Demographic structure and genetic variability throughout the distribution of Platte thistle (Cirsium canescens Asteraceae)

Aim Understanding spatial variation in the demographic and genetic structure of populations is central to explaining causes of species range limits and to species conservation. The Abundant Centre Hypothesis (ACH) predicts that as one moves away from the centre of a species’ biogeographical range, populations become less frequent and more isolated, as well as exhibiting decreasing within-population density. This increased isolation may lead to reduced genetic variability in peripheral populations by limiting gene flow. In this study, we asked whether the frequency, within-population density and genetic diversity of Cirsium canescens (Platte thistle) populations decreased from the range centre to the edge, as predicted by the ACH. Location Central United States, including portions of the Great Plains and Rocky Mountains. Methods Frequency of population occurrence at regional and landscape scales, within-population density, and within-population genetic variation were evaluated along eight centre-edge transects within the species’ distribution. Leaf tissue samples were collected from each population to establish genetic variability using six simple sequence repeat loci. Results Consistent with the ACH, peripheral regions of C. canescens’ range were less likely to contain populations than central regions. In regions where C. canescens did occur, however, frequency of populations at a landscape scale peaked at intermediate distances from centre and within-population density was unrelated to distance. Populations exhibited reduced genetic variability towards range edges. Main conclusions The ACH underestimates the complexity of the relationship between variation in abundance and genetic diversity with distance from C. canescens’ range centre. Decreases in Platte thistle population frequency combined with no decreases in within-population density near range edges suggest that quality habitat exists in the peripheral range, but these patches are rarer. Although genetic variability was reduced at the distribution edges, this decline was stronger towards the western edge, associated with increased topographic complexity.

[1]  C. Eckert,et al.  Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond , 2008, Molecular ecology.

[2]  S. Byars,et al.  Effect of altitude on the genetic structure of an Alpine grass, Poa hiemata. , 2009, Annals of botany.

[3]  F. Woodward,et al.  Seed production and population density decline approaching the range-edge of Cirsium species. , 2003, The New phytologist.

[4]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[5]  J. Hsiao,et al.  Altitudinal Genetic Differentiation and Diversity of Taiwan Lily (Lilium longiflorum var. formosanum; Liliaceae) Using RAPD Markers and Morphological Characters , 2001, International Journal of Plant Sciences.

[6]  R. Sagarin Recent studies improve understanding of population dynamics across species ranges , 2006 .

[7]  R. Petit,et al.  Conserving biodiversity under climate change: the rear edge matters. , 2005, Ecology letters.

[8]  N. Swenson,et al.  Clustering of Contact Zones, Hybrid Zones, and Phylogeographic Breaks in North America , 2005, The American Naturalist.

[9]  T. Waite,et al.  Spatial patterns of demography and genetic processes across the species' range: Null hypotheses for landscape conservation genetics , 2003, Conservation Genetics.

[10]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[11]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[12]  P. Siikamäki,et al.  Genetic Diversity, Population Size, and Fitness in Central and Peripheral Populations of a Rare Plant Lychnis viscaria , 1999 .

[13]  R. Frankham Relationship of genetic variation to population size in wildlife , 1996 .

[14]  Patrick J. McIntyre,et al.  Evolution and Ecology of Species Range Limits , 2009 .

[15]  C. Richards,et al.  Accurate Inference of Subtle Population Structure (and Other Genetic Discontinuities) Using Principal Coordinates , 2009, PloS one.

[16]  James H. Brown On the Relationship between Abundance and Distribution of Species , 1984, The American Naturalist.

[17]  H. Nybom Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants , 2004, Molecular ecology.

[18]  R. Lande Genetics and demography in biological conservation. , 1988, Science.

[19]  R. Petit,et al.  Glacial Refugia: Hotspots But Not Melting Pots of Genetic Diversity , 2003, Science.

[20]  F. Bunnell,et al.  Conservation priorities for peripheral species: the example of British Columbia , 2004 .

[21]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[22]  F. Rousset genepop’007: a complete re‐implementation of the genepop software for Windows and Linux , 2008, Molecular ecology resources.

[23]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[24]  James B. Beck,et al.  DOES HYBRIDIZATION DRIVE THE TRANSITION TO ASEXUALITY IN DIPLOID BOECHERA? , 2012, Evolution; international journal of organic evolution.

[25]  Robert H. Whittaker,et al.  Vegetation of the Great Smoky Mountains , 1956 .

[26]  Pedro Jordano,et al.  Can Population Genetic Structure Be Predicted from Life‐History Traits? , 2007, The American Naturalist.

[27]  Emily Crowe,et al.  Conservation genetics of Pitcher's thistle (Cirsium pitcheri), an endangered Great Lakes endemic. , 2010 .

[28]  Peter Lesica,et al.  When Are Peripheral Populations Valuable for Conservation , 1995 .

[29]  Ary A. Hoffmann,et al.  A reassessment of genetic limits to evolutionary change , 2005 .

[30]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[31]  J. Stewart,et al.  Refugia revisited: individualistic responses of species in space and time , 2010, Proceedings of the Royal Society B: Biological Sciences.

[32]  Ashley B. Morris,et al.  Comparative phylogeography of unglaciated eastern North America , 2006, Molecular ecology.

[33]  S. Orsenigo,et al.  Effects of marginality on plant population performance , 2014 .

[34]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[35]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[36]  S. Gaines,et al.  The ‘abundant centre’ distribution: to what extent is it a biogeographical rule? , 2002 .

[37]  Rob Hengeveld,et al.  The distribution of abundance. I. Measurements , 1982 .

[38]  A. Bradshaw The Croonian Lecture, 1991. Genostasis and the limits to evolution. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  J. Freeland,et al.  Conservation genetics of Hill’s thistle (Cirsium hillii) , 2010 .

[40]  Biology and Ecology of the Platte Thistle (Cirsium canescens)1 , 1981 .

[41]  Christopher R. Herlihy,et al.  Demographic and population‐genetic tests provide mixed support for the abundant centre hypothesis in the endemic plant Leavenworthia stylosa , 2013, Molecular ecology.

[42]  A. Radosavljević,et al.  The influence of contemporary and historic landscape features on the genetic structure of the sand dune endemic, Cirsium pitcheri (Asteraceae) , 2014, Heredity.

[43]  Bridgett M. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2011, Conservation Genetics Resources.

[44]  C. Daly,et al.  A Statistical-Topographic Model for Mapping Climatological Precipitation over Mountainous Terrain , 1994 .

[45]  R. Petit,et al.  Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure , 2009, BMC Evolutionary Biology.

[46]  M. Kirkpatrick,et al.  Evolution of a Species' Range , 1997, The American Naturalist.

[47]  G. Hewitt The genetic legacy of the Quaternary ice ages , 2000, Nature.

[48]  Y. Ide,et al.  Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains , 2008 .

[49]  C. Eckert,et al.  Testing the abundant center model using range-wide demographic surveys of two coastal dune plants. , 2007, Ecology.