Author's personal copy Molecular evidence for recent founder populations and human-mediated migration in the barley scald pathogen Rhynchosporium secalis C.C. Linde a, * , M. Zala b , B.A. McDonald b a School of Botany and Zoology, The Australian National University, Daley Rd, Canberra, 0200 ACT, Australia b Plant Pathology, Institute of Integrative Biology, ETH Zurich, LFW B16, CH-8092 Zürich, Switzerland article info Article history: Received 4 September 2008 Revised 22 February 2009 Accepted 6 March 2009 Available online 14 March 2009 Keywords: Rhynchosporium secalis Anthropogenic migration Bottleneck Founder effect Host jump abstract Rhynchosporium secalis is an important pathogen of barley globally. Fourteen polymorphic microsatellites were analyzed for 1664 R. secalis isolates sampled from 37 field populations to infer their demographic history. The results falsified the hypothesis that R. secalis co-evolved with its barley host in the Middle East. Populations from Scandinavia had significantly higher allelic diversities, the greatest number of pri- vate alleles and the highest genotypic diversities. All but three of the analyzed populations had an excess of gene diversity compared to the number of alleles, consistent with a recent population bottleneck. The remaining populations had a gene diversity deficit consistent with a population expansion following a recent population bottleneck in the last ±100 years. A coalescent analysis revealed that the effective pop- ulation sizes based on h, of the analyzed populations were small relative to their ancestral population sizes, indicating that only a fraction of the diversity present in the ancestral populations was transmitted into current populations. These findings are consistent with the hypothesis that the pathogen population on barley experienced a selection bottleneck imposed by the host and/or are founder populations. The mean estimate of migration rates was 2.2 (avg 90% confidence interval = 1.3–3.1). Major migration routes were identified among populations separated by long distances, eg between South Africa and Australia, as well as among North Africa, the Middle East and California, suggesting contemporary exchange of infected barley seed. In contrast with earlier findings, most populations exhibited significant gametic dis- equilibrium, probably as a result of genetic drift. We conclude that the majority of R. secalis populations have experienced human-mediated migration that led to numerous and relatively recent founder events around the world. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction Analyses of genetic diversity provide useful information on the epidemiology and evolutionary history of infectious diseases. Infectious agents vary in effective population sizes, transmission abilities and reproduction, all which can be used to infer the pop- ulation history of the pathogen (Gordo and Campos, 2007). For fun- gal pathogens infecting agricultural crops, founder populations established through the spread of their hosts are expected to have less genetic diversity than the pathogen source population. In the- ory, bottlenecks reduce gene diversity and the number of alleles in populations. Empirically it was also shown that founder events fre- quently reduce allelic diversity and more rarely gene diversity (Clegg et al., 2002; Friar et al., 2000; Hufbauer et al., 2004). Thus, we can detect founder populations or determine whether a popu- lation has experienced a demographic bottleneck by using genetic information to determine whether a population has excess gene diversity relative to the number of alleles (Cornuet and Luikart, 1996; Luikart et al., 1998) or lower allelic richness than expected from gene diversity (Leberg, 2002). Because ancestral populations are older, we expect these populations to have the highest levels of genetic diversity, possess the most alleles and have more private alleles. Rhynchosporium secalis is a haploid fungal pathogen of barley currently found in all major barley-growing countries. Cultivated barley evolved from its wild progenitor Hordeum spontaneum in the Fertile Crescent where it was domesticated 12,000 years ago. Barley followed an eastward direction of spread from the Fertile Crescent, as well as further domestication and diversification through the Himalayas, then to Europe (6000 years BP) and the rest of Asia (Salamini et al., 2002). Previous studies suggested that the center of origin of R. secalis was not in the Fertile Crescent (Brunner et al., 2007; Zaffarano et al., 2006) because the highest levels of pathogen genetic diversity were found in northern Europe instead of in populations from the Fertile Crescent. To better understand the demographic history of R. secalis and to elucidate population bottlenecks, we analyzed a large number 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.03.002 * Corresponding author. Fax: +61 2 61255573. E-mail address: celeste.linde@anu.edu.au (C.C. Linde). Molecular Phylogenetics and Evolution 51 (2009) 454–464 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev