Western Washington University Western CEDAR Biology Faculty and Staff ubP lications Biology 2014 Integrating Multiple Lines of Evidence into Historical Biogeography Hypothesis Testing: A Bison bison Case Study Jessica L. Metcalf Stefan Prost David Nogués-Bravo Eric G. DeChaine Western Washington University, [email protected] Christian Anderson See next page for additional authors Follow this and additional works at: https://cedar.wwu.edu/biology_facpubs Part of the Biology Commons Recommended Citation Metcalf, Jessica L.; Prost, Stefan; Nogués-Bravo, David; DeChaine, Eric G.; Anderson, Christian; Batra, Persaram; Araújo, Miguel B.; Cooper, Alan; and Guralnick, Robert P., "Integrating Multiple Lines of Evidence into Historical Biogeography Hypothesis Testing: A Bison bison Case Study" (2014). Biology Faculty and Staff Publications. 39. https://cedar.wwu.edu/biology_facpubs/39 This Article is brought to you for free and open access by the Biology at Western CEDAR. It has been accepted for inclusion in Biology Faculty and Staff ubP lications by an authorized administrator of Western CEDAR. For more information, please contact [email protected]. Authors Jessica L. Metcalf, Stefan Prost, David Nogués-Bravo, Eric G. DeChaine, Christian Anderson, Persaram Batra, Miguel B. Araújo, Alan Cooper, and Robert P. Guralnick This article is available at Western CEDAR: https://cedar.wwu.edu/biology_facpubs/39 Downloaded from rspb.royalsocietypublishing.org on January 24, 2014 Integrating multiple lines of evidence into historical biogeography hypothesis testing: a Bison bison case study Jessica L. Metcalf, Stefan Prost, David Nogués-Bravo, Eric G. DeChaine, Christian Anderson, Persaram Batra, Miguel B. Araújo, Alan Cooper and Robert P. Guralnick Proc. R. Soc. B 2014 281, 20132782, published 8 January 2014 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2014/01/06/rspb.2013.2782.DC1.h tml References This article cites 55 articles, 10 of which can be accessed free http://rspb.royalsocietypublishing.org/content/281/1777/20132782.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections ecology (1536 articles) evolution (1656 articles) palaeontology (157 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on January 24, 2014 Integrating multiple lines of evidence into historical biogeography hypothesis testing: a Bison bison case study rspb.royalsocietypublishing.org Jessica L. Metcalf1,2,†, Stefan Prost4,5,†, David Nogue´s-Bravo6, Eric G. DeChaine7, Christian Anderson8, Persaram Batra9, Miguel B. Arau´jo6,10,11, Alan Cooper1 and Robert P. Guralnick3 1Australian Centre for Ancient DNA, University of Adelaide, Adelaide, South Australia, Australia Research 2Department of Chemistry and Biochemistry, and 3Museum of Natural History, University of Colorado, Boulder, CO, USA 4 Cite this article: Metcalf JL, Prost S, Nogue´s- Allan Wilson Centre for Molecular Ecology and Evolution, University of Otago, Dunedin, New Zealand 5Department of Integrative Biology, University of California, Berkeley, CA, USA Bravo D, DeChaine EG, Anderson C, Batra P, 6Center for Macroecology, Evolution, and Climate, University of Copenhagen, Copenhagen, Denmark Arau´jo MB, Cooper A, Guralnick RP. 2014 7Department of Biology, Western Washington University, Bellingham, WA, USA Integrating multiple lines of evidence 8Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA 9 into historical biogeography hypothesis testing: Department of Geology, Greenfield Community College, Greenfield, MA, USA 10Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, CSIC, a Bison bison case study. Proc. R. Soc. B 281: Madrid, Spain 20132782. 11Imperial College London, Silwood Park Campus, Berkshire, UK http://dx.doi.org/10.1098/rspb.2013.2782 One of the grand goals of historical biogeography is to understand how and why species’ population sizes and distributions change over time. Multiple types of data drawn from disparate fields, combined into a single Received: 25 October 2013 modelling framework, are necessary to document changes in a species’s Accepted: 4 December 2013 demography and distribution, and to determine the drivers responsible for change. Yet truly integrated approaches are challenging and rarely performed. Here, we discuss a modelling framework that integrates spatio-temporal fossil data, ancient DNA, palaeoclimatological reconstruc- tions, bioclimatic envelope modelling and coalescence models in order to Subject Areas: statistically test alternative hypotheses of demographic and potential distri- ecology, evolution, palaeontology butional changes for the iconic American bison (Bison bison). Using different assumptions about the evolution of the bioclimatic niche, we generate Keywords: hypothetical distributional and demographic histories of the species. We ancient DNA, bison, bioclimatic envelope then test these demographic models by comparing the genetic signature pre- dicted by serial coalescence against sequence data derived from subfossils models, Late Quaternary, historical and modern populations. Our results supported demographic models that biogeography, palaeoclimatic reconstructions include both climate and human-associated drivers of population declines. This synthetic approach, integrating palaeoclimatology, bioclimatic envel- opes, serial coalescence, spatio-temporal fossil data and heterochronous Author for correspondence: DNA sequences, improves understanding of species’ historical biogeogra- phy by allowing consideration of both abiotic and biotic interactions at the Robert P. Guralnick population level. e-mail: [email protected] 1. Introduction A main goal of historical bioegeography is to determine drivers of species distributions and demography through time. Doing so, however, is challenging, †These authors contributed equally to this as multiple types of biotic and abiotic processes affect population dynamics, study. and, ideally, all these processes should be considered when making inferences about a species’s past distribution and demography. Carstens & Richards [1] Electronic supplementary material is available combined advances in bioclimatic envelope models (BEMs), statistical phylo- at http://dx.doi.org/10.1098/rspb.2013.2782 or geography and coalescence in an attempt to integrate disparate processes into a common modelling framework. Their workflow began by developing hypo- via http://rspb.royalsocietypublishing.org. theses in the form of demographic models that characterize potential past & 2014 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from rspb.royalsocietypublishing.org on January 24, 2014 2 true past reconstruction of the past rspb.royalsocietypublishing.org bioclimatic envelope models translate into congruence of palaeoclimate estimate of (1) estimate of climate envelope demographic hypothesis to modelling historical (2) prediction of suitable habitat hypotheses genetic data biogeography time 1 time 1 fossils precip Pop. 1 Pop. 2 climate temp max temp min climate biotic extinction interactions time 2 time 2 fossils Proc. R. Soc. B precip climate Pop. 2 temp max temp min 281 : 20132782 Figure 1. A workflow for reconstructing a species’s historical biogeography by integrating multiple data types. We show how fossils, palaeoclimate data along with radiocarbon dating and BEM techniques can be used to develop a hypothesis testing framework to be assessed with ancient and modern DNA datasets. The goal of combining several data types over multiple time frames is to improve estimates of historical biogeography so that they are closer to the species’s true history. (Online version in colour.) distributions of species using BEMs as a guide, and then test- Herein, we develop a multi-step, methodological work- ing those alternatives using coalescent methods [1]. Despite flow, which rigorously tests drivers of distributional and opportunities for integration of multiple lines of evidence, demographic changes, utilizing the American bison (Bison the vast majority of the many subsequent studies are still bison) as a focal case study group. Bison populations were limited along multiple dimensions. These limitations include: once extremely large, probably spanning most of western using only modern genetic data and modern occurrence data North America [7]. It remains unclear to what extent the to train and test demographic models about the past (e.g. [1]); changing climate and interactions with humans may have using only a single approach or method to build BEMs contributed to their decline [5,7,15]. For example, bison (e.g. [2]); considering only climate as a potential driver of were almost hunted to extinction in the nineteenth century, species’ distribution and demography (e.g. [3]); using ancient leaving populations today founded from as few as 30 to 50 DNA but only modern occurrence data (e.g. [4]), and quanti- individuals [16]. We explore in particular the following key fying only coarse parameters of overall range extent when questions. Are BEM-predicted changes in bison population population-level scales are likely to be very important (e.g. structure and size supported by genetic