Apocynaceae wood evolution matches key morphological innovations

Abstract

Premise: This paper provides an overview of the wood anatomy of the dogbane family (Apocynaceae), reconstructs wood anatomical trait evolution, and links this evolution with woody growth-form transitions and floral and seed trait innovations across the family.

Methods: Over 200 published wood anatomical descriptions were revised, and original light microscopic sections were made and described for another 50 species. Changes in wood anatomical characters through time were visualized with ancestral state reconstructions. Tests for correlated evolution were performed using a combined data set of anatomical and key floral and seed traits to identify potential synnovations and traits associated with growth-form adaptations.

Results: There was a shift toward a suite of wood anatomical traits that separate the rauvolfioids and early-branching apocynoids from the core apocynoids, including an increased presence of vessel multiples, vessel dimorphism, laticifers, vascular (cambial) variants, and paratracheal axial parenchyma. The presence of this trait suite, which continues in Periplocoideae, Secamonoideae, and Asclepiadoideae, coincides with a progression of floral morphological innovations that evolved on consecutive nodes in the family, and also relates to more frequent transitions toward the climbing and herbaceous habits. In addition, a considerable shortening of vessel elements and fibers along the phylogenetic backbone of the family is correlated with a general reduction in plant size.

Conclusions: There are clear evolutionary transitions in the wood anatomy of Apocynaceae representing structural adaptations across the family that are associated with a quick succession of evolutionary changes of the floral bauplan.

Keywords: evolution; lianas; morphology; phylogenetic comparative methods; synnovations; wood anatomy.

Figure 1

Cladogram showing phylogenetic relationships within Apocynaceae and key floral and seed morphological innovations, along with information on growth form, number of species, and evolution of the pollination system. Woody species are trees, shrubs, and/or lianas, black = presence, grey = absence. (A, B) Rauvolfioid versus APSA flower. Light gray = stamens; dark gray = style head. (A) Rauvolfioid flower with stamens free from style head; (B) APSA flower with gynostegium (anthers attached to style head). (C–F) Evolution of pollen aggregation and two morphologically distinct bauplans for translators composed of style‐head secretions and pollinaria (translator + pollinia) in Periplocoideae (C, D), Secamonoideae (E) and Asclepiadoideae (F). White = adhesive; light gray = pollen; dark gray = translator. (C) Side view of a firm scoop‐like translator with sticky adhesive lining by which the pollen (aggregated into porate tetrads) adhere to the scoop and with a sticky disc (viscidium) at the base of the translator to attach the translator to the pollinator. (D) Front view of pollinarium formed of a translator with adhesive‐lined scoop onto which porate pollen tetrads (aggregated into pollinia without a pollen wall) are shed, and with viscidium at the base. (E) Pollinarium comprising a translator with four sessile pollinia composed of inaperturate tetrads without a pollinium wall, attaching to the pollinator via a clip mechanism. (F) Pollinarium comprising a clip‐type translator and two pollinia composed of single inaperturate pollen grains with a pollinium wall and attached to the clip by arms. Additional potential drivers of diversification following Bitencourt et al. (2021): 1 = dry fruit with comose seeds, 2 = climbing habit. Tribes behind grey branches = rauvolfioids, blue = apocynoids, green = Periplocoideae, yellow = Secamonoideae, and red = Asclepiadoideae. Relationships after Fishbein et al. (2018) using the plastid phylogeny under constraint of the plastome, with updated relationships of Echiteae and sister clades based on Morales et al. (2017)—except for the position of Rhabdadenieae. Number of species per taxon and specifics on woody growth form type based on Endress et al. (2019). Botanical illustrations 1, 2, A, and B made by Esmée Winkel, C–F drawn and adapted from Endress (2003). Illustrations are not to scale.

Figure 2

Overview of informative Apocynaceae wood anatomical characters based on LM sections (A–L, N) and SEM surfaces (M, O). (A) Willughbeia coriacea—cross section, mainly solitary vessels (arrow). (B) Thevetia ahouai—cross section, vessels mainly in radial multiples (arrow). (C) Gongronemopsis tenacissima—cross section, vessels in radially oriented clusters including many narrow (arrows) and few wide vessels (vessel dimorphism). (D) Minaria acerosa—tangential section, ground tissue composed of densely pitted imperforate tracheary cells (tracheids, arrow pointing right), which are difficult to distinguish from narrow vessels with simple perforations (tilted arrow pointing left) surrounding wider vessels (tilted arrow pointing right). (E) Kanahia laniflora—tangential section, ground tissue composed of fiber‐tracheids with distinctly bordered pits (arrows). (F) Cerberiopsis candelabra—tangential section, ground tissue composed of few minutely bordered libriform fibers (arrows point to pits). (G) Dyera costulata—tangential section, uni‐ (arrow pointing left), and multiseriate rays (arrow pointing right). (H) Aspidosperma oblongum—cross section, apotracheal axial parenchyma (arrow). (I) Aspidosperma album—cross section, paratracheal axial parenchyma (arrow). (J) Secamonopsis madagascariensis—tangential section, laticifer in multiseriate ray (arrow pointing left) and vasicentric tracheids (arrow pointing right). (K) Leptadenia arborea—cross section, cambial variant (arrows) leading to zones of nonlignified xylem (in blue) including fibers, parenchyma, rays, and traces of interxylary phloem cells. (L) Mandevilla rugellosa—radial section, septate libriform fibers (arrows pointing to septa). (M) Pentopetia grevei—tangential surface, prismatic crystals in ray cells (arrow). (N) Aspidosperma megalocarpon—radial section, prismatic crystals in chambered axial parenchyma cells (arrow), (O) Funastrum clausum—cross section, druses in nonlignified tissue.

Figure 3

Maximum likelihood mapping of fiber length (in µm) on the phylogram of Fishbein et al. (2018).

Figure 4

Ancestral state reconstructions with stochastic mapping using the chloroplast‐based chronogram of Fishbein et al. (2018) showing a suite of associated wood traits. Branches with less than 90% bootstrap support or indicates clades with conflicting arrangement are indicated with dashed lines (after support values in Fishbein et al., 2018). The chronogram only includes woody species for which anatomical traits were collected (all herbaceous species have been removed). Pie charts at the nodes represent prior probabilities for each state at each node. (A) Presence of paratracheal parenchyma (often in addition to apotracheal axial parenchyma). (B) Presence of dominant vessel grouping type. (C) Presence of vascular (cambia) variants. (D) Presence of vessel dimorphism. (E) Presence of laticifers in rays. (F) Woody growth‐form, important flower and seed traits A–F and 1–2 following Figure 1: A = stamens free of style head, B = gynostegium, C = scoop‐like translator with pollen in tetrads, D = scoop‐like translator with four pollinia, E = clip translator with four pollinia, F = clip translator with two pollinia, 1 = dry fruit with comose seeds, 2 = increase in climbing habit.