Variation and evolutionary transformation of some characters of the pollinarium and pistil in Epidendroideae (Orchidaceae)
Plant Systematics and Evolution
https://doi.org/10.1007/s00606-019-01575-5
ORIGINAL ARTICLE
Variation and evolutionary transformation of some characters
of the pollinarium and pistil in Epidendroideae (Orchidaceae)
Hilda R. Mosquera‑Mosquera1,3
· Rosa M. Valencia‑Barrera2
· Carmen Acedo3
Received: 24 June 2018 / Accepted: 21 March 2019
© The Author(s) 2019
Abstract
We studied the variation in the pollinarium and pistil of Epidendroideae and reconstructed the ancestral states of the characters (pollinia number, pollinium orientation, pollinium with suture, and pollinium texture). The pollinarium is complete
(formed by pollinium, caudicle, stipe, and viscidium) in Vandeae, Epidendreae, and Cymbidieae, but the caudicle is absent
in some Aeridinae and the viscidium in Laeliinae and Pleurothallidinae. Neottieae, Arethuseae, Sobralieae, Epidendreae,
and Xerorchideae included some genera having sessile pollinia. The more frequent state in the family is to have two pollinia,
followed by four, eight, and six pollinia. The pistil is unilocular, although it seems to have experienced reversals several times
within Epidendroideae because intermediate states were observed (e.g. Vanda and Angraecum). In these cases, a prolongation of the placental tissue is developed that in Huntleya and Peristeria make contact but do not fuse. Most members of the
subfamily have pistil composed of three carpels divided into six emerging valves, but only three are fertile. In Cattleya and
Sophronitis the sterile valves are much reduced and the pistil seems to have only three valves. We have generated useful and
valuable information to understand the evolution of the reproductive organs in Epidendroideae. Probably, these transformations in the pollinarium and pistil have co-evolved in tandem with pollinators to make the pollination more efficient. Our
results suggest that the common ancestor of Epidendroideae had a complete pollinarium, formed probably of four juxtaposed
granular pollinia without suture, bearing caudicle, tegular stipe and viscidium, but several early transformations occurred
during the Epidendroideae diversification.
Keywords Carpels · Epidendroideae · Evolution · Locules · Pollinarium · Pollinia
Introduction
Handling Editor: Louis P. Ronse De Craene.
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s00606-019-01575-5) contains
supplementary material, which is available to authorized users.
* Hilda R. Mosquera‑Mosquera
1
Department of Biology, Research Group Plant and Microbial
Biotechnology ‑ GEBIUT, Faculty of Sciences, University
of Tolima, PO Box 730006299, Ibagué, Colombia
2
Department of Biodiversity and Environment Management,
Botany, Research Group Aerobiology ‑ AERULE, University
of León, 24071 León, Spain
3
Department of Biodiversity and Environment Management,
Botany, Research Group Taxonomy and Biodiversity
Conservation ‑ TaCoBi, Faculty of Biological
and Environmental Sciences, University of León,
24071 León, Spain
Epidendroideae is the largest subfamily of Orchidaceae having more genera and species than all the others together. It
is characterized by its variety and diversity of forms (Kułak
et al. 2006), including several phylogenetically advanced and
morphologically derived tribes and subtribes (Chase et al.
2003, 2015). Recently, Freudenstein and Chase (2015) analysed the phylogenetic relationships in Epidendroideae and
progressive specialization and diversification including morpho-anatomical characters, habit and distribution together
with DNA sequences.
Only Epidendroideae and Orchidoideae, among the five
subfamilies of Orchidaceae, present authentic pollinia and
pollinarium (Singer et al. 2008), both subfamilies are also
the richest in the number of species and genera (Chase et al.
2003), and important contributions have been made to their
phylogenies (for example, Inda et al. 2010, 2012; Chase et al.
2015). Some traits of the pollinarium of Epidendroideae
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H. R. Mosquera-Mosquera et al.
and Orchidoideae have been previously studied (Schill and
Pfeiffer 1977; Dressler 1981, 1993; Rasmussen 1982; Blackman and Yeung 1983; Burns-Balogh and Funk 1986; Yeung
and Law 1987; Seidenfaden and Wood 1992; Freudenstein
1994; Freudenstein and Rasmussen 1996, 1997; Claessens
and Kleynen 1998; Johnson and Edwards 2000; Szlachetko
and Rutkowski 2000; Freudenstein et al. 2002; Szlachetko
and Margońska 2002; Szlachetko 2003; Barone Lumaga
et al. 2006; Bhanwra et al. 2006; Hidayat et al. 2006; Szlachetko et al. 2006; Rothacker 2007; Singer et al. 2008; Nieto
and Damon 2008; Chase 2009; Chase et al. 2009; Szlachetko
and Mytnik-Ejsmont 2009; Damon and Nieto 2012; Szlachetko et al. 2012; Pedersen et al. 2013; Freudenstein and
Chase 2015; Freudenstein et al. 2017). However, there is
still little information about the states of each character
and the evolutionary pathways related to the pollinarium of
the Epidendroideae, which is probably the subfamily having greater variability in this structure. Therefore, here we
improve the pollinia description, by studying details of the
accessory structures because most of the available descriptions in the literature available are oversimplified or lack
this information.
The pollinaria are a key innovation in the evolutionary history of Orchidaceae and probably contribute to the
diversification of this important family. Strategies such as
the compaction grades of pollen grains and the presence of
accessory structures (caudicle, stipe, and viscidium) provide easier transport by pollinators (Johnson and Edwards
2000). The number of pollinaria in the flower of Orchidaceae
depends on the number of viscidia and of stalks to which
the pollinia are attached (Szlachetko and Rutkowski 2000).
There is an even number of pollinia per anther that varies
from two to eight, being usually uniform within a genus
and probably also within the subtribes and tribes (Freudenstein and Rasmussen 1996). However, there are exceptions:
In Brachionidium the number of pollinia varies from six
to eight (Stenzel 2000; Becerra 2005). With respect to the
number of pollinia, several interpretations have been made.
Dressler (1993) inferred a possible pattern of reduction from
eight, six, four to two pollinia, being the most advanced
state. However, Freudenstein and Rasmussen (1996) considered that four pollinia are a plesiomorphic condition in
orchids, two pollinia are the result of the merger of the four,
and the eight pollinia may be caused by the transverse or
longitudinal division of the pollen sacs.
The texture of Epidendroideae pollinia varies from granular, sectile to compact. This last type represents the greatest
degree of cohesion of pollen and is deposited in full within
the stigma. The compact and sectile pollinia are entire or
have a longitudinal, dorsi-ventral or lateral suture or groove
(Rasmussen 1982; Freudenstein and Rasmussen 1996, 1997;
Johnson and Edwards 2000; Chase 2009). On th (...truncated)
