Afro-alpine flagships revisited: Parallel adaptation, intermountain admixture and shallow genetic structuring in the giant senecios (Dendrosenecio)

Abstract

Distantly related lineages of the enigmatic giant rosette plants of tropical alpine environments provide classical examples of convergent adaptation. For the giant senecios (Dendrosenecio), the endemic landmarks of the East African sky islands, it has also been suggested that parallel adaptation has been important for within-lineage differentiation. To test this hypothesis and to address potential gene flow and hybridization among the isolated sky islands, we organized field expeditions to all major mountains. We sampled all currently accepted species and all but one subspecies and genotyped 460 plants representing 109 populations. We tested whether genetic structuring corresponds to geography, as predicted by a parallel adaptation hypothesis, or to altitudinal belt and habitat rather than mountains, as predicted by a hypothesis of a single origin of adaptations. Bayesian and Neighbor-Net analyses showed that the main genetic structure is shallow and largely corresponds to geography, supporting a hypothesis of recent, rapid radiation via parallel altitude/habitat adaptation on different mountains. We also found evidence for intermountain admixture, suggesting several long-distance dispersals by wind across vast areas of unsuitable habitat. The combination of parallel adaptation, secondary contact, and hybridization may explain the complex patterns of morphological variation and the contradicting taxonomic treatments of these rare enigmatic giants, supporting the use of wide taxonomic concepts. Notably, the within-population genetic diversity was very low and calls for increased conservation efforts.

Climate Vulnerability Assessment of the Espeletia Complex on Páramo Sky Islands in the Northern Andes

“…Inter-mountain exchange is also plausible, as reported in other tropical sky islands (Chala et al, 2020;Tusiime et al, 2020).…”

History and evolution of the afroalpine flora: in the footsteps of Olov Hedberg

“…Helichrysum, on the other hand, one of the most species-rich genera in the afroalpine flora, colonised the tropical alpine zone at least five times independently from local ancestors Fig. 2 The afroalpine flagship genus Dendrosenecio shows conspicuous and intricate variation in growth form and morphology, resulting from parallel altitude/habitat adaptation on different mountains combined with occasional long-distance dispersal and hybridization (Tusiime et al 2020;Gizaw et al in press;photos: Abel Gizaw). a-d: Growth form differentiation in high-altitude habitats on Mt Kenya.…”

“…i-o Plants at higher altitudes tend to have thick stems with a prominent layer of insulating old leaves, exemplified by plants of D. adnivalis in the Ruwenzori Mts (i, j), D. kilimanjari on Mt Kilimanjaro (k, l) and D. elgonensis on Mt Elgon (m-o). Adopted from Tusiime et al (2020) at lower elevations (Galbany-Casals et al 2014). This genus originated in Southern Africa and spread via the Drakensberg Mountains into the montane and alpine regions of eastern Africa.…”

“…The lineage radiated throughout the Pliocene to the late Pleistocene (Knox and Li 2017). In Dendrosenecio, the situation is not yet fully clarified, but a recent study based on high-throughput sequencing (Hyb-Seq) suggests that the lineage diversified from the Late Miocene and well into the Pleistocene (Gizaw et al in press), and the current species diversity seems to result from parallel altitude/habitat adaptation in four mountain groups (Tusiime et al 2020). Knox and Palmer (1995) suggested, contrary to Hedberg (1986) and others that the giant senecios originated at high altitudes on Mt Kilimanjaro.…”

“…The giant Lobelia lineage in eastern Africa diversified into 21 species to occupy a range of habitats in montane forests and the afroalpine zone (Knox and Palmer 1998), representing a combination of adaptive radiation and intermountain allopatric speciation. In Dendrosenecio, parallel altitudinal adaptation in different mountain groups, in a few cases combined with adaptation to different habitats within individual mountains, seem to have resulted in 5-10 species (Tusiime et al 2020;Gizaw et al, in press;note, however, that Knox 2005 and in particular Hedberg 1957Hedberg , 1969 accepted more species). In Senecio, the most speciesrich genus in the afroalpine flora, one of the independent immigrations resulted in seven species (Kandziora et al 2016).…”