Comparative landscape genetics of two pond‐breeding amphibian species in a highly modified agricultural landscape

Evaluating fine‐scale population structure of multiple species in the same landscape increases our ability to identify common patterns as well as discern ecological differences among species’ landscape genetic relationships. In the Palouse bioregion of northern Idaho, USA, 99% of the native prairie has been converted to nonirrigated agriculture and exotic grasslands. Columbia spotted frogs (Rana luteiventris) and long‐toed salamanders (Ambystoma macrodactylum) in this area breed almost entirely in artificial ponds on private land. We used genetic distances (FST and Dc) derived from eight microsatellite loci in 783 samples to evaluate the relationships among sympatric breeding populations (N = 20 and 26) of these species in a 213‐km2 landscape. Both species showed a pattern of isolation by distance that was not improved when distance was measured along drainages instead of topographically corrected straight lines (P < 0.01). After testing for autocorrelation among genetic distances, we used an information theoretic approach to model landscape resistance based on slope, soil type, solar insolation, and land cover, and multi‐model inference to rank the resistance of landscape surfaces to dispersal (represented by genetic distance). For both species, urban and rural developed land cover provided the highest landscape resistances. Resistance values for long‐toed salamanders followed a moisture gradient where forest provided the least resistance, while agriculture and shrub/clearcut provided the least resistance for Columbia spotted frogs. Comparative landscape genetics can be a powerful tool for detecting similarities and differences between codistributed species, and resulting models can be used to predict species‐specific responses to landscape change.

[1]  W. K. Savage,et al.  Novel Jefferson salamander, Ambystoma jeffersonianum, microsatellite DNA markers detect population structure and hybrid complexes , 2003 .

[2]  M Slatkin,et al.  A measure of population subdivision based on microsatellite allele frequencies. , 1995, Genetics.

[3]  Magnus Wang,et al.  The impact of habitat fragmentation and social structure on the population genetics of roe deer (Capreolus capreolus L.) in Central Europe , 2001, Heredity.

[4]  R. Shine,et al.  Abiotic and biotic influences on the dispersal behavior of metamorph cane toads (Bufo marinus) in tropical Australia. , 2008, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[5]  R. M’Closkey,et al.  Species richness patterns of amphibians in southwestern Ontario ponds , 1998 .

[6]  A. Storfer,et al.  Landscape genetics of high mountain frog metapopulations , 2010, Molecular ecology.

[7]  John T. Beneski,et al.  DEMOGRAPHY AND MIGRATORY PATTERNS OF THE EASTERN LONG-TOED SALAMANDER, , 1986 .

[8]  Rong-Cai Yang,et al.  A LIKELIHOOD‐BASED APPROACH TO ESTIMATING AND TESTING FOR ISOLATION BY DISTANCE , 2004, Evolution; international journal of organic evolution.

[9]  Samuel A. Cushman,et al.  Effects of habitat loss and fragmentation on amphibians: A review and prospectus , 2006 .

[10]  T. Hels,et al.  The effect of road kills on amphibian populations , 2001 .

[11]  Pierre Legendre,et al.  An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model , 1999 .

[12]  F. Rousset,et al.  ARE PARTIAL MANTEL TESTS ADEQUATE? , 2001, Evolution; international journal of organic evolution.

[13]  J. Gibbs,et al.  Amphibian production in forested landscapes in relation to wetland hydroperiod: A case study of vernal pools and beaver ponds , 2009 .

[14]  M. Blouin,et al.  Genetic structure in a montane ranid frog: restricted gene flow and nuclear–mitochondrial discordance , 2003, Molecular ecology.

[15]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[16]  S. Harris,et al.  Predation of wildlife by domestic cats Felis catus in Great Britain , 2003 .

[17]  A. Storfer,et al.  Influence of life‐history variation on the genetic structure of two sympatric salamander taxa , 2009, Molecular ecology.

[18]  N. Scott,et al.  Terrestrial activity and conservation of adult California red-legged frogs Rana aurora draytonii in coastal forests and grasslands , 2003 .

[19]  S. J. Arnold,et al.  Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[20]  Raymond D. Semlitsch,et al.  Differentiating Migration and Dispersal Processes for Pond-Breeding Amphibians , 2008 .

[21]  P. G. Demaynadier,et al.  Forest canopy closure and juvenile emigration by pool-breeding amphibians in Maine , 1999 .

[22]  J. Burger,et al.  Relationships among Isolated Wetland Size, Hydroperiod, and Amphibian Species Richness: Implications for Wetland Regulations , 2000 .

[23]  J. Gibbons,et al.  Habitat Selection and Movement of Pond-Breeding Amphibians in Experimentally Fragmented Pine Forests , 2008 .

[24]  K. Foresman,et al.  LONG-TOED SALAMANDERS IN HARVESTED AND INTACT DOUGLAS-FIR FORESTS OF WESTERN MONTANA , 2000 .

[25]  L. Knowles,et al.  Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence , 2009, Molecular ecology.

[26]  R. Lawson,et al.  Patterns of Population Subdivision and Gene Flow in Three Sympatric Natricine Snakes , 2001, Copeia.

[27]  F. Moore,et al.  Population structure of spotted salamanders (Ambystoma maculatum) in a fragmented landscape , 2009, Molecular ecology.

[28]  W. K. Savage,et al.  Landcover predicts isolation in Ambystoma salamanders across region and species , 2009 .

[29]  J. Goudet.  FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics , 1995 .

[30]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[31]  D. Marsh,et al.  Metapopulation Dynamics and Amphibian Conservation , 2001 .

[32]  P. Hedrick.  A STANDARDIZED GENETIC DIFFERENTIATION MEASURE , 2005, Evolution; international journal of organic evolution.

[33]  P. Verrell,et al.  Demography and reproductive ecology of the Columbia spotted frog (Rana luteiventris) across the Palouse , 2005 .

[34]  L. Waits,et al.  Putting the ‘landscape’ in landscape genetics , 2007, Heredity.

[35]  G. Gerlach,et al.  Fragmentation of Landscape as a Cause for Genetic Subdivision in Bank Voles , 2000 .

[36]  L. Waits,et al.  Using habitat models to determine conservation priorities for pond-breeding amphibians in a privately-owned landscape of northern Idaho, USA , 2009 .

[37]  C. Goldberg,et al.  From the frog's mouth: Buccal swabs for collection of DNA from amphibians , 2003 .

[38]  M. Fortin,et al.  Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis , 2010, Molecular ecology.

[39]  K. Selkoe,et al.  Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species , 2010, Molecular ecology.

[40]  M. Knutson,et al.  Effects of Landscape Composition and Wetland Fragmentation on Frog and Toad Abundance and Species Richness in Iowa and Wisconsin, U.S.A. , 1999 .

[41]  B. Grant,et al.  Comparative landscape genetics and the adaptive radiation of Darwin's finches: the role of peripheral isolation , 2005, Molecular ecology.

[42]  P. Meirmans.  USING THE AMOVA FRAMEWORK TO ESTIMATE A STANDARDIZED GENETIC DIFFERENTIATION MEASURE , 2006, Evolution; international journal of organic evolution.

[43]  R. D. Semlitsch,et al.  Grasslands as movement barriers for a forest-associated salamander: Migration behavior of adult and juvenile salamanders at a distinct habitat edge , 2006 .

[44]  T. Beebee,et al.  Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation , 1997, Heredity.

[45]  James P. Gibbs,et al.  Amphibian Movements in Response to Forest Edges, Roads, and Streambeds in Southern New England , 1998 .

[46]  K. Pope,et al.  A Telemetric Study of the Movement Patterns and Habitat Use of Rana muscosa, the Mountain Yellow-legged Frog, in a High-elevation Basin in Kings Canyon National Park, California , 1999 .

[47]  Max Nielsen-Pincus,et al.  Predicting land use change: comparison of models based on landowner surveys and historical land cover trends , 2008, Landscape Ecology.

[48]  Jean Thioulouse,et al.  The ade4 package - I : One-table methods , 2004 .

[49]  R. D. Semlitsch,et al.  The Role of Microhabitats in the Desiccation and Survival of Anurans in Recently Harvested Oak–Hickory Forest , 2008, Copeia.

[50]  R. G. Wright,et al.  Amphibian habitat preferences among artificial ponds in the Palouse region of northern Idaho , 1999 .

[51]  M. Hunter,et al.  Amphibian Distributions in a Landscape of Forests and Agriculture: an Examination of Landscape Composition and Conf iguration , 2002 .

[52]  D. A. Patrick,et al.  Effects of Timber Harvest on Amphibian Populations: Understanding Mechanisms from Forest Experiments , 2009 .

[53]  Craig Moritz,et al.  Comparative phylogeography: concepts and applications , 1998 .

[54]  E. Petit,et al.  Quantifying genotyping errors in noninvasive population genetics , 2004, Molecular ecology.

[55]  C. Haddad.  Amphibian Declines: The Conservation Status of United States Species , 2008, Copeia.

[56]  J. Corander,et al.  Bayesian identification of admixture events using multilocus molecular markers , 2006, Molecular Ecology.

[57]  T. Beebee,et al.  A microsatellite analysis of natterjack toad, Bufo calamita, metapopulations , 2000 .

[58]  Samuel A. Cushman,et al.  Gene Flow in Complex Landscapes: Testing Multiple Hypotheses with Causal Modeling , 2006, The American Naturalist.

[59]  F. Allendorf,et al.  Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape , 2005, Molecular ecology.

[60]  David B. Lindenmayer,et al.  A comparison of constructed and natural habitat for frog conservation in an Australian agricultural landscape , 2004 .

[61]  S. Funk,et al.  Ecological factors influence population genetic structure of European grey wolves , 2006, Molecular ecology.

[62]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: dominant markers and null alleles , 2007, Molecular ecology notes.

[63]  C. Schlötterer,et al.  microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets , 2003 .

[64]  Anne E. Black,et al.  Land use history at multiple scales: implications for conservation planning , 1998 .

[65]  Paul Beier,et al.  Circuit theory predicts gene flow in plant and animal populations , 2007, Proceedings of the National Academy of Sciences.

[66]  Marie-Josée Fortin,et al.  Utility of computer simulations in landscape genetics , 2010, Molecular ecology.

[67]  Jinliang Wang,et al.  Sibship reconstruction from genetic data with typing errors. , 2004, Genetics.

[68]  Pierre Taberlet,et al.  Landscape genetics: combining landscape ecology and population genetics , 2003 .

[69]  Yves Van de Peer,et al.  zt: A Sofware Tool for Simple and Partial Mantel Tests , 2002 .

[70]  F. Allendorf,et al.  Genetic Differentiation among Long-Toed Salamander (Ambystoma macrodactylum) Populations , 2000, Copeia.

[71]  S. Kalinowski.  Evolutionary and statistical properties of three genetic distances , 2002, Molecular ecology.

[72]  D. Pilliod,et al.  Seasonal migration of Columbia spotted frogs (Rana luteiventris) among complementary resources in a high mountain basin , 2002 .

[73]  A. Chan-McLeod.  Factors affecting the permeability of clearcuts to red-legged frogs , 2003 .

[74]  L. Cavalli-Sforza,et al.  PHYLOGENETIC ANALYSIS: MODELS AND ESTIMATION PROCEDURES , 1967, Evolution; international journal of organic evolution.

[75]  Thomas Bäck.  An Empirical Comparison , 1996 .

[76]  Rob Roy Ramey,et al.  Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep , 2005 .

[77]  K. Babbitt,et al.  An experimental assessment of buffer width: Implications for salamander migratory behavior , 2009 .

[78]  Raymond J. Dezzani,et al.  Statistical approaches in landscape genetics: an evaluation of methods for linking landscape and genetic data , 2009 .

[79]  J. Cornuet,et al.  GENECLASS2: a software for genetic assignment and first-generation migrant detection. , 2004, The Journal of heredity.

[80]  L. Waits,et al.  Quantification and reduction of bias from sampling larvae to infer population and landscape genetic structure , 2010, Molecular ecology resources.

[81]  Takashi Asaeda,et al.  Heat storage of pavement and its effect on the lower atmosphere , 1996 .

[82]  Raymond D. Semlitsch,et al.  An Experimental Investigation of Landscape Resistance of Forest versus Old‐Field Habitats to Emigrating Juvenile Amphibians , 2002 .

[83]  N. Schtickzelle,et al.  Quantifying functional connectivity: experimental evidence for patch-specific resistance in the Natterjack toad (Bufo calamita) , 2004, Landscape Ecology.