Hybrid floral scent novelty drives pollinator shift in sexually deceptive orchids.
BACKGROUND
Sexually deceptive orchids of the genus Ophrys attract their pollinators, male insects, on a highly specific basis through the emission of odour blends that mimic the female sex pheromone of the targeted species. In this study, we have investigated a contact site between Ophrys arachnitiformis and O. lupercalis, two sympatric orchid species that are usually reproductively isolated via the exploitation of different pollinator "niches", but occasionally hybridise despite their apparent combination of ethological and mechanical isolation barriers. In particular, we have investigated the extent to which these Ophrys hybrids generate "emergent" combinations (i.e. novel and unpredictable from the parents' phenotypes) of floral traits, and how these phenotypic novelties, particularly the odour blends emitted by the flower, could facilitate the invasion of a novel pollinator "niche" and induce the rapid formation of reproductive isolation, a prerequisite for adaptive evolutionary divergence.


RESULTS
Our chemical analyses of floral scents show that the Ophrys F1 hybrids investigated here produce more compounds, significantly different ratios (% of odour compounds in the total blend), as well as new compounds in their floral odour compared to their progenitors. When tested for their attractiveness to the pollinator of each parent orchid species, we found that floral scent extracts of the hybrids triggered less inspecting flights and contacts by the male bees with the scented dummy than those of the parental orchid species. However, a series of additional behavioural bioassays revealed that the novel floral scent of the hybrids was significantly more attractive than either of the two parents to a pollinator species not initially involved in the pollination of any of the parent Ophrys species.


CONCLUSIONS
Collectively, our results illustrate that the process of hybridisation can lead to the generation of evolutionary novelties, and that novel combinations of floral traits can drive pollinator shifts and rapid reproductive isolation in highly specific plant-pollinator interactions.
Vereecken
Nicolas J
NJ
Evolutionary Biology & Ecology, Free University of Brussels/Université Libre de Bruxelles, B-1050 Brussels, Belgium. nicolas.vereecken@ulb.ac.be
Cozzolino
Salvatore
S
Schiestl
Florian P
FP
D000818:Animals; D005260:Female; D006824:Hybridization, Genetic; D006927:Hymenoptera / Q000145:classification / Q000502:physiology*; D008297:Male; D029595:Orchidaceae / Q000502:physiology*; D054817:Pollination; D012724:Sex Attractants; D012726:Sexual Behavior, Animal; D013045:Species Specificity
D012724:Sex Attractants
Proc Natl Acad Sci U S A. 1996 May 14;93(10):5090-3
11607681
Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):3-10
11607448
Proc Biol Sci. 2003 Mar 7;270(1514):517-22
12641907
Proc Biol Sci. 2005 Jun 22;272(1569):1271-8
16024392
Ann Bot. 2009 Aug;104(3):497-506
19001428
Evolution. 2005 Jul;59(7):1449-63
16153031
J Hered. 2005 May-Jun;96(3):241-52
15618301
Am Nat. 2002 May;159(5):438-50
18707428
J Chem Ecol. 2005 Aug;31(8):1765-87
16222807
Science. 2009 Feb 6;323(5915):737-41
19197053
Evolution. 2007 Nov;61(11):2623-42
17908246
Science. 2003 Aug 29;301(5637):1211-6
12907807
Annu Rev Entomol. 2009;54:425-46
19067636
Bioinformatics. 2012 Oct 1;28(19):2537-9
22820204
Nucleic Acids Res. 1995 Nov 11;23(21):4407-14
7501463
Trends Ecol Evol. 1992 Aug;7(8):255-9
21236024
Heredity (Edinb). 2000 Apr;84 ( Pt 4):441-51
10849068
Nature. 2003 Nov 13;426(6963):176-8
14614505
J Hered. 2000 May-Jun;91(3):242-6
10833052
Evolution. 2000 Dec;54(6):1995-2006
11209776
Am J Bot. 2008 Apr;95(4):472-81
21632372
Br Foreign Med Chir Rev. 1862 Oct;30(60):312-318
30163543
Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8089-91
7667249
Proc Natl Acad Sci U S A. 2008 May 27;105(21):7484-8
18508972
Ann Bot. 2009 Nov;104(6):1077-84
19692390
J Hered. 2003 Nov-Dec;94(6):442-8
14691310
Mol Ecol. 2001 Mar;10(3):551-68
11298968
Philos Trans R Soc Lond B Biol Sci. 2004 Oct 29;359(1450):1523-35
15519970
New Phytol. 2005 May;166(2):685-94
15819930
J Chem Ecol. 2007 Jan;33(1):199-212
17146720
Am Nat. 1997 Dec;150(6):730-43
18811333
Annu Rev Genet. 2008;42:443-61
18983261