Ecological and geological processes impacting speciation modes drive the formation of wide‐range disjunctions within tribe Putorieae (Rubiaceae)

Abstract

Wide‐range geographically discontinuous distributions have long intrigued scientists. We explore the role of ecology, geology, and dispersal in the formation of these large‐scale disjunctions, using the angiosperm tribe Putorieae (Rubiaceae) as a case study. From DNA sequences of nuclear ITS and six plastid markers, we inferred a phylogeny with 65% of all known Putorieae species. Divergence times, ancestral ranges, and diversification rate shifts were then estimated using Bayesian inference. We further explored species climatic tolerances and performed ancestral niche reconstruction to discriminate among alternative speciation modes, including geographical and ecological vicariance, and ecogeographical, ecological, and dispersal‐mediated speciation. As a result, we identified seven major clades in Putorieae, some of which exhibit striking geographical disjunctions, matching the Rand Flora pattern, with sister species in the Canary Islands and eastern and southern Africa. Initial diversification within the tribe occurred in the early Miocene, coincident with a period of climate warming; however, most clades diverged within the last 10 Myr. Aridification and high extinction rates, coupled with ecological vicariance, explain the oldest disjunctions. Adaptation to new environmental conditions, after allopatry, is observed in several clades. Dispersal, either long‐distance or via corridors made available by mountain uplift, is behind the most recent disjunctions. Some of these events were followed by ecological speciation and rapid diversification, with species becoming adapted to xeric or increasingly colder continental climates. We show that an integrative approach may help discriminate among speciation modes invoked to explain disjunctions at macroevolutionary time scales, even when extinction has erased the signature of past events.

Rare and widespread: integrating Bayesian MCMC approaches, Sanger sequencing and Hyb‐Seq phylogenomics to reconstruct the origin of the enigmatic Rand Flora genus Camptoloma

“…The scenario described above supports the “climatic refugia” hypothesis, according to which the current disjunct distribution of Camptoloma across Africa is the result of fragmentation and extinction events associated to a historical aridification process (Sanmartín et al, 2010; Mairal et al, 2015a, 2017; Pokorny et al, 2015; Villaverde et al, 2018; Rincón‐Barrado et al, 2021). This scenario does not preclude the possibility of dispersal events.…”

“…In many groups, the eastern/western disjunction across North Africa is estimated to be older than the eastern–southern African disjunction (Pokorny et al, 2015). This is explained by initial vicariance in the north (i.e., due to the Late Miocene formation of the Sahara Desert; Senut et al, 2009), followed by stepping‐stone dispersal from eastern to southern Africa along the temperate‐climate corridor formed by the uplift of the Eastern Arc Mountains in the Pliocene (Sepulchre et al, 2006; Mairal et al, 2015a; Rincón‐Barrado et al, 2021).…”

“…Uplift of the Eastern Arc Mountains started in the Late Miocene, ~7–8 Ma, and reached a maximum during the Pliocene (5–3 Ma), with the formation of semiarid plateaus (the Ethiopian Highlands) and the desertification of low‐lying areas in the Horn of Africa (Sepulchre et al, 2006). These mountain ranges could have acted as biogeographic corridors, allowing migration of Rand Flora lineages and other Afrotemperate taxa, between southern and northern Africa (Galley et al, 2007; Popp et al, 2008; Roquet et al, 2009; Barres et al, 2013; Mairal et al, 2015a; Meseguer et al, 2015; Rincón‐Barrado et al, 2021). The crown‐ancestor of Camptoloma (~4.3 Ma, Figure 3A) was inferred to occur in all three regions where the genus is currently present by the Early Pliocene (Figure 4).…”

“…This scenario does not preclude the possibility of dispersal events. Indeed, some short‐to‐medium range dispersal scenario is needed to explain the current disjunction, i.e., along the Eastern Arc corridor or across North Africa, as it has been suggested in other Rand Flora taxa ( Canarina , Mairal et al, 2015a; Plocama , Rincón‐Barrado et al, 2021). Yet, the deep temporal divergences (Early–Mid Pliocene) among the three Camptoloma species observed do not support a recent, long‐distance dispersal explanation (Coleman et al, 2003; Désamoré et al, 2010).…”

“…However, some Rand Flora lineages exhibit an even wider disjunction, spanning the entire African continent, a west/east/south biogeographic disjunct pattern. Examples are found in genus Kleinia (Asteraceae; Pelser et al, 2007) and Plocama (Rubiaceae; Backlund et al, 2007; Rincón‐Barrado et al, 2021).…”