Differential Evolutionary History in Visual and Olfactory Floral Cues of the Bee-Pollinated Genus Campanula (Campanulaceae)
Abstract
:1. Introduction
2. Results
2.1. Comparisons of Floral Colour Reflectance among Campanula Species
2.2. Comparisons of Floral Scent Bouquets among Campanula Species
2.3. Phylogenetic Signals in Floral Colour and Scent
2.3.1. Floral Color
2.3.2. Floral Scents
3. Discussion
3.1. Floral Colour and Its Evolution in Campanula
3.2. Floral Scent Composition and Its Evolution in Campanula
4. Materials and Methods
4.1. Study Species
4.2. Colour Measurements of Campanula Flowers and Bee Colour Hexagon
4.3. Sampling of Floral Scents
4.4. Chemical Characterization of Floral Scents
4.5. Statistical Analyses of Floral Colour and Scent
4.6. Phylogenetic Signals in Colour and Scent
4.6.1. Phylogenetic Reconstructions
4.6.2. Phylogenetic Signal and Phylogenetic Principal Component Analyses (pPCA)
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Compound Name | KI | GLO | LAC | LAT | MED | PER | PUN | RPC | RAP | ROT | THY | TRA |
---|---|---|---|---|---|---|---|---|---|---|---|---|
No. of compounds | 43 | 32 | 30 | 15 | 28 | 10 | 30 | 33 | 41 | 46 | 55 | |
Aliphatics | ||||||||||||
(E)-2-Hexenal * | 855 | - | - | - | - | - | - | - | - | 0.88 | - | |
(Z)-3-Hexenol * | 857 | - | - | - | - | - | - | - | - | 4.14 | - | |
(E)-2-Hexenol | 867 | - | - | - | - | - | - | - | - | 1.55 | - | |
Hexanol * | 868 | - | - | - | - | - | - | - | - | 1.21 | - | |
(Z)-3-Hexenyl acetate * | 1006 | 12.99 | 12.24 | - | - | 48.60 | - | - | 55.54 | - | 16.70 | |
Hexyl acetate * | 1013 | - | 0.13 | - | - | 28.93 | - | - | 2.64 | - | - | |
2-Nonanone * | 1094 | - | - | - | - | - | - | - | - | - | 1.26 | |
Tridecane * | 1300 | - | - | - | - | - | - | - | - | - | 4.61 | |
Aromatics | ||||||||||||
p-Methylanisole * | 1025 | 0.70 | - | 2.92 | - | - | - | - | - | - | - | |
Benzyl alcohol * | 1039 | - | - | - | - | 8.03 | - | 6.71 | 2.30 | 0.33 | - | |
Phenylacetaldehyde * | 1050 | - | - | - | - | 2.42 | - | 61.71 | 41.13 | - | - | 3.40 |
1-Phenylethanol | 1066 | - | - | - | - | - | - | - | 0.46 | - | - | |
o-Guaiacol * | 1095 | 0.33 | - | 0.23 | - | - | - | - | - | - | 0.06 | |
2-Phenylethanol * | 1121 | 4.29 | 0.11 | 0.75 | - | 5.58 | 6.76 | 9.87 | 9.85 | 2.68 | 0.20 | 4.60 |
Benzyl acetate * | 1169 | - | - | - | - | - | - | 1.30 | 0.25 | - | - | |
Methyl salicylate * | 1209 | 5.39 | - | - | - | - | - | 8.62 | 8.75 | 1.82 | 0.75 | |
o-Anisaldehyde | 1253 | 0.68 | - | - | - | - | - | - | - | - | - | |
2-Phenylethyl acetate * | 1263 | - | - | - | - | - | 0.31 | 0.80 | 0.25 | - | 0.10 | |
p-Anisaldehyde * | 1266 | 0.97 | - | - | - | - | 0.61 | - | - | - | - | |
4-Ethylguaiacol | 1287 | - | - | - | - | - | - | - | 0.10 | - | - | |
Irregular terpenes | ||||||||||||
4-Oxoisophorone * | 1151 | 1.37 | 0.03 | 0.31 | 1.90 | 0.16 | - | 0.47 | 0.59 | 0.06 | 0.12 | - |
Geranyl acetone * | 1460 | - | - | - | 4.05 | - | - | - | - | - | 0.24 | |
Monoterpenes | ||||||||||||
Artemisiatriene | 928 | - | - | - | - | - | - | - | - | 0.03 | - | |
α-Pinene * | 942 | - | - | - | - | 2.24 | - | - | - | - | - | - |
Sabinene * | 982 | 5.09 | - | 0.51 | - | 1.10 | - | - | - | - | 0.47 | - |
β-Pinene * | 985 | - | - | - | - | 0.57 | - | - | - | - | - | - |
β-Myrcene * | 995 | - | 0.51 | 2.14 | - | 8.52 | - | - | - | 0.45 | 7.01 | - |
α-Phellandrene * | 1010 | - | - | - | - | - | - | - | - | 0.38 | - | |
δ-3-Carene * | 1018 | 1.06 | - | 1.24 | - | - | - | - | - | - | 0.27 | |
α-Terpinene * | 1027 | - | - | - | 2.81 | - | - | - | - | 0.35 | - | |
Limonene * | 1036 | - | - | - | - | - | - | - | - | 3.77 | - | |
β-Phellandrene * | 1038 | - | - | - | - | - | - | - | - | 0.48 | - | |
(Z)-β-Ocimene * | 1040 | - | 20.26 | - | - | 8.18 | - | - | - | - | 1.60 | 4.16 |
Eucalyptol * | 1041 | - | - | - | 69.29 | - | - | - | - | 0.24 | - | |
(E)-β-Ocimene * | 1052 | - | 59.69 | - | - | 24.60 | - | - | - | 7.33 | 4.40 | 38.57 |
γ-Terpinene * | 1065 | - | - | - | - | - | - | - | - | 0.23 | - | |
(Z)-Linalool oxide (furanoid) * | 1079 | - | - | - | - | - | - | - | - | 0.09 | - | |
(E)-Linalol oxide (furanoid) * | 1094 | - | - | - | - | 1.31 | - | 9.67 | - | - | 1.03 | 0.05 |
Terpinolene * | 1096 | 0.46 | - | - | - | 0.32 | - | - | - | - | 0.93 | 0.07 |
Linalool * | 1103 | - | - | - | - | 1.57 | - | - | - | - | 10.30 | 1.95 |
Allo-ocimene * | 1132 | - | 0.64 | - | - | 3.60 | - | - | - | - | 0.55 | - |
p-Cymene * | 1133 | - | - | - | - | - | - | - | - | - | 0.43 | |
(E)-Epoxyocimene * | 1144 | - | 0.08 | - | - | 0.33 | - | - | - | - | - | 0.28 |
Neo-allo-ocimene * | 1145 | - | 0.02 | - | - | 0.27 | - | - | - | - | 0.04 | - |
Citronellal * | 1156 | - | - | - | - | - | - | - | - | 0.10 | - | |
Nerol oxide | 1159 | - | - | - | - | - | - | - | - | 0.11 | - | |
Dill ether | 1162 | - | 0.15 | - | - | - | - | - | - | 0.24 | - | |
(Z)-Isocitral | 1167 | - | - | - | - | - | - | - | - | 0.09 | - | |
Lavandulol | 1172 | - | - | 2.19 | - | - | - | - | - | 1.19 | - | |
p-Mentha-1,5-dien-8-ol | 1176 | - | 0.09 | - | - | - | - | - | - | - | - | |
(E)-Linalool oxide (pyranoid) | 1181 | - | - | - | - | - | 4.21 | - | - | 0.04 | - | |
(E)-Isocitral | 1185 | - | - | - | - | - | - | - | - | 0.18 | - | |
α-Terpineol * | 1203 | 0.63 | - | - | - | 1.78 | - | - | 0.38 | 0.20 | 1.53 | 0.03 |
Verbenone * | 1227 | - | - | - | - | - | - | - | - | - | 0.05 | |
β-Citronellol * | 1230 | - | - | - | - | - | - | - | - | 0.77 | - | |
Nerol * | 1234 | - | - | - | - | - | - | - | - | 22.86 | - | |
(Z)-Ocimenone | 1237 | - | 0.06 | - | - | - | - | - | - | - | - | |
Neral * | 1247 | - | - | - | - | - | - | - | - | 2.22 | - | |
Geraniol * | 1258 | - | - | - | - | - | - | - | - | 22.21 | - | |
Geranial * | 1276 | - | - | - | - | - | - | - | - | 2.69 | - | |
Lavandulyl acetate * | 1289 | 0.17 | - | 0.87 | 0.54 | - | - | 0.03 | 0.41 | 0.65 | - | |
Methyl geranate * | 1326 | - | - | - | - | - | - | - | - | 0.05 | - | |
N-compounds | ||||||||||||
Benzeneacetonitrile | 1147 | 1.69 | - | 3.80 | - | 0.59 | 3.08 | 0.72 | - | - | - | - |
Indole * | 1304 | - | - | - | - | - | 0.67 | 0.04 | 0.11 | - | - | |
1-Nitro-2-phenyl ethane | 1309 | 0.71 | - | 0.70 | - | 0.39 | 0.18 | - | - | - | - | |
o-Aminoacetophenone | 1313 | - | 0.37 | - | - | - | 0.23 | 0.12 | - | - | - | |
Sesquiterpenes | ||||||||||||
α-Cubebene | 1365 | 1.59 | - | - | 0.86 | - | 0.40 | 0.09 | 0.07 | - | 0.23 | |
α-Longipinene | 1379 | - | - | - | - | 0.48 | - | - | - | - | - | 0.12 |
α-Ylangene | 1389 | 2.04 | - | 68.8 | - | 10.78 | - | 2.00 | 0.61 | 1.43 | - | 0.68 |
α-Copaene * | 1395 | 6.47 | - | 0.63 | 2.73 | - | 1.17 | 0.16 | 0.69 | - | 0.34 | |
Longifolene * | 1402 | - | - | - | - | - | - | - | - | - | 0.08 | |
β-Bourbonene | 1407 | - | - | - | 2.13 | 0.67 | - | 1.67 | 3.05 | 0.94 | - | - |
β-Elemene | 1407 | - | - | - | - | - | - | - | - | - | 1.99 | |
Ylanga-2,4(15)-diene | 1422 | - | - | 0.21 | - | - | - | - | - | - | - | |
β-Cedrene | 1441 | 0.52 | - | 1.33 | - | - | - | 7.57 | 0.22 | - | 0.59 | |
(E)-β-Caryophyllene * | 1445 | 5.16 | - | 0.56 | 2.30 | 11.72 | - | - | 2.77 | 7.08 | 0.85 | 0.64 |
(E)-α-Bergamotene | 1454 | - | - | - | - | - | - | - | - | - | 2.08 | |
β-Gurjunene | 1460 | - | - | - | - | - | - | 0.20 | - | - | - | |
(E)-β-Farnesene * | 1460 | 2.05 | 0.30 | - | - | - | 0.50 | 0.31 | 0.08 | - | 1.79 | |
α-Caryophyllene * | 1480 | 0.45 | 0.18 | 0.11 | - | - | - | - | 1.51 | - | - | |
Prezizaene | 1484 | - | - | - | - | 0.62 | - | - | 3.60 | 0.03 | - | 1.58 |
Amorpha-4,11-diene | 1485 | - | - | - | - | - | - | - | - | - | 0.80 | |
Allo-aromadendrene | 1488 | 0.64 | - | - | 1.15 | - | 0.43 | 0.05 | 0.09 | - | - | |
β-Cubenene | 1493 | 0.12 | - | - | - | - | 0.13 | - | - | - | - | |
Ar-Curcumene | 1494 | - | - | - | - | - | - | 0.11 | Tr | - | 0.95 | |
γ-Muurolene | 1496 | 0.24 | - | - | - | - | 0.38 | 0.18 | 0.09 | - | - | |
(Z,E)-α-Farnesene * | 1496 | 0.27 | - | - | - | - | 0.15 | - | - | - | 0.42 | |
Germacrene D * | 1506 | 12.36 | - | - | - | 0.65 | - | - | 0.49 | 2.55 | - | 0.70 |
(E,E)-α-Farnesene * | 1510 | - | 0.06 | - | - | 0.70 | - | - | - | - | 0.22 | - |
β-Selinene | 1517 | - | - | - | - | - | - | - | - | - | 0.78 | |
α-Muurolene | 1527 | - | - | - | 2.17 | - | - | - | - | - | 1.35 | |
α-Selinene | 1529 | - | - | - | - | - | - | - | - | - | 0.50 | |
(Z)-γ-Bisabolene | 1535 | - | - | - | - | - | - | - | - | - | 0.69 | |
β-Sesquiphellandrene | 1542 | - | - | - | - | - | - | - | - | - | 0.69 | |
δ-Cadinene | 1542 | 1.36 | - | - | - | - | - | - | 0.26 | - | 0.42 | |
α-Calacorene | 1567 | - | - | - | - | - | - | - | - | - | 0.12 | |
Spiroacetals | ||||||||||||
1,6-Dioxaspiro[4.5] decane * | 1057 | - | - | 0.41 | 0.64 | 0.01 | 0.06 | - | - | - | - | 0.01 |
(E)-Conophthorin * | 1065 | 5.84 | - | 1.79 | 6.70 | 0.16 | 3.94 | 0.01 | - | 0.03 | 0.04 | 0.41 |
(Z)-Conophthorin * | 1140 | 0.41 | - | 0.13 | 1.53 | 0.16 | - | - | Tr | - | - | |
2-Methyl-1,7-dioxaspiro(5.5)undecane * | 1152 | - | - | - | - | - | - | - | - | - | 0.14 | |
7-Ethyl-1,6-dioxaspiro(4.5)decane * | 1156 | 0.31 | - | 0.42 | - | 0.06 | 0.16 | - | - | - | 0.93 | |
(Z)-7-Ethyl-1,6-dioxaspiro [4.5]decane * | 1231 | - | - | - | - | - | - | - | - | - | 0.08 | |
Unidentified: (no. of compounds), % amount | (11) | (15) | (9) | (1) | (4) | (0) | (8) | (9) | (10) | (3) | (9) | |
23.61 | 5.09 | 9.90 | 1.19 | 11.08 | - | 4.34 | 11.27 | 3.40 | 1.79 | 3.28 | ||
Total identified (%) | 76.39 | 94.91 | 90.1 | 98.81 | 88.92 | 100 | 95.66 | 88.73 | 96.6 | 98.37 | 96.72 |
References
- Dafni, A. Pollination Ecology—A Practical Approach; Oxford University Press: Oxford, UK, 1992; p. 242. [Google Scholar]
- Cox, P.A. Hydrophilous pollination. Annu. Rev. Ecol. Syst. 1988, 19, 261–279. [Google Scholar] [CrossRef]
- Ackerman, J.D. Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives. Plant Syst. Evol. 2000, 222, 167–185. [Google Scholar] [CrossRef]
- Ollerton, J.; Winfree, R.; Tarrant, S. How many flowering plants are pollinated by animals? Oikos 2011, 120, 321–326. [Google Scholar] [CrossRef]
- Schiestl, F.P.; Huber, F.K.; Gomez, J.M. Phenotypic selection on floral scent: Trade-off between attraction and deterrence? Evol. Ecol. 2010, 25, 237–248. [Google Scholar] [CrossRef] [Green Version]
- Schiestl, F.P.; Johnson, S.D. Pollinator-mediated evolution of floral signals. Trends Ecol. Evol. 2013, 28, 307–315. [Google Scholar] [CrossRef]
- Shrestha, M.; Dyer, A.G.; Boyd-Gerny, S.; Wong, B.B.M.; Burd, M. Shades of red: Bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytol. 2013, 198, 301–310. [Google Scholar] [CrossRef] [PubMed]
- Faegri, K.; van der Pijl, L. The Principles of Pollination Ecology, 3rd ed.; Pergamon Press: Oxford, UK, 1979. [Google Scholar]
- Michener, C.D. The Bees of the World, 2nd ed.; The Johns Hopkins University Press: Baltimore, MD, USA, 2007; p. 992. [Google Scholar]
- Roubik, D.W. Ecology and Natural History of Tropical Bees, 1st ed.; Cambridge University Press: New York, NY, USA, 1989; p. 514. [Google Scholar]
- Chittka, L.; Raine, N.E. Recognition of flowers by pollinators. Curr. Opin. Plant Biol. 2006, 9, 428–435. [Google Scholar] [CrossRef]
- Willmer, P. Pollination and Floral Ecology; Princeton University Press: Princeton, NJ, USA, 2011. [Google Scholar]
- Ollerton, J.; Alarcón, R.; Waser, N.M.; Price, M.V.; Watts, S.; Cranmer, L.; Hingston, A.; Peter, C.; Rotenberry, J. A global test of the pollination syndrome hypothesis. Ann. Bot. 2009, 103, 1471–1480. [Google Scholar] [CrossRef] [Green Version]
- Dobson, H.E.M. Relationship between floral frangrance composition and type of pollinator. In Biology of Floral Scent; Dudareva, N., Pichersky, E., Eds.; CRC Press: Boca Raton, FL, USA, 2006; pp. 147–198. [Google Scholar]
- Peitsch, D.; Fietz, A.; Hertel, H.; De Souza, J.; Ventura, D.; Menzel, R. The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A 1992, 170, 23–40. [Google Scholar] [CrossRef]
- Briscoe, A.D.; Chittka, L. The evolution of colorvision in insects. Annu. Rev. Èntomol. 2001, 46, 471–510. [Google Scholar] [CrossRef] [Green Version]
- Chittka, L. Does bee color vision predate the evolution of flower color? Naturwissenschaften 1996, 83, 136–138. [Google Scholar] [CrossRef]
- Robertson, H.M.; Wanner, K.W. The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family. Genome Res. 2006, 16, 1395–1403. [Google Scholar] [CrossRef] [Green Version]
- Burger, H.; Ayasse, M.; Dötterl, S.; Kreissl, S.; Galizia, C.G. Perception of floral volatiles involved in host-plant finding behaviour: Comparison of a bee specialist and generalist. J. Comp. Physiol. A 2013, 199, 751–761. [Google Scholar] [CrossRef] [Green Version]
- Schäffler, I.; Balao, F.; Dötterl, S. Floral and vegetative cues in oil-secreting and non-oil-secreting Lysimachia species. Ann. Bot. 2012, 110, 125–138. [Google Scholar] [CrossRef] [Green Version]
- Kovacic, S. The genus Campanula L. (Campanulaceae) in Croatia, circum-adriatic and west balkan region. Acta Bot. Croat. 2004, 63, 171–202. [Google Scholar]
- Binnenböse, S. Blüten-und Reproduktionsbiologie von Campanula; Bachelor Monograph; Universität Ulm: Ulm, Germany, 1995. [Google Scholar]
- Blionis, G.J.; Vokou, D. Pollination ecology of Campanula species on Mt Olympos, Greece. Ecography 2001, 24, 287–297. [Google Scholar] [CrossRef]
- Roquet, C.; Sáez, L.; Aldasoro, J.J.; Susanna, A.; Alarcón, M.L.; Garcia-Jacas, N. Natural Delineation, Molecular Phylogeny and Floral Evolution in Campanula. Syst. Bot. 2008, 33, 203–217. [Google Scholar] [CrossRef]
- Schlindwein, C.; Wittmann, D.; Martins, C.F.; Hamm, A.; Siqueira, J.A.; Schiffler, D.; Machado, I.C. Pollination of Campanula rapunculus L. (Campanulaceae): How much pollen flows into pollination and into reproduction of oligolectic pollinators? Plant Syst. Evol. 2005, 250, 147–156. [Google Scholar] [CrossRef]
- Stebbins, G.L. Adaptive Radiation of Reproductive Characteristics in Angiosperms, I: Pollination Mechanisms. Annu. Rev. Ecol. Syst. 1970, 1, 307–326. [Google Scholar] [CrossRef]
- Aigner, P.A. Optimality modeling and fitness trade-offs: When should plants become pollinator specialists? Oikos 2001, 95, 177–184. [Google Scholar] [CrossRef]
- Fialho, M.D.C.Q.; Guss-Matiello, C.P.; Zanuncio, J.C.; Campos, L.A.O. A comparative study of the antennal sensilla in corbiculate bees. J. Apic. Res. 2014, 53, 392–403. [Google Scholar] [CrossRef]
- Martin, J.P.; Beyerlein, A.; Dacks, A.M.; Reisenman, C.E.; Riffell, J.A.; Lei, H.; Hildebrand, J.G. The neurobiology of insect olfaction: Sensory processing in a comparative context. Prog. Neurobiol. 2011, 95, 427–447. [Google Scholar] [CrossRef]
- Wcislo, W.T. Sensilla numbers and antennal morphology of parasitic and non-parasitic bees (Hymenoptera: Apoidea). Int. J. Insect Morphol. Embryol. 1995, 24, 63–81. [Google Scholar] [CrossRef]
- Wittwer, B.; Hefetz, A.; Simon, T.; Murphy, L.E.K.; Elgar, M.; Pierce, N.E.; Kocher, S.D. Solitary bees reduce investment in communication compared with their social relatives. Proc. Natl. Acad. Sci. USA 2017, 114, 6569–6574. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brandt, K.; Dötterl, S.; Francke, W.; Ayasse, M.; Milet-Pinheiro, P. Flower Visitors of Campanula: Are Oligoleges More Sensitive to Host-Specific Floral Scents Than Polyleges? J. Chem. Ecol. 2016, 43, 4–12. [Google Scholar] [CrossRef] [PubMed]
- Clarke, K.R.; Gorley, R.N. Primer v6: User Manual/Tutorial; Primer-E: Plymouth, UK, 2006; p. 91. [Google Scholar]
- Arnold, S.E.J.; Faruq, S.; Savolainen, V.; McOwan, P.W.; Chittka, L. FReD: The Floral Reflectance Database—A Web Portal for Analyses of Flower Colour. PLoS ONE 2010, 5, e14287. [Google Scholar] [CrossRef]
- Dyer, A.G.; Boyd-Gerny, S.; McLoughlin, S.; Rosa, M.; Simonov, V.; Wong, B.B.M. Parallel evolution of angiosperm colour signals: Common evolutionary pressures linked to hymenopteran vision. Proc. R. Soc. B Biol. Sci. 2012, 279, 3606–3615. [Google Scholar] [CrossRef] [Green Version]
- McEwen, J.R.; Vamosi, J.C. Floral colour versus phylogeny in structuring subalpine flowering communities. Proc. R. Soc. B Biol. Sci. 2010, 277, 2957–2965. [Google Scholar] [CrossRef] [Green Version]
- Ings, T.C.; Raine, N.E.; Chittka, L. A population comparison of the strength and persistence of innate colour preference and learning speed in the bumblebee Bombus terrestris. Behav. Ecol. Sociobiol. 2009, 63, 1207–1218. [Google Scholar] [CrossRef]
- Raine, N.E.; Ings, T.C.; Dornhaus, A.; Saleh, N.; Chittka, L. Adaptation, Genetic Drift, Pleiotropy, and History in the Evolution of Bee Foraging Behavior. Adv. Study Behav. 2006, 36, 305–354. [Google Scholar] [CrossRef]
- Morawetz, L.; Svoboda, A.; Spaethe, J.; Dyer, A.G. Blue colour preference in honeybees distracts visual attention for learning closed shapes. J. Comp. Physiol. A 2013, 199, 817–827. [Google Scholar] [CrossRef] [PubMed]
- Milet-Pinheiro, P.; Ayasse, M.; Dötterl, S. Visual and Olfactory Floral Cues of Campanula (Campanulaceae) and Their Significance for Host Recognition by an Oligolectic Bee Pollinator. PLoS ONE 2015, 10, e0128577. [Google Scholar] [CrossRef] [PubMed]
- Kuss, P.; Ægisdóttir, H.H.; Stöcklin, J. The biological flora of Central Europe: Campanula thyrsoides L. Perspect. Plant Ecol. Evol. Syst. 2007, 9, 37–51. [Google Scholar] [CrossRef]
- Simonds, V.; Plowright, C. How do bumblebees first find flowers? Unlearned approach responses and habituation. Anim. Behav. 2004, 67, 379–386. [Google Scholar] [CrossRef]
- Raine, N.E.; Chittka, L. The Adaptive Significance of Sensory Bias in a Foraging Context: Floral Colour Preferences in the Bumblebee Bombus terrestris. PLoS ONE 2007, 2, e556. [Google Scholar] [CrossRef] [Green Version]
- Chittka, L.; Ings, T.C.; Raine, N.E. Chance and adaptation in the evolution of island bumblebee behaviour. Popul. Ecol. 2004, 46, 243–251. [Google Scholar] [CrossRef] [Green Version]
- Kevan, P.G. Insect Pollination of high artic flowers. J. Ecol. 1972, 60, 831–847. [Google Scholar] [CrossRef]
- Arnold, S.E.J.; Savolainen, V.; Chittka, L. Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod-Plant Interact. 2009, 3, 27–43. [Google Scholar] [CrossRef]
- Wardle, P. Origin of the New Zealand mountain flora, with special reference to trans-Tasman relationships. N. Z. J. Bot. 1978, 16, 535–550. [Google Scholar] [CrossRef]
- Prieto-Benítez, S.; Millanes, A.M.; Dötterl, S.; Giménez-Benavides, L. Comparative analyses of flower scent in Sileneae reveal a contrasting phylogenetic signal between night and day emissions. Ecol. Evol. 2016, 6, 7869–7881. [Google Scholar] [CrossRef] [Green Version]
- Schäffler, I.; Steiner, K.E.; Haid, M.; Van Berkel, S.S.; Gerlach, G.; Johnson, S.D.; Wessjohann, L.A.; Dötterl, S. Diacetin, a reliable cue and private communication channel in a specialized pollination system. Sci. Rep. 2015, 5, 12779. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jürgens, A.; Wee, S.-L.; Shuttleworth, A.; Johnson, S.D. Chemical mimicry of insect oviposition sites: A global analysis of convergence in angiosperms. Ecol. Lett. 2013, 16, 1157–1167. [Google Scholar] [CrossRef]
- Maia, A.C.D.; Dötterl, S.; Kaiser, R.; Silberbauer-Gottsberger, I.; Teichert, H.; Gibernau, M.; Navarro, D.M.A.F.; Schlindwein, C.; Gottsberger, G. The Key Role of 4-methyl-5-vinylthiazole in the Attraction of Scarab Beetle Pollinators: A Unique Olfactory Floral Signal Shared by Annonaceae and Araceae. J. Chem. Ecol. 2012, 38, 1072–1080. [Google Scholar] [CrossRef] [PubMed]
- Milet-Pinheiro, P.; Gonçalves, E.G.; Navarro, D.M.D.A.F.; Nuñez-Avellaneda, L.A.; Maia, A.C.D. Floral scent chemistry and pollination in the Neotropical aroid genus Xanthosoma (Araceae). Flora 2017, 231, 1–10. [Google Scholar] [CrossRef]
- Milet-Pinheiro, P.; Gerlach, G. Biology of the Neotropical orchid genus Catasetum: A historical review on floral scent chemistry and pollinators. Perspect. Plant Ecol. Evol. Syst. 2017, 27, 23–34. [Google Scholar] [CrossRef]
- Blight, M.M.; Le Métayer, M.; Delègue, M.-H.P.; Pickett, J.A.; Marion-Poll, F.; Wadhams, L.J. Identification of Floral Volatiles Involved in Recognition of Oilseed Rape Flowers, Brassica napus by Honeybees, Apis mellifera. J. Chem. Ecol. 1997, 23, 1715–1727. [Google Scholar] [CrossRef]
- Ramirez, S.; Dressler, R.L.; Ospina, M. Abejas euglosinas (Hymenoptera: Apidae) de la région neotropical: Listado de especies con notas sobre su biología. Biota Colomb. 2002, 3, 7–118. [Google Scholar]
- Dötterl, S.; Vereecken, N. The chemical ecology and evolution of bee–flower interactions: A review and perspectivesThe present review is one in the special series of reviews on animal–plant interactions. Can. J. Zool. 2010, 88, 668–697. [Google Scholar] [CrossRef]
- Dobson, H.E.M. The ecology and evolution of pollen odors. Plant Syst. Evol. 2000, 222, 63–87. [Google Scholar] [CrossRef]
- Raguso, R.A. Why do flowers smell?—The chemical ecology of fragrance-driven pollination. In Advances in Insect Chemical Ecology; Cardé, R.T., Millar, J.G., Eds.; Cambridge University Press: Cambridge, UK, 2004; pp. 151–178. [Google Scholar]
- De Moraes, C.M.; Mescher, M.C.; Tumlinson, J.H. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nat. Cell Biol. 2001, 410, 577–580. [Google Scholar] [CrossRef]
- Chen, W.; Viljoen, A. Geraniol—A review of a commercially important fragrance material. S. Afr. J. Bot. 2010, 76, 643–651. [Google Scholar] [CrossRef] [Green Version]
- Yoon, C.; Moon, S.-R.; Jeong, J.-W.; Shin, Y.-H.; Cho, S.-R.; Ahn, K.-S.; Yang, J.-O.; Kim, G.-H. Repellency of lavender oil and linalool against spot clothing wax cicada, Lycorma delicatula (Hemiptera: Fulgoridae) and their electrophysiological responses. J. Asia Pac. Èntomol. 2011, 14, 411–416. [Google Scholar] [CrossRef]
- Rudinsky, J.A.; Novak, V.; Svihra, P. Attraction of the Bark Beetle Ips typographus L. to Terpenes and a Male-Produced Pheromone 1. Z. Angew. Entomol. 2009, 67, 179–188. [Google Scholar] [CrossRef]
- Sfara, V.; Zerba, E.N.; Alzogaray, R.A. Fumigant insecticidal activity and repellent effect of five essential oils and seven monoterpenes on first-instar nymphs of Rhodnius prolixus. J. Med. Èntomol. 2009, 46, 511–515. [Google Scholar] [CrossRef]
- Farré-Armengol, G.; Filella, I.; Llusià, J.; Peñuelas, J. β-Ocimene, a Key Floral and Foliar Volatile Involved in Multiple Interactions between Plants and Other Organisms. Molecules 2017, 22, 1148. [Google Scholar] [CrossRef] [Green Version]
- Chehab, E.; Kaspi, R.; Savchenko, T.; Dehesh, K. Hexenyl acetate mediates indirect plant defense responses. Proc. ANAS (Biol. Sci.) 2010, 65, 145–151. [Google Scholar]
- De Lira, M.H.P.; Júnior, F.P.D.A.; Moraes, G.F.Q.; Macena, G.D.S.; Pereira, F.D.O.; Lima, I.O. Antimicrobial activity of geraniol: An integrative review. J. Essent. Oil Res. 2020, 32, 187–197. [Google Scholar] [CrossRef]
- Suppakul, P.; Miltz, J.; Sonneveld, A.K.; Bigger, S.W. Antimicrobial Properties of Basil and Its Possible Application in Food Packaging. J. Agric. Food Chem. 2003, 51, 3197–3207. [Google Scholar] [CrossRef] [PubMed]
- Hendry, E.R.; Worthington, A.; Conway, B.; Lambert, P.A. Antimicrobial efficacy of eucalyptus oil and 1,8-cineole alone and in combination with chlorhexidine digluconate against microorganisms grown in planktonic and biofilm cultures. J. Antimicrob. Chemother. 2009, 64, 1219–1225. [Google Scholar] [CrossRef] [PubMed]
- Breitkopf, H.; Onstein, R.E.; Cafasso, D.; Schlüter, P.M.; Cozzolino, S. Multiple shifts to different pollinators fuelled rapid diversification in sexually deceptive Ophrys orchids. New Phytol. 2015, 207, 377–389. [Google Scholar] [CrossRef]
- Peakall, R.; Ebert, D.; Poldy, J.; Barrow, R.A.; Francke, W.; Bower, C.C.; Schiestl, F.P. Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: Implications for pollinator-driven speciation. New Phytol. 2010, 188, 437–450. [Google Scholar] [CrossRef]
- Waelti, M.O.; Muhlemann, J.K.; Widmer, A.; Schiestl, F.P. Floral odour and reproductive isolation in two species of Silene. J. Evol. Biol. 2007, 21, 111–121. [Google Scholar] [CrossRef]
- Larue, A.C.; Raguso, R.A.; Junker, R.R. Experimental manipulation of floral scent bouquets restructures flower–visitor interactions in the field. J. Anim. Ecol. 2016, 85, 396–408. [Google Scholar] [CrossRef]
- Schlindwein, C.; Westerkamp, C.; Carvalho, A.T.; Milet-Pinheiro, P. Visual signalling of nectar-offering flowers and specific morphological traits favour robust bee pollinators in the mass-flowering tree Handroanthus impetiginosus (Bignoniaceae). Bot. J. Linn. Soc. 2014, 176, 396–407. [Google Scholar] [CrossRef] [Green Version]
- Raguso, R.A.; Levin, R.A.; Foose, S.E.; Holmberg, M.W.; McDade, L.A. Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana. Phytochemistry 2003, 63, 265–284. [Google Scholar] [CrossRef]
- Burger, H.; Ayasse, M.; Häberlein, C.; Schulz, S.; Dötterl, S. Echium and Pontechium specific floral cues for host–plant recognition by the oligolectic bee Hoplitis adunca. S. Afr. J. Bot. 2010, 76, 788–795. [Google Scholar] [CrossRef] [Green Version]
- Prieto-Benítez, S.; Dötterl, S.; Giménez-Benavides, L. Diel Variation in Flower Scent Reveals Poor Consistency of Diurnal and Nocturnal Pollination Syndromes in Sileneae. J. Chem. Ecol. 2015, 41, 1095–1104. [Google Scholar] [CrossRef] [PubMed]
- Stokl, J.; Paulus, H.; Dafni, A.; Schulz, C.; Francke, W.; Ayasse, M. Pollinator attracting odour signals in sexually deceptive orchids of the Ophrys fusca group. Plant Syst. Evol. 2005, 254, 105–120. [Google Scholar] [CrossRef]
- Ackerman, J.D.; Cuevas, A.A.; Hof, D. Are deception-pollinated species more variable than those offering a reward? Plant Syst. Evol. 2011, 293, 91–99. [Google Scholar] [CrossRef]
- Ashman, T.-L. Sniffing out patterns of sexual dimorphism in floral scent. Funct. Ecol. 2009, 23, 852–862. [Google Scholar] [CrossRef]
- Arenas, A.; Farina, W. Learned olfactory cues affect pollen-foraging preferences in honeybees, Apis mellifera. Anim. Behav. 2012, 83, 1023–1033. [Google Scholar] [CrossRef]
- Wright, G.A.; Schiestl, F.P. The evolution of floral scent: The influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Funct. Ecol. 2009, 23, 841–851. [Google Scholar] [CrossRef] [Green Version]
- Rieseberg, L.H.; Willis, J.H. Plant Speciation. Science 2007, 317, 910–914. [Google Scholar] [CrossRef]
- Schiestl, F.P.; Schlüter, P.M. Floral Isolation, Specialized Pollination, and Pollinator Behavior in Orchids. Annu. Rev. Èntomol. 2009, 54, 425–446. [Google Scholar] [CrossRef] [Green Version]
- Milet-Pinheiro, P.; Ayasse, M.; Dobson, H.E.M.; Schlindwein, C.; Francke, W.; Dötterl, S. The Chemical Basis of Host-Plant Recognition in a Specialized Bee Pollinator. J. Chem. Ecol. 2013, 39, 1347–1360. [Google Scholar] [CrossRef] [PubMed]
- Rosenbauer, A. Campanulaceae. In Die Farn-und Blütenpflanzen Baden-Württembergs. Band 5: Spezieller Teil. (Spermatophyta, Unterklasse Asteridae) Buddlejaceae bis Caprifoliaceae; Sebald, O., Seybold, S., Philippi, G., Wörz, A., Eds.; Verlag Eugen Ulmer: Stuttgart, Germany, 1996; pp. 417–449. [Google Scholar]
- Inoue, K.; Amano, M. Evolution of Campanula punctata Lam. in the Izu Islands: Changes of Pollinators and Evolution of Breeding Systems. Plant Species Biol. 1986, 1, 89–97. [Google Scholar] [CrossRef]
- Chittka, L. The colour hexagon: A chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J. Comp. Physiol. A 1992, 170, 533–543. [Google Scholar] [CrossRef]
- Chittka, L.; Kevan, P.G. Flower colour as advertisement. In Practical Pollination Biology; Dafni, A., Kevan, P.G., Husband, B.C., Eds.; Enviroquest Ltd.: Cambridge, UK, 2005; pp. 157–196. [Google Scholar]
- Chittka, L.; Shmida, A.; Troje, N.; Menzel, R. Ultraviolet as a component of flower reflections, and the colour perception of hymenoptera. Vis. Res. 1994, 34, 1489–1508. [Google Scholar] [CrossRef]
- Dyer, A.G.; Chittka, L. Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 2004, 91, 224–227. [Google Scholar] [CrossRef] [PubMed]
- Dotterl, S.; Jurgens, A. Spatial fragrance patterns in flowers of Silene latifolia: Lilac compounds as olfactory nectar guides? Plant Syst. Evol. 2005, 255, 99–109. [Google Scholar] [CrossRef]
- Adams, R.P. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry, 4th ed.; Allured Publishing Corporation: Carol Stream, IL, USA, 2007; p. 804. [Google Scholar]
- Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef] [Green Version]
- Castresana, J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Mol. Biol. Evol. 2000, 17, 540–552. [Google Scholar] [CrossRef] [Green Version]
- Talavera, G.; Castresana, J. Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments. Syst. Biol. 2007, 56, 564–577. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatic 2006, 22, 2688–2690. [Google Scholar] [CrossRef] [PubMed]
- Huelsenbeck, J.P.; Ronquist, F.; Nielsen, R.; Bollback, J.P. Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology. Science 2001, 294, 2310–2314. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ronquist, F.; Huelsenbeck, J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatic 2003, 19, 1572–1574. [Google Scholar] [CrossRef] [Green Version]
- Posada, D. jModelTest: Phylogenetic Model Averaging. Mol. Biol. Evol. 2008, 25, 1253–1256. [Google Scholar] [CrossRef] [PubMed]
- Millanes, A.M.; Truong, C.; Westberg, M.; Diederich, P.; Wedin, M. Host Switching Promotes Diversity in Host-Specialized Mycoparasitic Fungi: Uncoupled Evolution in Thebiatoropsis-Usneasystem. Evolution 2014, 68, 1576–1593. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drummond, A.J.; Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7, 214. [Google Scholar] [CrossRef] [Green Version]
- Blomberg, S.P.; Garland, T. Tempo and mode in evolution: Phylogenetic inertia, adaptation and comparative methods. J. Evol. Biol. 2002, 15, 899–910. [Google Scholar] [CrossRef]
- Jombart, T.; Pavoine, S.; Devillard, S.; Pontier, D. Putting phylogeny into the analysis of biological traits: A methodological approach. J. Theor. Biol. 2010, 264, 693–701. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dray, S.; Jombart, T. Adephylo: Exploratory analyses for the phylogenetic comparative method. Bioinformatics 2008, 26, 1907–1909. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018. [Google Scholar]
- Abouheif, E. A method for testing the assumption of phylogenetic independence in comparative data. Evol. Ecol. Res. 1999, 1, 895–909. [Google Scholar]
- Pavoine, S.; Ollier, S.; Pontier, D.; Chessel, D. Testing for phylogenetic signal in phenotypic traits: New matrices of phylogenetic proximities. Theor. Popul. Biol. 2008, 73, 79–91. [Google Scholar] [CrossRef] [PubMed]
- Münkemüller, T.; Lavergne, S.; Bzeznik, B.; Dray, S.; Jombart, T.; Schiffers, K.; Thuiller, W. How to measure and test phylogenetic signal. Methods Ecol. Evol. 2012, 3, 743–756. [Google Scholar] [CrossRef]
- Adams, D.C. A Generalized K Statistic for Estimating Phylogenetic Signal from Shape and Other High-Dimensional Multivariate Data. Syst. Biol. 2014, 63, 685–697. [Google Scholar] [CrossRef] [PubMed]
- Harmon, L.J.; Weir, J.T.; Brock, C.D.; Glor, R.; Challenger, W. GEIGER: Investigating evolutionary radiations. Bioinformatic 2007, 24, 129–131. [Google Scholar] [CrossRef] [Green Version]
Campanula Species | Native Occurrence | Color Analyses | Scent Analyses (No. of Samples; No of Individuals; Total No. of Flowers) | GenBank Accession Number (petD/trnL–F/ITS) |
---|---|---|---|---|
C. glomerata L. | Eurasia (A) | Yes * | Yes * (5; 15; 235) | JX914747/HQ704671/HQ704552 |
C. lactiflora M. Bieb | Turkey and Caucasus (B) | Yes * | Yes * (5; 10; 300) | JX915131/FJ589212/- |
C. latifolia L. | Eurasia (A) | Yes | Yes (6; 12; 139) | JX914791/EF088732/- |
C. medium L. | South Europe (B) | Yes | Yes (5; 10; 63) | FN397024/EF088738/HQ823432 |
C. moravica (Spitzn.) Kovanda | Europe | Yes | No | -/EF088740/- |
C. patula L. | Europe (A) | Yes | No | JX914974/EF213148/FM212739 |
C. persicifolia L. | Europe (A) | Yes * | Yes * (12; 12; 669) | JX915226/EF088743/DQ304590 |
C. punctata Lam. | Asia (C) | Yes | Yes (2; 6; 24) | JX915031/EF088753/HQ704550 |
C. rapunculoides L. | Eurasia (A) | Yes * | Yes * (6; 18; 451) | JX915191/EF088757/HQ823434 |
C. rapunculus L. | Europe/North Africa (A) | Yes | Yes (6; 18; 1049) | JX914708/EF088758/FM212738 |
C. rotundifolia L. | Circumpolar (A) | Yes * | Yes * (7; 18; 418) | JX915164/EF088759/DQ304615 |
C. scheuchzeri Vill. | Europe (A) | Yes | No | JX915162/EF088762/DQ304614 |
C. thyrsoides L. | Europe (D) | Yes | Yes (8; 16; 154) | FN397046/KJ512699/DQ304575 |
C. trachelium L. | Eurasia (A) | Yes * | Yes ** (6; 18; 379) | JX914678/EF088774/DQ304572 |
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Milet-Pinheiro, P.; Santos, P.S.C.; Prieto-Benítez, S.; Ayasse, M.; Dötterl, S. Differential Evolutionary History in Visual and Olfactory Floral Cues of the Bee-Pollinated Genus Campanula (Campanulaceae). Plants 2021, 10, 1356. https://doi.org/10.3390/plants10071356
Milet-Pinheiro P, Santos PSC, Prieto-Benítez S, Ayasse M, Dötterl S. Differential Evolutionary History in Visual and Olfactory Floral Cues of the Bee-Pollinated Genus Campanula (Campanulaceae). Plants. 2021; 10(7):1356. https://doi.org/10.3390/plants10071356
Chicago/Turabian StyleMilet-Pinheiro, Paulo, Pablo Sandro Carvalho Santos, Samuel Prieto-Benítez, Manfred Ayasse, and Stefan Dötterl. 2021. "Differential Evolutionary History in Visual and Olfactory Floral Cues of the Bee-Pollinated Genus Campanula (Campanulaceae)" Plants 10, no. 7: 1356. https://doi.org/10.3390/plants10071356