Staminal features in Barnadesioideae (Asteraceae): description, evolution, and function

SVOMA E.; MAYER V.; STUESSY T. F.; URTUBEY E. AUTOR CORRESPONSAL

BOTANICAL JOURNAL OF THE LINNEAN SOCIETY

WILEY-BLACKWELL PUBLISHING, INC

Lugar: Londres; Año: 2019 vol. 192 p. 474 - 497

0024-4074

Received 19 February 2019; revised 26 July 2019; accepted for publication October 2019_________________________________________________________________________________________Morphological features of the heads (capitula) of Asteraceae have been used extensively in classification of the family at different levels of the taxonomic hierarchy. Among the various characters, features of stamens have been employed to determine relationships from specific to tribal levels, and these include size, shape, color, cell size and shape of the thecae, downward extensions from the thecae (spurs or tails), the apex and base of the connective between the thecae, the antheropodium that joins the connective to the filament, and the filament itself. We investigate variation in these staminal features in 88 species of ten genera of Barnadesioideae (Asteraceae), which is the cladistic sister group to the rest of the family and representing the basal complex. A new morphological categorization of antheropodia and anther bases is presented, features which show the widest ranges of variation within the subfamily. Other characters, such as apices of the connectives and fusion of filaments are less variable. Six staminal characters are optimized over a molecular phylogeny of Barnadesioideae. Putative plesiomorphies for the ancestor of the subfamily are hypothesized to be entire apices of the connectives, antheropodia shorter than these appendages, and filaments free and glabrous. The ancestral conditions for pollen sac extension and for attachment of anthers on the corolla tube are equivocal. Hypotheses are offered on the possible adaptive function of staminal features, such that antheropodia seem significant in structural support of the thecal tube, and spurs and tails may function in protection of the basal portion of the thecae from insect probing.KEYWORDS: adaptation ? androecium ? anthers ? character evolution ? Compositae. *Corresponding author: E-mail: eurtubey@darwin.edu.ar_____________________________________________________________________INTRODUCTIONNearly all classifications within flowering plants over the past three centuries have been based fundamentally on morphological characters selected from the phenotype. In recent decades, data from the genotype, mostly nucleotide sequences, have added much to our understanding of phylogenetic history and classification among angiosperms. Usually these insights have confirmed patterns of similarities and differences that have been observed from morphology, but in some instances new hypotheses of classification have been suggested (Scrophulariaceae Juss. is a good example; Olmstead et al, 2001; Albach et al., 2005; Oxelman et al., 2005). It is important that investigations of both morphological features and DNA sequences continue to be studied in detail, because they both offer tests of existing classifications based on previously available data. Both also are significant for the process of evolution: natural selection acts primarily on the phenotype, but it is the genotype that is responsible for fixing variation for transferal to subsequent generations.A wealth of morphological features in the large family Asteraceae Bercht. & J. Presl. has been used historically for classification at different levels of the taxonomic hierarchy (Cassini, 1829; Lessing, 1832; Bentham, 1873a; Small, 1917; Cronquist, 1955). In addition to features from leaves, stems, and roots, the characteristic flowering head (capitulum) of the family harbors numerous morphological characters that have long been selected to aid in constructing classifications. The number, size, and reproductive structures of florets, plus associated receptacular bracts within the head (paleae) and those surrounding it (phyllaries), combine to provide many features of potential value for understanding systematic and evolutionary relationships (e.g., Funk et al., 2009). One set of morphological features that has been used frequently for classification within Asteraceae derives from the stamens (e.g., Bentham, 1873b; Cronquist 1955, 1977; Bremer, 1994a). Consisting of anthers and filaments, these structures harbor considerable variation in the size, shape, color, cell size and shape of the thecae (pollen producing sacs), downward extensions from the thecae (spurs or tails), the apex and base of the connective between the thecae, the antheropodium that joins the connective to the filament, and the filament itself.Because of the complexity of staminal features within Asteraceae, it is not only important to document patterns of variation within different taxonomic groups but also to attempt to understand evolutionary modifications over time. This can best be accomplished by examining structural conditions and character state optimizations in context of phylogenetic hypotheses (trees), now most reliably based on nucleotide data either from the nucleus or chloroplast (or both). Many hundreds of phylogenetic trees have been formulated for different groups within Asteraceae, including metatrees involving the entire family (Funk et al., 2005; Funk et al., 2009; Mandel et al., 2015, 2017).Armed with a good understanding of morphological variation within any group, and also in possession of well-resolved and statistically supported phylogenetic trees, one is then in a position to examine patterns for speculation on possible adaptive or functional roles of these structures. There have been cautions regarding over-interpretion of functions when no experiments have been done to test adaptational hypotheses (e.g., Gould & Lewontin, 1979), but other workers have supported the search for adaptations when done carefully (e.g., Mayr, 1983; Rose & Lauder, 1996). It is also important to distinguish between adaptive responses and phylogenetic inertia within specific groups (Hansen & Orzack, 2005). The challenge is to creatively interpret plant structures in a phylogenetic and ecological context and use this background to critically establish working hypotheses for adaptive value of morphological features (Frumhoff & Reeve, 1994). This can serve as a stimulus for tests to determine fitness of specific characters (e.g., Conner & Sterling, 1995; Dudley, 1996).Most previous hypotheses of adaptive value of morphological features within Asteraceae have centered on fruiting heads or isolated fruits (achenes or cypselae; Wagenitz, 1976). Workers have speculated on functional aspects of the entire flowering head or capitulum (Zohary, 1950; Leppik, 1960, 1970, 1977; Burtt, 1961, 1977; Zhang et al., 2018) or of individual fruits, especially on the value of the pappus (Burrows, 1973, 1975; Sheldon & Borrows, 1973; Andersen, 1993; Stuessy & Garver, 1996; Greene & Quesada, 2011) and other associated structures (Venable & Levin, 1983). Other investigations have examined the number of fruits produced per head (Levin & Turner, 1977), the architecture of fruits within the capitulum (Vogel, 1979; Ridley, 1982a, b), and receptacular bracts (paleae; Stuessy & Spooner, 1988). Occasionally tests have been conducted to determine fitness, such as with neuter ray florets (Stuessy et al., 1986; Nielsen et al., 2002). An appropriate group of Asteraceae in which to understand the evolution and function of staminal features is subfamily Barnadesioideae K.Bremer & R.K.Jansen, an ancient group cladistically sister to the rest of the family (Jansen & Palmer, 1987). Molecular clock estimates suggest that this group may have originated in Late Cretaceous, some 83-50 million years ago (Panero et al., 2014; Panero & Crozier, 2016; Mandel et al., 2019), and fossil evidence also supports such a long evolutionary history for the family (Katinas et al., 2007; Barreda et al., 2010, 2012, 2015). Barnadesioideae contain ten genera and more than 90 species and reflect much morphological diversity in vegetative and floral features, including staminal characters (Stuessy et al., 2009; Ferreira et al., 2019). Understanding the variety of staminal features and their evolution within the subtribe should allow insights to the early evolution of such structures within the entire family and also to suggest hypotheses for their function as evolution proceeded in the group.Different publications at generic and infrageneric levels within Barnadesioideae have provided preliminary information about diversity of structure of stamens and possible taxonomic implications. Cabrera (1959: 34) used the shape of apical connective appendices as one of two characters for diagnosing subgenera of Dasyphyllum Kunth: obtuse or slightly emarginate for subg. Archidasyphyllum Cabrera (now genus Archidasyphyllum (D.Don) P.L.Ferreira, Saavedra & Groppo) and bifid for subg. Dasyphyllum (now genus Dasyphyllum). In the same revision, he illustrated the stamens of some species of Dasyphyllum, Fulcaldea laurifolia (Bonpl.) Poir., Doniophyton anomalum (D.Don) Kurtz, and Barnadesia odorata Griseb., in which differences in basal appendages of the anthers can be distinguished among genera. In Chuquiraga Juss., long, sagittate anthers and acute to rounded apices of the connectives are found in the genus (Ezcurra, 1985: 229). Stuessy & Sagástegui (1993: 13) treated Arnaldoa Cabrera (at that time two species), in which one difference between species is the pubescence on filaments, densely villous in Arnaldoa macbrideana Ferreyra but glabrous in A. weberbaueri (Muschl.) Ferreyra. More recently, a new species of Arnaldoa has been described by Ulloa et al. (2002), A. argentea C. Ulloa, P. Jørg. & M.O. Dillon, which also has densely villous filaments. Pesacreta & Stuessy (1996) examined the antheropodial epidermis for 20 species of Barnadesioideae. They found that in most species autofluorescent cell walls were evenly thickened. In several species of Barnadesia Mutis, however, some had spiral or irregular thickenings, hypothesized as a possible adaptation for increased strength with longer filaments and anthers as part of a hummingbird pollination syndrome. In the genus Doniophyton Wedd., connectival appendages serve to differentiate Doniophyton anomalum and D. weddellii Katinas & Stuessy, the apex being caudate versus acute (rarely apiculate), respectively (Katinas & Stuessy 1997: 38). Urtubey (1999), in her revision of Barnadesia, analyzed the base of the anther, filaments, and attachment on the corolla for all species. She classified the anthers as being adnate to the filament or shortly sagittate with filaments free or fused, and inserted at the base of the corolla, on the middle part, at the throat, or between the middle part and throat. Urtubey & Stuessy (2001) used three staminal characters (apex of the connectives, filament fusion, and filament attachment) in their morphological phylogenetic hypotheses. They analysed the evolution of two characters, bifid apices of the connectives as synapomorphies for Dasyphyllum subg. Dasyphyllum, and different filament attachments that appear repeatedly as parallelisms.In addition to these morphological observations and taxonomic implications, a number of phylogenetic hypotheses have been generated among taxa of Barnadesioideae. The most resolved trees based on morphological data were presented by Bremer (1994b), Stuessy et al. (1996), and Urtubey & Stuessy (2001). These morphological interpretations were followed by phylogenetic analyses based on DNA data by Gustaffson et al. (2001) using trnL intron chloroplast and nuclear ITS sequences, and most recently by Gruenstaeudl et al. (2009) from ITS and ten chloroplast sequences plus 11 morphological characters. This latter study is to date the most complete hypothesis of phylogenetic relationships, summarized again in Stuessy et al. (2009). The purposes of the present investigation, therefore, are to: (1) describe variation in apices of the connectives, antheropodia, and anther bases among species and genera of subfamily Barnadesioideae; (2) present hypotheses of evolution of these characters based on character optimization on molecular phylogenetic reconstructions; and (3) speculate on functions of the staminal characters within the subfamily and by extension, the family.