Harnessing genomics for delineating conservation units.

Genomic data have the potential to revolutionize the delineation of conservation units (CUs) by allowing the detection of adaptive genetic variation, which is otherwise difficult for rare, endangered species. In contrast to previous recommendations, we propose that the use of neutral versus adaptive markers should not be viewed as alternatives. Rather, neutral and adaptive markers provide different types of information that should be combined to make optimal management decisions. Genetic patterns at neutral markers reflect the interaction of gene flow and genetic drift that affects genome-wide variation within and among populations. This population genetic structure is what natural selection operates on to cause adaptive divergence. Here, we provide a new framework to integrate data on neutral and adaptive markers to protect biodiversity.

[1]  Gordon Luikart,et al.  Next‐generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout , 2011, Molecular ecology resources.

[2]  W. Li,et al.  Maintenance of Genetic Variability under the Joint Effect of Mutation, Selection and Random Drift. , 1978, Genetics.

[3]  O. Gaggiotti,et al.  INVITED REVIEW: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity , 2006, Molecular ecology.

[4]  D. Demaster,et al.  Rethinking the Stock Concept: A Phylogeographic Approach , 1992 .

[5]  H. Ellegren,et al.  A guide to the genomics of ecological speciation in natural animal populations. , 2011, Ecology letters.

[6]  P Taberlet,et al.  A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation , 2007, Molecular ecology.

[7]  Michael A. Thomas,et al.  Genomics for the ecological toolbox. , 2004, Trends in ecology & evolution.

[8]  Joseph K. Pickrell,et al.  The Role of Geography in Human Adaptation , 2009, PLoS genetics.

[9]  C. Baer,et al.  Population genomics: genome-wide sampling of insect populations. , 2001, Annual review of entomology.

[10]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[11]  S. Kalinowski.  How well do evolutionary trees describe genetic relationships among populations? , 2009, Heredity.

[12]  P. Taberlet,et al.  The power and promise of population genomics: from genotyping to genome typing , 2003, Nature Reviews Genetics.

[13]  J. Haldane.  A mathematical theory of natural and artificial selection. (Part VI, Isolation.) , 1930, Mathematical Proceedings of the Cambridge Philosophical Society.

[14]  Michele R. Dudash,et al.  Predicting the Probability of Outbreeding Depression , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[15]  M. Gilpin,et al.  Metapopulation Biology: Ecology, Genetics, and Evolution , 1997 .

[16]  John C. Avise,et al.  Molecular Markers, Natural History and Evolution , 1993, Springer US.

[17]  Gordon Luikart,et al.  Landscape Genomics: A Brief Perspective , 2010 .

[18]  O. Gaggiotti,et al.  A Genome-Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective , 2008, Genetics.

[19]  O. Gaggiotti,et al.  Quantifying population structure using the F‐model , 2010, Molecular ecology resources.

[20]  S. Narum,et al.  Comparison of FST outlier tests for SNP loci under selection , 2011, Molecular ecology resources.

[21]  Joseph K. Pickrell,et al.  The Genetics of Human Adaptation: Hard Sweeps, Soft Sweeps, and Polygenic Adaptation , 2010, Current Biology.

[22]  A. Meyer,et al.  Adaptation in the age of ecological genomics: insights from parallelism and convergence. , 2011, Trends in ecology & evolution.

[23]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.

[24]  John C. Avise,et al.  Molecular Markers, Natural History, and Evolution , 1993 .

[25]  C. Moritz.  Defining 'Evolutionarily Significant Units' for conservation. , 1994, Trends in ecology & evolution.

[26]  Nicholas Stiffler,et al.  Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags , 2010, PLoS genetics.

[27]  M. Salemi,et al.  The phylogenetic handbook : a practical approach to DNA and protein phylogeny , 2003 .

[28]  VARIATION IN RESISTANCE AND VIRULENCE IN THE INTERACTION BETWEEN ARABIDOPSIS THALIANA AND A BACTERIAL PATHOGEN , 2006, Evolution; international journal of organic evolution.

[29]  Antonis Rokas,et al.  Harnessing genomics for evolutionary insights. , 2009, Trends in ecology & evolution.

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

[31]  J. Beaulieu,et al.  Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce , 2008, Molecular ecology.

[32]  G. Luikart,et al.  SNPs in ecology, evolution and conservation , 2004 .

[33]  S. Harrison,et al.  “How Local Is Local?”—A Review of Practical and Conceptual Issues in the Genetics of Restoration , 2005 .

[34]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[35]  LOCAL ADAPTATION, PATTERNS OF SELECTION, AND GENE FLOW IN THE CALIFORNIAN SERPENTINE SUNFLOWER (HELIANTHUS EXILIS) , 2006, Evolution; international journal of organic evolution.

[36]  Detlef Weigel,et al.  Genome‐wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies , 2010, Molecular ecology.

[37]  Mandy J. Haldane,et al.  A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation , 1927, Mathematical Proceedings of the Cambridge Philosophical Society.

[38]  E. Ostrander,et al.  Genomics and conservation genetics. , 2006, Trends in ecology & evolution.

[39]  T. Glenn.  Field guide to next‐generation DNA sequencers , 2011, Molecular ecology resources.

[40]  J. McKay,et al.  Adaptive population divergence: markers, QTL and traits , 2002 .

[41]  R. Frankham.  Challenges and opportunities of genetic approaches to biological conservation. , 2010 .

[42]  P. Phillips,et al.  Using Population Genomics to Detect Selection in Natural Populations: Key Concepts and Methodological Considerations , 2010, International Journal of Plant Sciences.

[43]  R. DeSalle,et al.  Diagnosing Units of Conservation Management , 1994 .

[44]  S. Edmands.  Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management , 2006, Molecular ecology.

[45]  Montgomery Slatkin,et al.  Gene Flow in Natural Populations , 1985 .

[46]  John C. Avise,et al.  Molecular Markers, Natural History and Evolution , 1993, Springer US.

[47]  R. Waples.  Pacific Salmon, Oncorhynchus spp., and the Definition of "Species" Under the Endangered Species Act , 1991 .

[48]  Catherine A. Wilson,et al.  Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[49]  T. Saitoh,et al.  The gap between the concept and definitions in the Evolutionarily Significant Unit: the need to integrate neutral genetic variation and adaptive variation , 2007, Ecological Research.

[50]  G. Luikart,et al.  Genomics and the future of conservation genetics , 2010, Nature Reviews Genetics.

[51]  D. Balding,et al.  Identifying adaptive genetic divergence among populations from genome scans , 2004, Molecular ecology.

[52]  J. Slate,et al.  Adaptation genomics: the next generation. , 2010, Trends in ecology & evolution.

[53]  Aurélie Bonin,et al.  Population genomics: a new generation of genome scans to bridge the gap with functional genomics , 2008, Molecular ecology.

[54]  O. Ryder.  Species conservation and systematics: the dilemma of subspecies , 1986 .

[55]  J. F. Storz,et al.  INVITED REVIEW: Using genome scans of DNA polymorphism to infer adaptive population divergence , 2005, Molecular ecology.

[56]  François Pompanon,et al.  Population Adaptive Index: a New Method to Help Measure Intraspecific Genetic Diversity and Prioritize Populations for Conservation , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[57]  K. Crandall,et al.  Considering evolutionary processes in conservation biology. , 2000, Trends in ecology & evolution.

[58]  Arnaud Estoup,et al.  Geneland: a computer package for landscape genetics , 2005 .

[59]  David Reznick,et al.  THE IMPACT OF PREDATION ON LIFE HISTORY EVOLUTION IN TRINIDADIAN GUPPIES (POECILIA RETICULATA) , 1982, Evolution; international journal of organic evolution.

[60]  M. Fortin,et al.  Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field , 2010, Molecular ecology.

[61]  M. Rockman.  THE QTN PROGRAM AND THE ALLELES THAT MATTER FOR EVOLUTION: ALL THAT'S GOLD DOES NOT GLITTER , 2012, Evolution; international journal of organic evolution.

[62]  A. Guggisberg,et al.  RAD in the realm of next‐generation sequencing technologies , 2011, Molecular ecology.

[63]  R. Butlin,et al.  Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers , 2001 .

[64]  J. Beaulieu,et al.  Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce , 2011, Molecular ecology.

[65]  C. Moritz.  CONSERVATION UNITS AND TRANSLOCATIONS : STRATEGIES FOR CONSERVING EVOLUTIONARY PROCESSES , 2004 .

[66]  M Raymond,et al.  Testing differentiation in diploid populations. , 1996, Genetics.

[67]  Felix Gugerli,et al.  Adaptive vs. neutral genetic diversity: implications for landscape genetics , 2006, Landscape Ecology.

[68]  J. Bergelson,et al.  VARIATION IN RESISTANCE AND VIRULENCE IN THE INTERACTION BETWEEN ARABIDOPSIS THALIANA AND A BACTERIAL PATHOGEN , 2006, Evolution; international journal of organic evolution.

[69]  F. Allendorf,et al.  Identification of management units using population genetic data. , 2007, Trends in ecology & evolution.

[70]  P. Legendre,et al.  Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina , 2010, Molecular ecology.

[71]  S. Joost,et al.  Spatial analysis method (sam): a software tool combining molecular and environmental data to identify candidate loci for selection , 2008, Molecular ecology resources.

[72]  L. Bernatchez,et al.  Adaptive evolutionary conservation: towards a unified concept for defining conservation units , 2001, Molecular ecology.

[73]  Joy Bergelson,et al.  References and Notes Supporting Online Material Adaptation to Climate across the Arabidopsis Thaliana Genome , 2022 .