b	16.6 ± 0.94^a	12.4 ± 0.76^b	11.2 ± 0.80^a	4.47 ± 0.28^a	3.21 ± 0.23^b	4.30 ± 0.26^a	14.3 ± 0.68^a	26.1 ± 1.85^a
P	0.0407	0.000	0.000	0.000	0.000	0.0585	0.000	0.000	0.000	0.0011

	单株花序总数 No. of infloresce- nce in individual plant	假圆锥花序分枝数 No. of branch in a false panicle	假总状花序的轮伞花序数 No. of verticillaster in a false raceme	轮伞花序小花总数 No. of flower in a verticillaster	轮伞花序同时开放小花数 No. of flowering in a verticillaster	单株总花数 Total no. of flower in individual plant	单株总开花数 Total no. of flowering in individual plant
舌瓣鼠尾草 S. liguliloba	2.0±2.1^a (n = 35)	2.0±1.9^b (n = 39)	9.3±2.4^a (n = 83)	5.6±1.1^b (n = 93)	1.4±1.7^b (n = 234)	262±299^b (n = 26)	21±30^a (n = 36)
南丹参 S. bowleyana	2.2±0.45^a (n = 5)	5.8±3.0^a (n = 11)	9.5±1.9^a (n = 40)	9.8±1.9^a (n = 160)	1.8±1.0^a (n = 160)	891±472^a (n = 5)	48±56^a (n = 16)
P	0.681	0.0020	0.7166	0.000	0.0053	0.0005	0.089

	单株花序总数 No. of infloresce- nce in individual plant	假圆锥花序分枝数 No. of branch in a false panicle	假总状花序的轮伞花序数 No. of verticillaster in a false raceme	轮伞花序小花总数 No. of flower in a verticillaster	轮伞花序同时开放小花数 No. of flowering in a verticillaster	单株总花数 Total no. of flower in individual plant	单株总开花数 Total no. of flowering in individual plant
舌瓣鼠尾草 S. liguliloba	2.0±2.1^a (n = 35)	2.0±1.9^b (n = 39)	9.3±2.4^a (n = 83)	5.6±1.1^b (n = 93)	1.4±1.7^b (n = 234)	262±299^b (n = 26)	21±30^a (n = 36)
南丹参 S. bowleyana	2.2±0.45^a (n = 5)	5.8±3.0^a (n = 11)	9.5±1.9^a (n = 40)	9.8±1.9^a (n = 160)	1.8±1.0^a (n = 160)	891±472^a (n = 5)	48±56^a (n = 16)
P	0.681	0.0020	0.7166	0.000	0.0053	0.0005	0.089

	相对频次 Relative frequency	单花访问时间 Visit time per flower (s)	活跃度 Activity rate	访花频率 Visitation rate
舌瓣鼠尾草 S. liguliloba	0.14 ± 0.017^b (n = 3)	2.01 ± 0.85 ^a (n = 30)	9.71 ± 3.15^b (n = 7)	1.36 ± 0.17^b (n = 3)
南丹参 S. bowleyana	0.86 ± 0.017^a (n = 3)	1.80 ± 0.63 ^a (n = 30)	16.2 ± 3.4 ^a (n = 52)	13.9 ± 0.28^a (n = 3)
P	0.000	0.2758	0.000	0.000