Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought

Abstract

Background One of the major trends in angiosperm evolution was the shift from woody to herbaceous habit. However, reversals known as derived woodiness have also been reported in numerous, distantly related clades. Among theories evoked to explain the factors promoting the evolution of derived woodiness are moderate climate theory and cavitation theory. The first assumes that woody habit evolves in response to mild climate allowing for prolonged life span, which in turn leads to bigger and woodier bodies. The second sees woodiness as a result of natural selection for higher cavitation resistance in seasonally dry environments. Here, we compare climatic niches of woody and herbaceous, mostly southern African, umbellifers from the Lefebvrea clade to assess whether woody taxa in fact occur in markedly drier habitats. We also calibrate their phylogeny to estimate when derived woodiness evolved. Finally, we describe the wood anatomy of selected woody and herbaceous taxa to see if life forms are linked to any particular wood traits. Results The evolution of derived woodiness in chamaephytes and phanerophytes as well as the shifts to short-lived annual therophytes in the Lefebvrea clade took place at roughly the same time: in the Late Miocene during a trend of global climate aridification. Climatic niches of woody and herbaceous genera from the Cape Floristic Region overlap. There are only two genera with distinctly different climatic preferences: they are herbaceous and occur outside of the Cape Floristic Region. Therefore, studied herbs have an overall climatic niche wider than their woody cousins. Woody and herbaceous species do not differ in qualitative wood anatomy, which is more affected by stem architecture and, probably, reproductive strategy than by habit. Conclusions Palaeodrought was likely a stimulus for the evolution of derived woodiness in the Lefebvrea clade, supporting the cavitation theory. The concurrent evolution of short-lived annuals withering before summer exemplifies an alternative solution to the same problem of drought-induced cavitation. Changes of the life form were most likely neither spurred nor precluded by any qualitative wood traits, which in turn are more affected by internode length and probably also reproductive strategy.

Comparative wood anatomy and origin of woodiness in subfamilies Secamonoideae and Asclepiadoideae (Apocynaceae)

“…The abundance of derived woody Asclepiadoideae in (seasonally) dry environments is in line with the drought hypothesis, which states that drought could have been a major evolutionary driver of wood formation (Lens & al., 2013a,b; Zizka & al., 2022). While we cannot be fully confident that drought is the main driver of wood formation in the otherwise predominantly herbaceous Asclepiadoideae lineages, the link between increased woodiness and increased drought tolerance (1) supports earlier studies on the distribution of insular woodiness on the Canary Islands (Lens & al., 2013a; Hooft van Huysduynen & al., 2021), (2) agrees with drought as one of the most important drivers triggering wood formation on islands (Zizka & al., 2022), and (3) is in line with experimental work demonstrating that species with more wood formation or lignification in the stem are better able to prevent the formation and spread of drought‐induced gas bubbles inside the water conducting xylem cells (Lens & al., 2013b; Dória & al., 2018, 2019; Thonglim & al., 2020; Frankiewicz & al., 2021). However, we do acknowledge that drought may not be the only potential driver of woodiness and that these drivers may be lineage specific (Carlquist, 1974; Kidner & al., 2016; Neupane & al., 2017; Frankiewicz & al., 2020; Zizka & al., 2022).…”

Raylessness and paedomorphosis: losses and gains of xylem rays en route from procambium to vascular cambium

“…The interfascicular areas are sites of formation of interfascicular cambia, which interconnect fascicular cambia into a continuous ring. When stem thickening begins, the newly produced secondary xylem is either homogenous (wood deposited in fascicular and interfascicular areas do not differ to any perceptible degree) or heterogenous (vessels, fibres, and parenchyma are deposited in fascicular areas, while interfascicular areas are occupied either by fibres or parenchyma, but devoid of vessels) (Frankiewicz et al 2021(Frankiewicz et al , 2022b. In plants with primary tissues organised in continuous rings (e.g., Plantaginaceae, Polemoniaceae, Rubiaceae), the newly produced wood is always homogenous (Kostytschew 1924;Metcalfe & Chalk 1950;Krumbiegel & Kästner 1993;Oskolski et al 2021).…”

“…Intermediate cases (i.e., retention of fascicular/interfascicular distinction and initiation of new rays) also exist. The second case, as well as intermediate ones, are found mostly among plants with limited cambial activity, including representatives of Apiaceae, Begoniaceae, Piperaceae, and many others (Carlquist 1985a;Crivellaro & Schweingruber 2013;Schweingruber et al 2013a,b;Kidner et al 2015;Trueba et al 2015;Frankiewicz et al 2021Frankiewicz et al , 2022a.…”

“…Are rays really necessary in thin stems? Complete raylessness is observed only in stems with thin-walled xylem cylinders, while thicker ones eventually develop rays (Frankiewicz et al 2020(Frankiewicz et al , 2021(Frankiewicz et al , 2022a. The short distance between pith, cambium, and phloem can be crossed by water and photosynthates through the network of axial parenchyma, vessels, and in some cases imperforate tracheary elements (Carlquist & Zona 1988;Carlquist 2007Carlquist , 2018.…”