Evolution of the staminode in a representative sample of Scrophularia and its role as nectar safeguard in three widespread species

Abstract

Approximately 30% of the genera of Scrophulariaceae s.str. have a staminode, which is the remnant of a sterile stamen. However, there are no studies of the functionality or evolutionary pattern of staminodes in that family. This paper investigates three Scrophularia species with different staminode sizes to determine if the staminode safeguards nectar from dilution by rainwater and if it influences pollinator behavior. We also study staminode evolution and ancestral state reconstruction onto a phylogeny containing 71 species and subspecies with four different staminode developmental stages: tiny, large, enormous, and absent. The results showed that large staminodes did not hinder nectar collection or modify pollinator-visiting time but acted as a barrier to reduce rainwater entry. The latter reduced the dilution of nectar, which did not occur with tiny staminodes. The phylogenetic study revealed that the ancestral state in the genus corresponds with the presence of a large staminode vs. the tiny and enormous staminodes that are considered as derived. The complete disappearance of the staminode has occurred independently at least twice. Events occurred that increased or reduced the staminode size in one of the clades (Clade II), which includes species of sect. Caninae; most of these events occurred during the Pleistocene (0.6-2.7 Ma).

The Biomechanical Screening Game between Visitor Power and Staminode Operative Strength of Delphinium caeruleum (Ranunculaceae)

“…Staminodes are common floral structures that help both to attract visitors and to protect the sex organs [20,29], but our observations found that visitors of D. caeruleum contacted the anthers and stigmatic surface by opening the door-like structure of the staminodes. A considerable number of plant species are known, e.g., members of genera such as Salvia, Cornus, Calceolaria, etc., where flowers have movable parts, which are obstacles that must be actively moved by a visitor to access the flower rewards and achieve pollination [12,26].…”

“…Recent studies have found that staminodes form physical barrier structures in some plant species and could play several different functional roles. The staminode of the three Scrophularia species (S. lyrata, S. scorodonia, and S. canina) flowers, for example, is found to protect the nectar from dilution by rainwater [20]. Such staminodes may also perform the function of insect screening.…”

The tribe Scrophularieae (Scrophulariaceae): A Review of Phylogenetic Studies

“…During seven years of molecular phylogenetic analyses of Scrophularieae taxa, from the beginning of 2011 to the end of 2017, 12 studies have been published, which cover three genera of the tribe Scrophularieae and address question at generic level (Scheunert & Heubl 2011, 2014, Attar et al 2011, Navarro-Pérez et al 2013, Ghahremaninejad et al 2015, Rodríguez-Riaño et al 2015, Sotoodeh 2015, Valtueña et al 2016, Chen et al 2017). All studies have used only sequence data as the marker in assessing phylogenetic relationships in the Scrophularieae.…”

“…When compared with other single copy protein coding genes, nuclear rRNA genes are routinely amplified due to their small size associated to the availability of highly conserved flanking sequences and easy to detect even from small quantities of DNA because of the high copy number of the rRNA clusters. Based on these technical advantages, ribosomal genes are among the first sequences that have been extensively exploited in phylogenetic analyses of the tribe Scrophularieae (Scheunert & Heubl 2011, 2014, Attar et al 2011, Navarro-Pérez et al 2013, Ghahremaninejad et al 2015, Rodríguez-Riaño et al 2015, Sotoodeh 2015, Valtueña et al 2016, Chen et al 2017.…”

“…Evolution of the staminode was investigated in three species of Scrophularia by Rodríguez-Riaño et al (2015). They optimized all four staminode types on a phylogenetic tree from datasets of reported studies and showed that the ancestral staminode type for the genus seems to be a large staminode.…”