J Syst Evol ›› 2021, Vol. 59 ›› Issue (5): 915-934.DOI: 10.1111/jse.12747

• Research Articles • Previous Articles     Next Articles

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

Mario Rincón‐Barrado1,2*, Sanna Olsson3, Tamara Villaverde1,4, Belén Moncalvillo5, Lisa Pokorny1,6, Alan Forrest7, Ricarda Riina1†, and Isabel Sanmartín1*†   

  1. 1 Real Jardín Botánico (RJB‐CSIC), Madrid 28014, Spain
    2 Area of Biodiversity and Conservation, School of Experimental Sciences and Technology (ESCET), Universidad Rey Juan Carlos, Móstoles, Madrid 28933, Spain
    3 Forest Research Centre, INIA‐CSIC, Madrid 28040, Spain
    4 Current address: Departamento de Biodiversidad, Ecología y Evolución, Facultad de Ciencias Biológicas, Universidad Complutense de Madrid, C/ José Antonio Novais, 12, Madrid 28040, Spain
    5 Department of Ecology, Faculty of Biology, Philipps‐University Marburg, Marburg D‐35043, Germany
    6 Current address: Centre for Plant Biotechnology and Genomics (CBGP UPM‐INIA), Pozuelo de Alarcón, Madrid 28223, Spain
    7 Centre for Middle Eastern Plants, Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh EH3 5LR, UK
  • Received:2021-02-01 Accepted:2021-03-31 Online:2021-04-06 Published:2021-09-01

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.

Key words: climate change, disjunct distribution, ecological vicariance, extinction rates, niche evolution, Rand Flora