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Echoes of the whispering land: interacting roles of vicariance and selection in shaping the evolutionary divergence of two Calceolaria (Calceolariaceae) species from Patagonia and Malvinas/Falkland Islands

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Abstract

A key to understanding the origin and identity of young species lays on the knowledge of the Quaternary climatic oscillations’ effect on gene flow and vicariance. Even though the effect of climatic fluctuations is relatively well understood for southern hemisphere plant species, little is known about their effect on the evolutionary histories of species from mainland and islands. Thus, we investigated whether Quaternary climate-driven fluctuations translated into lineage divergence and speciation, followed or not by climatic niche differentiation, in two allopatric plant species, Calceolaria uniflora and C. fothergillii from Patagonia and Malvinas/Falkland islands, respectively. We sampled the range of both species, and sequenced two chloroplastic (cpDNA; trnS–trnG and trnH–psbA), and one single copy “anonymous” non-coding nuclear region (nDNA). We performed phylogeographic and dating analyses, and adjusted spatio-temporal diffusion models. We complemented molecular evidence with climatic niche differentiation analyses and species paleo-distribution projections. A species coalescent reconstruction based on multi-locus data retrieved both species as monophyletic. Estimates from cpDNA indicated the species diverged during the Great Patagonian Glaciation. Chloroplast and nuclear DNA showed east–west distribution of the main genetic groups but with contrasting spatial genetic diversity. The spatio-temporal diffusion analyses showed that between 1–0.8 Mya and 570 Kya the lineage leading to C. fothergillii diverged from C. uniflora and arrived to the islands. Climatic niche projections hindcasted range expansions during glaciations, and contractions during the interglacial periods. Comparisons of climatic niches between the two study species indicated that temperature variables show evidence of niche conservatism while precipitation regimes supported niche divergence, even when considering the background environmental divergence. Our study indicates that glacial fluctuations affected the mainland/islands connections favouring speciation mediated not only by isolation, but also by climatic niche differentiation.

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Acknowledgements

A. C. and A. N. S. acknowledge the National Research Council of Argentina (CONICET) and the Universidad Nacional de Córdoba (UNC) as researchers, and M. C. B. as postdoctoral fellowship holder. We thank APN Argentina for permits to work within parks and reserves. The authors thank P. R. Riquez for allowing sampling in Ea. Verdadera Argentina, R. Upson, and the Falkland Conservation for providing samples and information on C. fothergillii, E. Dominguez for providing georeferences in Chile, A.A. Cocucci, S. Benitez Vieyra D. Carmona for field assistance, and M. C. Acosta for analytical support. Funding: National Research Council of Argentina [PIP 201101-00245, PIP 11220150100690CO] to A.N.S., the National Ministry of Science and Technology [FONCYT-PICT-2011-0837, PICT 2015-3089] to A.N.S., and A.E. was supported by the Swiss National Science Foundation [Grants P300P3 151141 and PBNEP3 140192]

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  1. Matías Cristian Baranzelli, Andrea Cosacov and Alicia Noemí Sérsic have contributed equally to this study and should be considered as co-first authors.

Authors and Affiliations

  1. Laboratorio de Ecología Evolutiva - Biología Floral, Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET-Universidad Nacional de Córdoba, Dirección postal: Casilla de Correo 495, X5000ZAA, Córdoba, Argentina

    Matías Cristian Baranzelli, Andrea Cosacov, Maria del Rosario Iglesias & Alicia Noemí Sérsic

  2. Department of Biological Sciences, University of Idaho, Life Sciences South 252, 875 Perimeter Dr. MS3051, Moscow, ID, 83844-3051, USA

    Anahí Espíndola

  3. Department of Biology, Pacific University, 2043 College Way, Forest Grove, OR, 97116, USA

    Lauren M. Chan

  4. Department of Biology and M. L. Bean Life Science Museum, Brigham Young University, Provo, UT, 84602, USA

    Leigh A. Johnson

  5. Instituto Multidisciplinario de Biología Vegetal (IMBIV), Ciudad Universitaria, Av. Vélez Sársfield 1611, X5016GCA, Córdoba, Argentina

    Alicia Noemí Sérsic

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  1. Matías Cristian Baranzelli
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Baranzelli, M.C., Cosacov, A., Espíndola, A. et al. Echoes of the whispering land: interacting roles of vicariance and selection in shaping the evolutionary divergence of two Calceolaria (Calceolariaceae) species from Patagonia and Malvinas/Falkland Islands. Evol Ecol 32, 287–314 (2018). https://doi.org/10.1007/s10682-018-9938-3

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