AWA: Academic Writing at Auckland

ABSTRACT

The family Orchidaceae is one of the largest angiosperm families, and show a remarkable diversity in floral morphology and form. This article reviews the main theories put forth to explain orchid evolution and speciation. The most popular and traditional theory focuses on pollinator specialisation. Fungal specialization is a more recent and understudied theory, but is nonetheless important. Studies have focused on deception as a valuable means of understanding orchid diversity. Recent genetic studies have also proposed predisposition to diversification. Epiphytism, predominant in orchids, has been proposed as a means of explaining orchid species richness. Lastly, a new ‘drift-selection’ model has been put forth to explain the overall forces likely to act on orchids. These theories need not be mutually exclusive and each have valuable insight into the many processes likely to have affected orchid evolution and speciation.

keywords: orchid, evolution, speciation, diversity, epiphyte, pollinator, fungal

INTRODUCTION

The family Orchidaceae comprises as many as 25,000 species known to science [1]. Orchids have successfully colonised almost every habitat and show astonishing floral variation and species richness [2]. Charles Darwin was the first to realise how the variation among orchids supported and exemplified his theories of natural selection and adaptation, and orchids have been an attractive avenue for plant biologists since [3]. However, the diversity shown by orchids has so far not been explained satisfactorily by any single theory. This article attempts to review the main theories for the purpose of answering, or at least understanding, the question: why are orchids so diverse?

POLLINATOR-SPECIALISATION

Most orchids are allogamous, and require animal vectors for pollination [3]. Orchids show a very wide variety of pollination mechanisms, and are often highly specialised to a single pollinator species [2]. It has been estimated that as many as 70% of orchids rely on a single pollinator species, and only a small few are generalised to any pollinator [4]. Pollinator specificity has therefore been considered critical in illuminating orchid species richness, as a high degree of reproductive isolation from other populations can be instigated if a plant is only visited by one species [1]. However, recent theories have been turning away from this theory as the main driver of orchid diversity, citing that other plant groups which show similar pollinator interactions do not show nearly the same diversity as orchids [1], and indeed orchids that show higher specificity towards pollinators actually show less divergent karyotypes than the more generalised orchids [5]. Gravendeel et. al. (2004) show in their statistical analysis that there is no evidence that pollinator specialisation has driven orchid speciation [1]. Conversely, Schiestl and Schlüster (2009) have found a correlation between pollinator specialisation and species richness; more specialised genera are richer in species [6]. This theory is therefore still under much debate, and while the importance of pollinator specialisation is certain to have had an effect on orchid evolution, it is far from clear as to whether it can be considered the principal driver of orchid species diversity.

ORCHID-MYCORRHIZAL INTERACTIONS

Orchids lack an endosperm, and therefore all orchid species rely on symbiotic relationships with mycorrhizal fungi for the energy and nutrients their seedlings require [7,8]. Such a relationship is certain to have affected orchid evolution, given that orchids often show strong specificity for certain mycorrhizal fungi, and vice versa [8].  The geographical distribution of orchids has been shown to be affected by its interactions with this fungus [9], and orchids commonly have small, low density, hyper-dispersed populations in their species [7]. While studies on orchid-mycorrhizal symbiosis are as yet scarce, it is clear that their interactions affect orchid distribution, and therefore its ecology and ability to diversify. Further studies will likely yield more information as to the relative importance of these interactions to the question of orchid diversity.

DECEPTION

While pollination-specificity has already been discussed, the mechanisms orchids have evolved to attract pollinators have not. While the majority of orchids follow the ‘normal’ flower pattern of reward based pollination (i.e., offering some type of reward, usually in the form of nectar, to entice pollinators to visit the plant), orchids show a high occurrence of non-rewarding flowers which are pollinated by ‘deceit’ [2]. Most common are ‘food deception’ whereby the pollinator is fooled into thinking the flower will offer a food reward (often achieved through mimicry of reward-offering plants in the area), and ‘sexual deception’ whereby the flower imitates mating signals in insects, especially by manipulating its floral odour to mimic insect pheromones [2]. True sexual deception is found only in orchids [6]. The use of deception is a somewhat puzzling aspect of orchid diversity, representing a full third of the orchid species, and almost all of the plant species who are pollinated by deceit belong to the orchid family (6500 are orchids out of a total 7500 deceptive species) [2]. Orchids clearly have some sort of predisposition towards diversity in this regard, despite deception being considered a relatively unstable evolutionary state (given that pollinators are likely to leave patches of plants after being deceived and are also capable of learning avoidance of non-rewarding plants) [2, 10]. Deceptive orchids are also known to have low fruit set and to be pollinator limited. However, deceptive plants are shown to have higher levels of outcrossing (due partially to insects leaving patches once deceived) and therefore lower rates of geitonogamy and inbreeding depression [8]. Genetic diversity and seed distribution is therefore aided in orchids by the use of deception, despite the seemingly counterintuitive strategy of non-rewarding flowers. Indeed, even if selection occurs in pollinators for the avoidance of deceptive orchids, this could then prompt further diversification and specialisation towards more enticing and deceptive signals in the orchid flower, i.e. ‘antagonistic co-evolution’ [10]. Orchids that are pollinated by sexual deceit have been suggested to be examples of sympatric speciation since the pheromones often mimicked by orchids are controlled by only a few genes, and mutation of these genes could result in instant specialisation towards a new insect species attracted to the different scent [6, 11]. While the forces surrounding the evolution of deception in orchids still largely remain mysterious, it is clear that further understanding of this mechanism is important for a holistic perspective on orchid diversity. However, other theories are needed to explain the diversity shown in the other two-thirds of orchid species which are not pollinated by deceit.

MUTATIONS AND FLORAL MORPHOLOGY

Recent genetic studies of the genes involved in flower development and morphology have yielded important results for the understanding of orchid evolution and diversity. Studies of MADS-box genes have demonstrated their importance in floral developmental morphology and diversity [12]. Mondrago-Palomino et al. (2009) make an important point when they stress that so far, in theories on orchid diversity, the focus has been on the ultimate rather than proximate causes of orchid speciation and radiation. They propose the proximate cause of orchid diversification as being a genetic predisposition towards great morphological variance, as a result of mutations and duplications  in organ identity genes collectively known as class B homeotic genes [13]. These genes have allowed different kinds of petals and tepals in orchids to develop individually and independently of the others, allowing great potential for morphological variance. Mondrago-Palomino et al. (2009) describe this as ‘deconstraining’ orchid morphology; a developmental inclination towards diversity in orchid flowers in conjuction with selective forces for the adaptation to specific pollinators [13]. This theory advocates that floral specialisation has led to orchid diversity, and while this is likely true in part, Armbruster (2009) also proposes that the reverse can be true also (that high species diversity can create floral specialisation due to the higher proportion of populations living in sympatry) [14] [Fig.1].  In either case, the ‘deconstrained’ floral evolution of the orchid is likely the central proximate cause of its diversity.

EPIPHYTISM: DIVERSITY THROUGH NICHE PARTITIONING?

In the orchid family, 18,000 of the species are epiphytes, predominantly tropical. 70% of orchids live in canopies [1]. Tropical epiphytic orchids therefore comprise the majority of orchid taxonomic diversity; and subsequently the overall question of orchid diversity should logically be concentrated on what factors have contributed to the success of the orchids in the epiphytic, tropical form [7]. Gentry and Dodson (1987) first proposed that epiphytes are able to achieve higher diversity due to their restricted habitat; tropical canopies offer greater “spatial heterogeneity” and therefore opportunities for niche partitioning and exploitatation [15]. Benzing (1990) proposed similarly that the habitat of epiphytes was more fragmented and therefore conducive to allopatric speciation [16]. Gravendeel et. al. found in statistical analysis that in both orchids and non-orchids, epiphytic genera had more species richness than terrestrial genera. Twig epiphytism in particular is known to have evolved more than once in the Orchidaceae, and is associated with speciation bursts [1]. Though more research is needed due to much of our knowledge of orchids being based on studies of European orchids, epiphytism in orchids is clearly an example of taxonomic diversity resulting from radiating into a habitat with many available niches [1].

THE DRIFT-SELECTION MODEL

As noted previously, orchids commonly occur in small scattered populations [2]. Reproductive success is often highly skewed toward only a few individuals who successfully produce fruit, and dispersal of seeds is possible over vast distances [8]. Tremblay et al. (2005) therefore proposed a model based on these known facts about orchids which essentially states that genetic drift may be just as important as natural selection in the diversity of the Orchidaceae [18]. Skewed reproductive success combined with long distance dispersal and restricted gene flow is likely to have created multiple founder populations. Cozzolino argues that temperate orchids do not follow this pattern, and instead often have large populations which show great genetic variation and large amounts of gene flow [5]. However, in tropical orchids this model is more likely to be applicable, and it is worth noting again that this is the more diverse group. Indeed, Tremblay et al. note the interesting paradox that it is the low reproductive success of orchids which may account for its diversity (species with skewed reproductive success are more vulnerable to drift) [18]. The model is therefore a useful and interesting method of looking at orchid diversity in terms of total species richness rather than viewing the more common, fecund orchid species as more ‘successful.’

CONCLUSION The review above outlines the main theories for the drivers of orchid taxonomic diversity. The most popular theory, based on pollinator specialisation, is no longer thought to be enough to explain diversification across the family. Recent theories based on mycorrhizal symbiotic associations and genetic studies are providing interpretations previously missing in the study of orchid evolution, and a new focus on the unusually high rate of deception in the Orchidaceae should yield clues to orchid diversity. Lastly, aconvincing case has been made for the importance of the tropical habitat and epiphytic floral form to the diversity of orchids, and the ‘drift selection’ model proposes an interesting explanation as to why orchid diversity could be so great despite what at first seems to bethe paradoxically low reproductive success and population densities common to many orchids. These theories are all likely to have some merit in explaining orchid diversity. It is likely that some factors outlined by the theories played more of a role in some orchid cladesthan others, such as niche partitioning in the tropical epiphytic orchids, but nonetheless these theories are not mutually exclusive.

References

[1] Gravendeel et. al. 2004. Epiphytism and pollinator specialization: drivers for orchid diversity? Philosophical Transactions: Biological Sciences 359 (1450), 1523-1535

[2] Jersákova et al. 2006. Mechanisms and evolution of deceptive pollination in orchids. Biological Review 81, 219-235

[3] Tsai, W.C et al. 2008. Molecular biology of orchid flowers: with emphasis on Phalaenopsis. In Advances in Botanical Research: Volume 47 (Kader, J.C and Delseny, M. eds) pp99-145, Elsevier Ltd.

[4] Tremblay,R. 1992. Trends in the pollination ecology of the Orchidaceae: evolution and systematic. Canadian Journal of Botany 70(3), 642–650

[5] Cozzolino, S. and Widmer, A. 2005. Orchid diversity: an evolutionary consequence of deception? Trends in Ecology and Evolution 20 (8), 487-94

[6] Schiestl, F. and Schlüster, P. 2009. Floral Isolation, Specialized Pollination, and Pollinator Behaviour in Orchids. Annual Review of Entomology 54, 424-446

[7] Otero, J. and Flanagan, N. 2006. Orchid diversity: beyond deception. Trends in Ecology and Evolution 21(2): 64-5

[8] Waterman, R. and Bidartondo, M. 2008. Deception above, deception below: linking pollination and mycorrhizal biology of orchids. Journal of Experimental Botany 59 (5), 1085-1096

[9] Taylor, D. and Bruns, T. 1999. Population, habitat and genetic correlates of mycorrhizal specialization in the 'cheating' orchids Corallorhiza maculata and C. mertensiana. Molecular Ecology 8 (10), 1719-1732.

[10] Gaskett, A. 2010. Orchid pollination by sexual deception: pollinator perspectives. Biological Reviews, 1-43

[11] Schiestl, F. and Ayasse, M. 2002. Do changes in floral odor cause speciation in sexually deceptive orchids? Plant Systematics and Evolution 234, 111-119 

[12] Johansen B, Frederiksen S. 2002. Orchid flowers: evolution and molecular development. In: Developmental genetics and plant evolution (Cronk QCB, Bateman RM, Hawkins JA, eds.) London: Taylor & Francis. 206–219

[13] Mondrago-Palomino, M. and Theißen, G. 2009. Why are orchid flowers so diverse? Reduction of evolutionary constraints by paralogues of class B floral homeotic genes. Annals of Botany 104 (3), 583-594

[14] Armbruster, W. and Muchhala, N. 2009. Associations between floral specialization and species diversity: cause, effect or correlation? Evolutionary Ecology 23, 159-179

[15] Gentry, A. and Dodson, C. 1987. Diversity and Biogeography of Neotropical Vascular Epiphytes. Annals of the Missouri Botanical Garden 74 (2), 205-233

[16] Benzing, D. 1990. Vascular Epiphytes: General Biology and Related Biota. Cambridge University Press

[17] Peakall, R. 2007. Speciation in the Orchidaceae: confronting the challenges. Molecular Ecology 16, 2834-2837

[18] Tremblay, R et. al. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnaean Society 84, 1-54.