Integrating fossils, phylogenies, and niche models into biogeography to reveal ancient evolutionary history: the case of hypericum (hypericaceae) Andrea Sanchez Meseguer, Jorge M. Lobo, Richard Ree, David J. Beerling, Isabel Sanmartin To cite this version: Andrea Sanchez Meseguer, Jorge M. Lobo, Richard Ree, David J. Beerling, Isabel Sanmartin. Inte- grating fossils, phylogenies, and niche models into biogeography to reveal ancient evolutionary history: the case of hypericum (hypericaceae). Systematic Biology, Oxford University Press (OUP), 2015, 64 (2), pp.215 - 232. 10.1093/sysbio/syu088. hal-02638449 HAL Id: hal-02638449 https://hal.inrae.fr/hal-02638449 Submitted on 28 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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For commercial re-use, please contact [email protected] DOI:10.1093/sysbio/syu088 Advance Access publication November 13, 2014 Integrating Fossils, Phylogenies, and Niche Models into Biogeography to Reveal Ancient Evolutionary History: The Case of Hypericum (Hypericaceae) , ,∗ ANDREA S. MESEGUER1 2 ,JORGE M. LOBO3,RICHARD REE4,DAV I D J. BEERLING5, AND ISABEL SANMARTÍN1 1Department of Biodiversity and Conservation, Real Jardín Botánico, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain; 2INRA, UMR 1062 CBGP Campus International de Baillarguet, 34988 Montferrier-sur-Lez, France; 3Department of Biogeography and Global Change, Museo Nacional Ciencias 4 5 Naturales-CSIC, 28006 Madrid, Spain; Department of Botany, Field Museum of Natural History, Chicago, IL 60605, USA and Department of Animal Downloaded from and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK ∗ Correspondence to be sent to: Department of Biodiversity and Conservation, Real Jardín Botánico, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain; E-mail: [email protected] and [email protected] Received 31 January 2014; reviews returned 27 May 2014; accepted 7 November 2014 Associate Editor: Austin Mast http://sysbio.oxfordjournals.org/ Abstract.—In disciplines such as macroevolution that are not amenable to experimentation, scientists usually rely on current observations to test hypotheses about historical events, assuming that “the present is the key to the past.” Biogeographers, for example, used this assumption to reconstruct ancestral ranges from the distribution of extant species. Yet, under scenarios of high extinction rates, the biodiversity we observe today might not be representative of the historical diversity and this could result in incorrect biogeographic reconstructions. Here, we introduce a new approach to incorporate into biogeographic inference the temporal, spatial, and environmental information provided by the fossil record, as a direct evidence of the extinct biodiversity fraction. First, inferences of ancestral ranges for those nodes in the phylogeny calibrated with the fossil record are constrained to include the geographic distribution of the fossil. Second, we use fossil distribution and past climate data to reconstruct the climatic preferences and potential distribution of ancestral lineages over time, and use this information to build a biogeographic model that takes into account “ecological connectivity” through time. To show the power of this approach, we reconstruct the biogeographic history of the large angiosperm genus Hypericum, which has a fossil record at INRA Institut National de la Recherche Agronomique on September 11, 2015 extending back to the Early Cenozoic. Unlike previous reconstructions based on extant species distributions, our results reveal that Hypericum stem lineages were already distributed in the Holarctic before diversification of its crown-group, and that the geographic distribution of the genus has been relatively stable throughout the climatic oscillations of the Cenozoic. Geographical movement was mediated by the existence of climatic corridors, like Beringia, whereas the equatorial tropical belt acted as a climatic barrier, preventing Hypericum lineages to reach the southern temperate regions. Our study shows that an integrative approach to historical biogeography—that combines sources of evidence as diverse as paleontology, ecology, and phylogenetics—could help us obtain more accurate reconstructions of ancient evolutionary history. It also reveals the confounding effect different rates of extinction across regions have in biogeography, sometimes leading to ancestral areas being erroneously inferred as recent colonization events. [Biogeography; Cenozoic climate change; environmental niche modeling; extinction; fossils; Hypericum; phylogenetics.] In historical biological disciplines such as (Ronquist and Sanmartín 2011). Similarly, in parametric macroevolution or macroecology, which are not methods such as dispersal–extinction–cladogenesis in general amenable to experimentation, scientists (DEC), ancestral ranges are inferred conditional on need to rely on present-day observations to make the distribution of the extant descendants; however, inferences about the past. For example, systematists correct estimates can only be obtained if extinction use current variation in morphological and/or DNA and dispersal rates—which are modeled as stochastic traits to reconstruct phylogenetic relationships and processes evolving along branches—are low in relation rates of nucleotide mutation. In historical biogeography, to cladogenesis (Ree and Smith 2008). biogeographers use phylogenetic relationships and One scenario that is particularly damaging to the present distribution data to infer ancestral geographic assumption that the present is the key to the past is ranges and past biogeographic events (Lomolino et al. when extinction rates are so high that the biodiversity 2010). Assuming that “the present is the key to the past” we observe today is no longer representative of the (and the future) is to a certain extent inevitable in a historical diversity. Extinction erases the evidence of comparative observational science that deals with scales past speciation events and, as we move back into the of space and time at which experimental manipulation is past, there is less information to infer ancestral states. hardly possible (Lomolino et al. 2010). This assumption This results in inferences for basal cladogenetic events permeates methods in biogeographic inference. For that are often uncertain and tend to include a large example, it is the basis for the assignment of cost values in number of areas (Ronquist and Sanmartín 2011), or event-based biogeographic methods, in which processes even wrong biogeographic reconstructions if extinction such dispersal and extinction are penalized (higher has been particularly high within an area (Lieberman cost) because they partly erase previous distributional 2005). A possible solution comes from the fossil history—preventing the recovery of “phylogenetically record, which provides direct evidence on the extinct conserved” distribution patterns—, whereas vicariance biodiversity fraction that we cannot observe. So far, the and within-area speciation are given a low cost because use of fossils in biogeography has been limited to the they involve inheritance of distributional ranges provision of calibration points for phylogenetic dating 215 [12:27 3/2/2015 Sysbio-syu088.tex] Page: 215 215–232 216 SYSTEMATIC BIOLOGY VOL. 64 (Ho and Phillips 2009). However, recent biogeographic time scales (Stigall Rode and Lieberman 2005; Stigall studies have shown that incorporating the geographic 2012). But the incompleteness of the fossil record and distribution of fossils to the analysis may change the lack of environmental data in the deep past have dramatically the inferred biogeographic scenario (Mao so far limited this approach to recent geological periods et al. 2012; Nauheimer et al. 2012; Wood et al. 2012). (Nogués-Bravo et al. 2008) and small geographical These studies, however, have relied on using fossils as regions (Maguire and Stigall 2009). additional lineages in the phylogeny, which requires Here, we introduce a new approach to incorporate coding the morphological traits of the fossil taxa into biogeographic inference the temporal, spatial, and alongside the extant molecular characters (e.g., Mao et al. climatic information provided by the fossil record as 2012), or assuming arbitrary branch lengths for the fossil direct evidence of the extinct biodiversity fraction. First, Downloaded from lineage (Nauheimer et al. 2012). the spatial range of a fossil is used to constrain the In addition to the temporal and spatial aspect,