Investigating niche and lineage diversifi cation in widely distributed taxa: phylogeography and ecological niche modeling of the Peromyscus maniculatus species group

Th e relationship between lineage formation and variation in the ecological niche is a fundamental evolutionary question. Two prevailing hypotheses refl ect this relationship: niche conservatism and niche divergence. Niche conservatism predicts a pattern where sister taxa will occupy similar niche spaces; whereas niche divergence predicts that sister taxa will occupy diff erent niche spaces. Widely distributed species often show distinct phylogeographic structure, but little research has been conducted on how the environment may be related to these phylogenetic patterns. We investigated the relationship between lineage divergence and environmental space for the closely related species Peromyscus maniculatus and P. polionotus utilizing phylogenetic techniques and ecological niche modeling (ENM). We estimated the phylogenetic relationship among individuals based on complete cytochrome b sequences that represent individuals from a majority of the species ranges. Niche spaces that lineages occupy were estimated by using 12 environmental layers. Diff erences in niche space were tested using multivariate statistics based on location data, and ENMs were employed using maximum entropy algorithms. Two similarity indices estimated signifi cant divergence in environmental space based on the ENM. Six geographically structured lineages were identifi ed within P. maniculatus. Nested within P. maniculatus we found that P. polionotus recently diverged from a clade occupying central and western United States. We estimated that the majority of the genetic lineages occupy distinct environmental niches, which supports a pattern of niche divergence. Two sister taxa showed niche divergence and represent diff erent ecomorphs, suggesting morphological, genetic and ecological divergence between the two lineages. Two other sister taxa were observed in the same environmental space based on multivariate statistics, suggesting niche conservatism. Overall our results indicate that a widely distributed species may exhibit both niche conservatism and niche divergence, and that most lineages seem to occupy distinct environmental niches.

[1]  Jacob F. Degner,et al.  Population genetics and conservation of the threatened southeastern beach mouse (Peromyscus polionotus niveiventris): subspecies and evolutionary units , 2007, Conservation Genetics.

[2]  J. Layne,et al.  Advances in the study of Peromyscus (Rodentia) , 1989 .

[3]  M. Blouin,et al.  EVOLUTIONARY HISTORY OF THE NORTHERN LEOPARD FROG: RECONSTRUCTION OF PHYLOGENY, PHYLOGEOGRAPHY, AND HISTORICAL CHANGES IN POPULATION DEMOGRAPHY FROM MITOCHONDRIAL DNA , 2004, Evolution; international journal of organic evolution.

[4]  M. Tannenbaum,et al.  Differences in daily torpor patterns among three southeastern species ofPeromyscus , 1984, Journal of Comparative Physiology B.

[5]  A. Peterson,et al.  PREDICTING SPECIES' GEOGRAPHIC DISTRIBUTIONS BASED ON ECOLOGICAL NICHE MODELING , 2001 .

[6]  A. Templeton,et al.  Phylogeography of the common vampire bat (Desmodus rotundus): Marked population structure, Neotropical Pleistocene vicariance and incongruence between nuclear and mtDNA markers , 2009, BMC Evolutionary Biology.

[7]  C. Dormann,et al.  Evolution of climate niches in European mammals? , 2010, Biology Letters.

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

[9]  M. Siddall,et al.  Phylogeography of Diadophis punctatus: extensive lineage diversity and repeated patterns of historical demography in a trans-continental snake. , 2008, Molecular phylogenetics and evolution.

[10]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

[11]  E. Martínez‐Meyer,et al.  Phylogeographic analyses and paleodistribution modeling indicate pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. , 2009, Molecular biology and evolution.

[12]  Margaret E K Evans,et al.  Climate, Niche Evolution, and Diversification of the “Bird‐Cage” Evening Primroses (Oenothera, Sections Anogra and Kleinia) , 2008, The American Naturalist.

[13]  J. Elith,et al.  Species Distribution Models: Ecological Explanation and Prediction Across Space and Time , 2009 .

[14]  F. Burbrink,et al.  Lineage diversification in a widespread species: roles for niche divergence and conservatism in the common kingsnake, Lampropeltis getula , 2009, Molecular ecology.

[15]  K. Mcnyset Ecological niche conservatism in North American freshwater fishes , 2009 .

[16]  C. Aquadro,et al.  Mitochondrial DNA differentiation during the speciation process in Peromyscus. , 1983, Molecular biology and evolution.

[17]  J. Losos Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. , 2008, Ecology letters.

[18]  A. Townsend Peterson,et al.  Novel methods improve prediction of species' distributions from occurrence data , 2006 .

[19]  K. Rowe,et al.  Surviving the ice: Northern refugia and postglacial colonization. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  E. A. Mearns Revision of the Mice of the American Genus Peromyscus , 1909 .

[21]  A. Schmitz,et al.  Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. , 2005, Systematic biology.

[22]  Bryan C. Carstens,et al.  Phylogeography's past, present, and future: 10 years after Avise, 2000. , 2010, Molecular phylogenetics and evolution.

[23]  C. Graham,et al.  Niche Conservatism: Integrating Evolution, Ecology, and Conservation Biology , 2005 .

[24]  M. Westoby,et al.  Seed Size and Phylogeny in Six Temperate Floras: Constraints, Niche Conservatism, and Adaptation , 1995, The American Naturalist.

[25]  M. Wooten,et al.  Old mice, young islands and competing biogeographical hypotheses , 2007, Molecular ecology.

[26]  K. E. Moore,et al.  Phylogeography of the deer mouse (Peromyscus maniculatus) provides a predictive framework for research on hantaviruses. , 2006, The Journal of general virology.

[27]  C. Aquadro,et al.  EXTENSIVE GENETIC VARIATION IN MITOCHONDRIAL DNA'S AMONG GEOGRAPHIC POPULATIONS OF THE DEER MOUSE, PEROMYSCUS MANICULATUS , 1983, Evolution; international journal of organic evolution.

[28]  T. Miller Systematics and evolution , 1987 .

[29]  Stanley C. Wecker THE ROLE OF EARLY EXPERIENCE IN HABITAT SELECTION BY THE PRAIRIE DEER MOUSE, PEROMYSCUS MANICULATUS BAIRDI , 1963 .

[30]  A. Peterson,et al.  Effects of sample size on the performance of species distribution models , 2008 .

[31]  L. Rissler,et al.  Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). , 2007, Systematic biology.

[32]  P. Taberlet,et al.  Comparative phylogeography and postglacial colonization routes in Europe , 1998, Molecular ecology.

[33]  J. Elith,et al.  Sensitivity of predictive species distribution models to change in grain size , 2007 .

[34]  K. Nicholas,et al.  GeneDoc: Analysis and visualization of genetic variation , 1997 .

[35]  J A Swets,et al.  Measuring the accuracy of diagnostic systems. , 1988, Science.

[36]  M. Turelli,et al.  Environmental Niche Equivalency versus Conservatism: Quantitative Approaches to Niche Evolution , 2008, Evolution; international journal of organic evolution.

[37]  Xiaoguang Zheng,et al.  Historical demography and genetic structure of sister species: deermice (Peromyscus) in the North American temperate rain forest , 2003, Molecular ecology.

[38]  Campbell O. Webb,et al.  Phylogenies and Community Ecology , 2002 .

[39]  C. W. Kilpatrick,et al.  TAXONOMIC STATUS OF PEROMYSCUS BOYLII SACARENSIS: INFERENCES FROM DNA SEQUENCES OF THE MITOCHONDRIAL CYTOCHROME-B GENE , 2000 .

[40]  V. Sánchez‐Cordero,et al.  Conservatism of ecological niches in evolutionary time , 1999, Science.

[41]  T. Castoe,et al.  Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus). , 2004, Molecular phylogenetics and evolution.

[42]  J. Elith Quantitative Methods for Modeling Species Habitat: Comparative Performance and an Application to Australian Plants , 2000 .

[43]  Trevor Hastie,et al.  A statistical explanation of MaxEnt for ecologists , 2011 .

[44]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[45]  Richard E. Glor,et al.  Niche lability in the evolution of a Caribbean lizard community , 2003, Nature.

[46]  J. Wiens,et al.  DOES NICHE CONSERVATISM PROMOTE SPECIATION? A CASE STUDY IN NORTH AMERICAN SALAMANDERS , 2006, Evolution; international journal of organic evolution.

[47]  C. Graham,et al.  INTEGRATING PHYLOGENETICS AND ENVIRONMENTAL NICHE MODELS TO EXPLORE SPECIATION MECHANISMS IN DENDROBATID FROGS , 2004, Evolution; international journal of organic evolution.

[48]  T. Schoener The Anolis Lizards of Bimini: Resource Partitioning in a Complex Fauna , 1968 .

[49]  E. Gering,et al.  Molecular evolution of cytochrome b in high- and low-altitude deer mice (genus Peromyscus) , 2009, Heredity.

[50]  J. Neigel,et al.  Intraspecific Phylogeography: The Mitochondrial DNA Bridge Between Population Genetics and Systematics , 1987 .

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

[52]  The Mammals of North America , 1959 .

[53]  ohn,et al.  Delimiting Species Using DNA and Morphological Variation and Discordant Species Limits in Spiny Lizards ( Sceloporus ) , 2002 .

[54]  P. Hernandez,et al.  The effect of sample size and species characteristics on performance of different species distribution modeling methods , 2006 .

[55]  Miroslav Dudík,et al.  Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation , 2008 .

[56]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[57]  T. Clutton‐Brock,et al.  Wild Mammals of North America. , 1983 .

[58]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[59]  E. T. Hooper An Effect on the Peromyscus maniculatus Rassenkreis of Land Utilization in Michigan , 1942 .

[60]  L. Rockwood Introduction to population ecology , 2006 .

[61]  W. F. Blair ECOLOGICAL FACTORS IN SPECIATION OF PEROMYSCUS , 1950 .

[62]  C. Graham,et al.  Integrating GIS-based environmental data into evolutionary biology. , 2008, Trends in ecology & evolution.