Within the tropics, the diversity of plant species is generally linked to water availability, with more moist biomes housing higher taxonomic diversity, particularly for woody plants (O'Brien et al., 2000; Daru et al., 2016; Esquivel-Muelbert et al., 2017). Within individual woody plant clades this pattern is also evident, with families and genera tending to be more species-rich in moist biomes compared to more arid biomes (Currie, 1991; Pennington et al., 2006). Assuming no systematic difference in the age of clades, these discrepancies could suggest that diversification rates are lower in arid versus moist biomes.

In contrast, scientists since Stebbins (1952) have argued that arid environments promote plant speciation (Axelrod, 1972; Böhnert et al., 2022). Arid biomes may house a greater diversity of edaphic conditions that can facilitate plant speciation (Stebbins, 1952; Axelrod, 1972; Buira et al., 2021), and the patchy distribution of species in arid biomes may be conducive to intermediate levels of gene flow among populations that can promote adaptive diversity and differentiation (Wright, 1940; Stebbins, 1952).

Present-day arid biomes have a dynamic climatological past, and increasing aridity since the Miocene across the globe has been cited as a causal factor in diversification of arid-affiliated plant lineages (Wu et al., 2018; Böhnert et al., 2022; Čalasan et al., 2022; Hua et al., 2022). Global aridification continued to increase throughout the Pliocene and Pleistocene climate cycles, with multiple examples of Quaternary diversification in arid-affiliated plant lineages (Kadereit and Abbott, 2021). There is ample evidence that arid biomes are areas of active and recent plant speciation. However, most studied examples pertain to herbaceous and succulent plant lineages (e.g., Klak et al., 2004; Arakaki et al., 2011; Guerrero et al., 2013; Böhnert et al., 2019; Lavor et al., 2019; Merklinger et al., 2021). Macroevolutionary studies of woody plant lineages, which show the most marked differences in diversity between arid and moist biomes, are scarce (although see Simon et al., 2009; Singhal et al., 2021). We do not yet have a firm idea of the relationship between arid climatic conditions and diversification in woody plant lineages.

Sub-Saharan Africa as a whole is dry in comparison to other regions of the tropics, such as the Americas and southeast Asia. Yet, arid regions of sub-Saharan Africa have received limited macroevolutionary study compared to regions like the Atacama Desert (Guerrero et al., 2013; Böhnert et al., 2019; Merklinger et al., 2021). The Namib Desert, in southwest Africa, is one of the oldest deserts on Earth, originating 55–80 Ma (Ward et al., 1983). It houses ancient iconic plant lineages such as the morphologically bizarre gymnosperm Welwitschia (Welwitschiaceae) and the similarly bizarre angiosperm lineage Tiganophyton (Tiganophytaceae, Swanepoel et al., 2020). These species-poor lineages are notable for occurring on long, isolated evolutionary branches, which have been termed “depauperons” (Donoghue and Sanderson, 2015). In contrast, other lineages emblematic of the Namib Desert have achieved markedly high taxonomic diversity, such as Euphorbia (Euphorbiaceae), Indigofera (Fabaceae), Commiphora (Burseraceae) and several genera of Acanthaceae (Craven, 2009; Darbyshire et al., 2020). Most of these clades are diverse across tropical Africa, and the species present in the hyper-arid region of southwest Africa are derived from multiple lineages.

One genus of Acanthaceae, Petalidium, stands out from other diverse genera in the region in that its diversity is centred in the Namib Desert and surrounding areas, and is hypothesized to derive from a single colonisation event (Tripp et al., 2017). Petalidium is furthermore a lineage of woody, non-succulent plants, a habit usually associated with higher diversity in moist regions. In the present study, we aim to test whether the arid conditions in the Namib Desert may have helped to spur diversification in the genus Petalidium, as proposed by Tripp et al. (2017). If supported, Petalidium would represent a notable counter-example to the assumption that tropical arid biomes inhibit woody plant diversification.

Petalidium is a genus of 36 accepted species that occur almost entirely in Namibia and Angola, with the exception of one species sister to the African taxa, which occurs in India and Nepal in a more moist climate and two species restricted to northeastern South Africa and adjacent areas in Zimbabwe (Tripp et al., 2017). Petalidium is the fifth most diverse genus in the arid Kaokoveld Region of northwestern Namibia and southwestern Angola (Craven, 2009) and is ecologically successful, being the dominant shrub cover in major portions of this region and also forming large populations of co-occurring species in many areas (all authors, pers. obs.). The total taxonomic diversity of Petalidium is likely higher than currently known as new species of Petalidium continue to be found after fieldwork in poorly studied regions (Swanepoel, 2020; Swanepoel and Manzitto-Tripp, 2022). African Petalidium appear to be undergoing an evolutionary radiation, with estimates for the crown age of the 35 African species ranging from 1.4 Ma to 3.6 Ma (Tripp et al., 2017). Species of Petalidium can occur in extremely arid areas where mean annual precipitation (MAP) is less than 50 mm per year, but other species of African Petalidium occur in more moist areas where MAP exceeds 700 mm. We know that at present the majority of species of Petalidium occur in more arid regions (Tripp et al., 2017), but the climatic history of the clade has not been studied. We do not know whether it originated in more moist or arid conditions. If it originated in more arid conditions, then its greater diversity in arid regions may simply be a result of a longer history of occupancy.

In order to examine the link between climatic conditions and diversification in Petalidium, we undertook the following steps: (i) we generated a new phylogeny for the genus using RAD sequencing, improving the species sampling from previous efforts by 50% (Tripp et al., 2017); (ii) we assessed variation in net diversification rate across the phylogeny; (iii) we reconstructed ancestral climatic niches across the phylogeny; and (iv) we tested for a link between net diversification and estimated ancestral climatic niche. Our overall aim was to test whether Petalidium shows higher species richness in arid climatic conditions relative to moist ones because of higher rates of net diversification in arid conditions or because of a longer history of occupancy of arid climatic environments, with equivalent or even lower net diversification in arid conditions.

In this study, we found that the higher species richness of Petalidium in arid areas relative to moist areas may indeed be linked to higher rates of net diversification in arid areas, in contrast to the alternative hypothesis of a longer history of occupancy in arid areas. Our analyses suggest that the genus as a whole originated in more moist conditions ca 5 Ma and that two lineages subsequently shifted to occurring in more arid conditions ca 1.6 Ma (Figure 4). One lineage in particular, the diverse arid clade, showed elevated rates of net diversification, and this clade occupies the most arid areas within the overall range of the genus. Yet, the singular nature of the diverse arid clade prevents us from making strong causal links between occupation of arid areas and net diversification rate within the genus Petalidium. However, combining the results here for Petalidium with published results for other clades suggests there indeed may be a causal link (Fisher et al., 2015; Darbyshire et al., 2020).

An evolutionary pattern of higher diversification rates in arid areas during the Pleistocene has been found in other lineages of Acanthaceae in the Namib Desert and surrounding regions (Fisher et al., 2015; Darbyshire et al., 2020). Similarly, the majority of the species-rich lineages in the neighbouring Succulent Karoo arid biome are younger than 10 Ma (Klak et al., 2004; Verboom et al., 2009; García-Aloy et al., 2017). Thus, Petalidium represents an additional data point, notably from a woody plant clade, supporting a growing body of evidence for rapid Quaternary diversifications of plants in the Namib Desert and surrounding regions. It is key to note though that the Namib Desert also houses incredibly old evolutionary lineages that are found nowhere else on earth, such as Welwitschia, which diverged from Gnetum in the Cretaceous (Hou et al., 2015) and Tiganophyton, an early diverging member of the Brassicaceae which originated in the Eocene (Hendriks et al., 2022).

How then do we explain the co-occurrence of recently radiated lineages and ancient depauperons (Donoghue and Sanderson, 2015) in the same space? We hypothesize that the answer lies in exceptional evolutionary turnover. Recent studies (Koenen et al., 2015; Pennington et al., 2015) have suggested that high diversity in tropical rain forests can be explained by the persistence of numerous evolutionary lineages through episodic periods of extinction, which then provide ample ‘seed lineages’ from which radiations can arise. If episodes of extinction in arid biomes are more severe, then fewer lineages would persist throughout these episodes and fewer would radiate afterwards. Overall, plant richness would be lower in arid compared to moist biomes (as observed), but there nonetheless could still be multiple lineages that show recent diversification.

There is extensive evidence that the Namib desert experienced climatic fluctuations during the Quaternary with alternating arid and mesic phases, or pluvial cycles (Scott et al., 1991, 2022; Lancaster, 2002; Dupont, 2006; Gil-Romera et al., 2006; Brook et al., 2007; Grodek et al., 2013; Greenbaum et al., 2014; Lim et al., 2016). These oscillating mesic–arid phases could have provided opportunities for isolation, but also opportunities for previously isolated populations to exchange genes and produce novel genetic combinations, with both processes contributing to diversification, as suggested by Stebbins (1952). Furthermore, high levels of inter-annual variability in rainfall and extended droughts may also drive vegetation die back (Crouchet et al., 2019; Wright et al., 2023), leaving a “clean slate” available for colonisation during mesic periods. In fact, in our most recent fieldwork in the Namib Desert and surrounding areas, we observed extensive dieback of plant populations compared to our first observations in the early 2010s, presumably as a result of widespread drought during the last decade.

Our molecular dataset of thousands of SNPs was sufficient to resolve the deepest nodes in the phylogeny of Petalidium, but not relationships within the diverse arid clade, which shows low bootstrap support values (Figure 2, Supplementary Figure S1). Such low support was not expected given that RADseq has shown sufficient power to resolve fine-scale phylogenetic relationships in Barleria, a closely related genus of Acanthaceae (Comito et al., 2022). This poor resolution in the shallow part of our phylogeny could be explained by hybridisation or incomplete lineage sorting, both of which may cause conflict among genes for relationships. Although field observations (all authors, pers. obs.) document the existence of putative hybrids in Petalidium, i.e., individuals with morphology intermediate between two co-occurring species, a preliminary test for hybridisation with our SNP data did not suggest any evidence for hybridisation (Supplementary Figure S2). Given the young age (1.63 Ma) and the high species richness of the diverse arid clade, incomplete lineage sorting could be a plausible explanation for the lack of support, but new genetic data, from full genomes or numerous unlinked nuclear loci (c.f. Morais et al., 2019), will be necessary to fully address this issue in Petalidium.

Future phylogeny construction based on unlinked nuclear loci, rather than SNP data, may also allow for the implementation of better algorithms for temporally calibrating phylogenies (e.g., Mirarab et al., 2014). We relied on penalized likelihood to calibrate our ML phylogeny, a method that is known to bias node ages towards older time (Carruthers and Scotland, 2022). Nevertheless, our estimates for the ages of younger clades in the phylogeny, such as the diverse arid clade are similar to Tripp et al. (2017), suggesting that future improvements to the phylogeny will be unlikely to invalidate our finding that the majority of diversification in Petalidium, particularly in the diverse arid clade, occurred during the Quaternary.

Our findings show a clear correlation between adaptation to extreme aridity and increased net diversification in Petalidium, albeit not a statistically significant one. We have suggested that alternating mesic and arid phases in a present-day arid region have driven this pattern, but there are alternative explanations. The genus exhibits a remarkable diversity of floral forms, associated with different pollinators, including open cup-shaped flowers (a generalist pollination syndrome), large tubular red flowers (bird pollinated), and small maroon flowers (pollinated by long-tongued flies), and the diverse arid clade has the greatest floral diversity in Petalidium. Interactions with pollinators is a long-hypothesized driver of angiosperm diversity (Van der Niet et al., 2014; Tripp et al., 2021), and changes in floral form linked to switching of pollinators and subsequent reproductive isolation may have promoted speciation in Petalidium. Pollinators do seem scarce in this arid region at present, but they may have been less so during past mesic phases. Clearly, further investigation is needed to unravel the potentially interacting factors that promoted such a recent and fast diversification in one of the driest environments on Earth.

The datasets presented in this study can be found in online repositories. The name of the repository and accession number can be found at: NCBI; PRJNA930345.

OL, EM-T, and KGD conceived the study. EM-T and KGD collected the samples in the field that underlie the phylogeny. EM-T executed laboratory analyses. OL and EM-T conducted bioinformatic and phylogenetic analyses. WS contributed key insights into identification of specimens and phylogenetic results. OL and KGD conducted downstream macroevolutionary analyses and wrote the first draft of the article. All authors contributed to the article and approved the submitted version.

OL received funding from the Swiss National Science Foundation (P2LAP3_191377 and P500PB_203081). EM-T gratefully acknowledges support from the National Science Foundation Award # 0919594. EM-T further acknowledges extensive support from the University of Colorado Herbarium (COLO) staff, in particular Dina Clark and Ryan Allen, for assistance with processing herbarium materials resulting from her fieldwork. KGD warmly thanks the British Ecological Society, the Systematics Association, the Moray Endowment Fund of the University of Edinburgh and the Natural Environment Research Council (NERC) of the UK via the SECO Large Grant NE/T01279X/1. EM-T and KGD acknowledge the National Commission on Research, Science and Technology of Namibia and the Ministério da Agricultura e Florestas of Angola for permission to conduct field research.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2023.1193728/full#supplementary-material