Multiple routes underground? Frost alone cannot explain the evolution of underground trees

Finckh et al. (2016; this issue of New Phytologist, pp. 904–909) query our inferences drawn from a recent study (Maurin et al., 2014) on the evolutionary origins of the geoxylic suffrutex life form in southern Africa. Geoxylic suffrutices, or more informally ‘underground trees’ represent a distinct growth form characterized by a long-lived woody xylopodia underground with often short lived aerial shoots (White, 1979; Simon & Pennington, 2012). Described in detail by White (1979), ‘geoxyles’ are common in fire-dependent savanna ecosystems. Using a time calibrated phylogenetic tree for the woody taxa of southern Africa, sampling 1400 taxa, we showed that the geoxylic suffrutex life form evolved independently multiple times, suggesting a selective advantage to going ‘underground’ (Maurin et al., 2014). We reviewed four putative drivers of the geoxyle habit: (1) winter frost on the South African Highveld, proposed by Burtt Davy (1922); (2) mammal herbivory; (3) edaphic factors, particularly seasonal waterlogging; and (4) fire. We discussed evidence in support of each, and found that escape from fire is the most general explanation. We noted that ‘poor growing conditions that reduce growth rates of juvenile trees would also result in reduced probabilities of reaching fire-proof sizes and transitioning to tall mature trees’ and that ‘geoxyles are common where site conditions reduce growth rates, such as on seasonally waterlogged and/or low-nutrient soils, or, . . . at high-altitude sites with cold winters’ (Maurin et al., 2014). Finckh et al. (2016) suggest we may have overestimated the link with fire, and overlooked the importance of frost; we revisit their arguments.