Ontogeny, anatomical structure and function of lobed stems in the evolution of the climbing growth form in Malvaceae (Byttneria Loefl.)

Abstract

Background and aims: Byttneria is one of the few climbing genera in Malvaceae. Some Byttneria are known for their lobed stems. We explore the development of these stems, how they have evolved within the group and their relevance in the evolution of the climbing growth form in Malvaceae.

Methods: We combine developmental anatomical work with phylogenetic comparative methods. We use Byttneria divaricata and B. filipes as models in the anatomical work, a review of herbarium vouchers, and the most recent phylogeny of Byttneria and allies to elucidate how these stems evolved within the clade under maximum-likelihood and Bayesian approaches. We use Pagel94 tests to analyse the correlated evolution of lobed stems and prickles.

Key results: Each lobe coincides with one of the five vascular bundles. By augmented activity of the fascicular cambium in the lobes coupled with reduced activity of the interfascicular cambium in the interlobes, secondary growth increases the lobulation already present during primary growth. Within Byttneria and allies, lobed young stems appeared at least three times, once in Ayenia and twice in the paraphyletic Byttneria. Lobed adult stems were conserved in Byttneria s.s., where lobed adult stems in combination with prickles were shown to have evolved as a climbing mechanism within the group; prickles were lost once within Byttneria s.s., in a shrubby subclade. Byttneria Clade 2 comprises climbers with twining cylindrical adult stems and no prickles, which constitutes a different climbing mechanism in the group.

Conclusions: We provide evidence of one of the few cambial variants known whose secondary body reflects the primary body vasculature and show that lobed adult stems and prickles in Byttneria could be used in the new delimitation of genera in the group. Lobed stems independently appeared in climbing Grewia, suggesting a convergence favouring the climbing growth form.

Keywords: Byttneria; Byttnerioideae; Climbing plants; Malvaceae; cambial variants; cambium differential activity; lianas; lobed stems; non-cylindrical stems; ontogeny.

Fig. 1.

Non-cylindrical stems within woody angiosperm orders (monocots not considered). Three main categories are recognized: angular, flattened and lobed stems; a single or multiple cambia may be involved in their development. To the best of our knowledge, Malvales only exhibits lobed stems in some Malvaceae genera, i.e. Byttneria, Gossypioides, Gossypium and Grewia (red arrow). Topology follows Stevens (2001 onwards), and Supplementary Data Table S1 lists in detail all the taxa used for mapping.

Fig. 2.

An overview of stem diversity within climbing Byttneria. (A, B) Regular stemmed species from Madagascar (Pace 1051 and Pace 1037) and Mexico (Acevedo-Rodríguez 16352), respectively. (A) Note their twining stems. (C, D, E) Lobed stemmed species from Mexico (Acevedo-Rodríguez 16123), Brazil (Acevedo-Rodríguez 16697) and Argentina (Pace 1159), respectively; these species have prickles and at nodes two lobes may fusion into one lobe. (C) Note species may be myrmecophytes, hence the hollow stem. (D) Young stems are lobed and prickles grow exclusively upon lobes. (E) This species may be regular in younger branches. Note that adventitious roots grow exclusively on the interlobe areas, while prickles have the opposite pattern. **B, C and D (only adult four-lobed) images by P. Acevedo-Rodríguez, added with permission of the author.

Fig. 3.

Terminology adopted for description of lobed stems. (A) Cylindrical stem (regular) during secondary growth. (B) Non-cylindrical lobed stem during secondary growth, with fascicular/lobular (dashed rectangles) areas and interfascicular/interlobular areas (solid lined rectangles). The fascicular/lobular area comprises a central area and a peripheral area (dashed lines). Blue filling corresponds to the bark (ba), which encompasses all tissues outside of the vascular cambium (vc, bold black line), namely secondary phloem, cortex and periderm, red to secondary xylem (sx) and white to the pith (pi), while yellow ovals represent protoxylem poles (pxp), indicating the location of vascular bundles during primary growth.

Fig. 4.

Ancestral character state reconstruction of (A) growth form and (B) climbing plant type within ABRM. Posterior probabilities of occurrence are expressed in pie charts on nodes. Turquoise blue filling represents non-climbing plants (tree, shrub, subshrub); magenta to purple colours represent represent climbing plants (scandent/leaning shrub, liana); and white represents the node no-occurrence probabilities from the sample of trees used in the Bayesian analyses. Climbers probably appeared twice in Byttneria only (nodes 23 and 36), but there is also considerable probability that climbers evolved once in node 35, which includes Rayleya. The climbing growth form was lost once in Byttneria s.s (node 30, top arrowhead).

Fig. 5.

Ancestral character state reconstruction of (A) young and (B) adult stem shape within ABRM. Probabilities of occurrence are expressed in pie charts on nodes. Turquoise blue filling represents regular, cylindrical stems; magenta represents non-cylindrical, lobed stems; and white represents the node no-occurrence probabilities. Young lobed stems appeared at least three times within ABRM (nodes 14, 23 and 36, arrowheads) and only within Byttneria s.s. (node 24, arrowhead) were lobed stems conserved in adult stems. A red dash indicates the location on the phylogeny where there was the transition from non-climbing to climbing plants. Red dots beside species indicate those with polymorphic adult stems.

Fig. 6.

Ancestral character state reconstruction of prickles within ABRM. Probabilities of occurrence are expressed in pie charts on nodes. Turquoise blue filling represents plants without prickles; magenta represents armed plants with prickles; and white represents the node no-occurrence probabilities. Only within Byttneria s.s. did prickles appear (node 23, bottom arrowhead) and were then lost once (node 31, top arrowhead).

Fig. 7.

Correlated ancestral character state reconstruction of adult stem shape and presence of prickles. Turquoise blue circles represent cylindrical, unarmed stems. Magenta filled circles represent lobed, armed stems. Lobed adult stems and presence of prickles are correlated (Pagel94 P < 0.05). Species indicated with a red dot are polymorphic and can have both cylindrical and lobed adult stems. Species indicated with red arrows have cylindrical adult stems and prickles (B. coriacea) or lobed adult stems with no prickles (e.g. B. jaculifolia).

Fig. 8.

The three stages in the ontogeny of Byttneria divaricata lobed stems. (A) Stage 1, stem while in primary growth. Lobed stems have this shape since primary growth and vascular bundles (marked by protoxylem poles in yellow brackets) match the central areas of each lobe. (B) Stage 2, onset of secondary growth. A single continuous vascular cambium becomes established. (C, D) Stage 3, advanced secondary growth; (C) note the pith remains lobed. f/l area = fascicular/lobular area, if/il area = interfascicular/interlobular area, fvc = fascicular vascular cambium, ifvc = interfascicular vascular cambium, ep = epidermis, cx = cortex, pxp = protoxylem pole, pi = pith, sp = secondary phloem, sx = secondary xylem. Yellow asterisks indicate peripheral fascicular/lobular areas and interfascicular/interlobular areas, and black arrowheads show remnants of lobe fusions.

Fig. 9.

Details of the ontogeny of lobed stems. (A, C–E, G–I) Byttneria divaricata; (B, F) B. filipes. (A, B) Primary growth in the fascicular/lobular (f/l) areas; note vascular bundles (indicated by protoxylem poles in yellow brackets) match the central f/l area, and less cortex is present in peripheral f/l areas and interfascicular/interlobular (i/l) areas (yellow asterisks) with respect to central f/l areas. (B) Incipient secondary growth. (C) Initial secondary growth in f/l areas; next to the pith note the protoxylem poles (yellow brackets) showing that a single vascular bundle might fragment in later stages given dilatation of the the primary xylem parenchyma. (D–F) Primary growth in if/il areas; solitary primary phloem strands (yellow brackets). (E) Close up of the phloem strands; (F) incipient secondary growth, with secondary xylem differentiation. (G–I) Mature secondary growth; secondary phloem production almost ceases within the peripheral f/l area and within if/il areas (yellow asterisks). Note in the central f/l area (dashed lines rectangles), tangential diameter of vessels is markedly greater with respect to peripheral f/l areas and if/il areas (solid lines rectangles). Greyscale diagram shows the position of D–F, H and I within a lobed stem. f/l area = fascicular/lobular area, if/il area = interfascicular/interlobular area, tr = trichome, ep = epidermis, dr = druse, cx = cortex (which includes ed = endodermis), pf = pericyclic fibres, pp = primary phloem, pps = primary phloem strands, ifvc = interfascicular vascular cambium, px = primary xylem, pxp = protoxylem poles, pi = pith, mc = mucilaginous cells, ba = bark (pd = peridermis + cx = cortex + sp = secondary phloem), sx = secondary xylem, lr = ’limiting ray’.

Fig. 10.

Prickles and adventitious roots in Byttneria filipes. (A) Prickle on an f/l area. (B) Prickles are formed by elongated cortical cells covered by an epidermal layer. (C) Root growing from a limiting ray within the if/il area. (D) Root emerging from the ray margins, displacing both secondary phloem and cortex as it breaks through the bark. Greyscale diagram shows the position of C and D within a lobed stem. f/l area = fascicular/lobular area, if/il area = interfascicular/interlobular area, tr = trichome, ep = epidermis, cx = cortex, ba = bark (pd = peridermis + cx = cortex + sp = secondary phloem), sx = secondary xylem, lr = limiting ray’, ma = meristematic activity, rc = root cap.