Spontaneous caudicle reconfiguration in Dactylorhiza fuchsii: A new self-pollination mechanism for Orchideae

Plant Systematics and Evolution https://doi.org/10.1007/s00606-019-01570-w ORIGINAL ARTICLE Spontaneous caudicle reconfiguration in Dactylorhiza fuchsii: A new self‑pollination mechanism for Orchideae Izabela Tałałaj1 · Jarosław Kotowicz2 · Emilia Brzosko1 · Beata Ostrowiecka1 · Olgierd Aleksandrowicz1 · Ada Wróblewska1 Received: 29 August 2018 / Accepted: 11 February 2019 © The Author(s) 2019 Abstract Deceptive plants represent a strategy that promotes outcrossing and protects against facilitated selfing. However, deception does not eliminate the possibility of autonomous self-pollination when pollinators are scarce or absent. Spontaneous autogamy is widespread in Orchidaceae, but the scale, mechanism, time of appearance and effectiveness remain underestimated. Using field and laboratory observations and experiments, for the first time, we documented the possibility of autonomous self-pollination in the deceptive orchid Dactylorhiza fuchsii, which might occur through the previously unspecified mechanism in the tribe Orchideae of caudicle reconfiguration. Self-pollination occurred through the pollinarium twisting to the side and downwards, which was different than caudicle bending forward on the body of pollinators. Caudicle reconfiguration was continuously distributed during anthesis and was common in the studied populations. This mechanism was independent on the flower position in the inflorescence, but was sensitive to pollinator activity. (The frequency of caudicle reconfiguration increased when more pollinaria in the inflorescence were untouched.) This process was effective (self-pollination leading to autogamous fruits and seeds) only when a full caudicle rotation occurred and the pollinium touched the stigma. However, most caudicle reconfigurations were completed before the stigma was reached, resulting in less than 1% of autogamous pollination in the studied populations. Keywords Autogamy · Caudicle bending movement · Reproductive success · Self-pollination Introduction One of the major selective forces acting on the evolution of plant breeding systems and directly related with the adaptation of floral traits is avoidance of inbreeding (Barrett 2003; Charlesworth 2006; Brys and Jacquemyn 2016). In hermaphroditic, self-incompatible plants, there are many adaptations to reduce self-pollination (Lloyd and Schoen 1992), ranging from morphological adaptations, e.g. dichogamy or herkogamy (Barrett 2002), to some functional strategies, such as deception (Jersáková et al. 2006). However, Handling Editor: Peter K. Endress. * Izabela Tałałaj 1 Institute of Biology, University of Bialystok, ul. Ciołkowskiego 1J, 15‑245 Białystok, Poland 2 Institute of Mathematics, University of Bialystok, ul. Ciołkowskiego 1M, 15‑245 Białystok, Poland pollinator availability is the primary factor limiting reproductive success in most angiosperms, and self-pollination may guarantee some reproductive assurance (Lloyd 1979, 1992). Selfing can be the exclusive breeding system or combined with cross-fertilization as part of mixed mating (Goodwillie et al. 2005; Goodwillie and Knight 2006; Johnston et al. 2009; Porcher et al. 2009). The time and the mechanism of self-pollination remain the subject of debate in many plant taxa and offer opportunities to increase our knowledge of the evolution of mating systems and floral traits (Zhang and Li 2008; Freitas and Sazima 2009; Brys et al. 2013; Bateman et al. 2015; Suetsugu 2015; Love et al. 2016; Yang et al. 2018). One of the problematic subjects is the functional approach of facultative autogamy (occurrence during a flower’s life span and contribution to breeding system), which has often been overlooked. The functional studies emphasizing the operation of facultative self-pollination mechanisms acting in autogamy demonstrate that this pollination mode usually occurs at the end of anthesis, after pollinators have failed 13 Vol.:(0123456789) I. Tałałaj et al. and after opportunities for outcrossing (Tałałaj and Brzosko 2008; Freitas and Sazima 2009; Suetsugu 2013). Therefore, delayed selfing should be favoured when pollinators are sometimes unreliable. Conversely, when self-pollination occurs during anthesis, it competes with cross-pollination (Lloyd and Schoen 1992). However, when pollinators are deficient, competing selfing may offer a selective advantage because the investment of resources in traits associated with attracting pollinators and optimizing visits is reduced, for example, floral longevity and size or nectar production (Yang et al. 2018). In reality, autogamous selfing does not fall into strict classes of floral life span and is instead continuously distributed (Goodwillie et al. 2005). The appearance and extent of autonomous selfing may differ among closely related species (Brys and Jacquemyn 2011; Kalisz et al. 2012; Yang et al. 2018), different populations of a single species and even between years within the same population (Kalisz et al. 1999; Elle et al. 2010; Brys et al. 2013; de Gusmão Lôbo and Stefenon 2018). Autonomous selfing is widespread in the Orchidaceae, and the phenomenon apparently evolved independently many times in this family (Catling 1990). Deficiency of pollinators is often documented in orchid populations (Tremblay et al. 2005), and autonomous self-pollination provides a reproductive assurance, when the frequency of pollination is unreliable. Despite obligatory autogamy, there are many studies that report cases of facultative autogamy occurring at the end of a flower’s life span (reviewed in Catling 1990; Claessens and Kleynen 2011). Some cases of facultative autogamy are accidental or even questionable. However, some of the data also document a continuous distribution of self-pollination starting from the beginning of anthesis and occurring in combination with cross-pollination, such as in Pseudorchis albida (Claessens and Kleynen 2011). Orchids display various mechanisms of self-pollination, including oversecretion of the stigma, different movements of the perianth, stigma, anther or pollinia, and numerous structural modifications (Catling 1990). One of the interesting mechanisms promoting autogamy is caudicle bending leading to a gradual reorientation of the pollinium. Most European orchids with caudicles as structural parts of the pollinaria exhibit caudicle bending on an insect body after withdrawal of the pollinarium from the flower (Claessens and Kleynen 2011), which is caused by the rapid dehydration of the part by which the caudicle is connected to the viscidium (Darwin 1877). On the one hand, caudicle bending brings the pollinia into appropriate position for touching the stigma; on the other hand, this movement occurs at different times after removal from the anther, depending on pollinator behaviour on the inflorescence. This mechanism is usually thought as prevention against selfing through geitonogamy and functions as an adaptation for outcrossing (Darwin 1877; Johnson and Edwards 2000 (...truncated)