Can Evolution Supply What Ecology Demands?

A simplistic view of the adaptive process pictures a hillside along which a population can climb: when ecological 'demands' change, evolution 'supplies' the variation needed for the population to climb to a new peak. Evolutionary ecologists point out that this simplistic view can be incomplete because the fitness landscape changes dynamically as the population evolves. Geneticists meanwhile have identified complexities relating to the nature of genetic variation and its architecture, and the importance of epigenetic variation is under debate. In this review, we highlight how complexity in both ecological 'demands' and the evolutionary 'supply' influences organisms' ability to climb fitness landscapes that themselves change dynamically as evolution proceeds, and encourage new synthetic effort across research disciplines towards ecologically realistic studies of adaptation.

[1]  Dara Newman,et al.  INCREASED PROBABILITY OF EXTINCTION DUE TO DECREASED GENETIC EFFECTIVE POPULATION SIZE: EXPERIMENTAL POPULATIONS OF CLARKIA PULCHELLA , 1997, Evolution; international journal of organic evolution.

[2]  F. Guillaume.  MIGRATION‐INDUCED PHENOTYPIC DIVERGENCE: THE MIGRATION–SELECTION BALANCE OF CORRELATED TRAITS , 2011, Evolution; international journal of organic evolution.

[3]  L. Hurst,et al.  Parent–progeny sequencing indicates higher mutation rates in heterozygotes , 2015, Nature.

[4]  M. Whitlock,et al.  Inbreeding changes the shape of the genetic covariance matrix in Drosophila melanogaster. , 2001, Genetics.

[5]  Michael M. Desai,et al.  Sex Speeds Adaptation by Altering the Dynamics of Molecular Evolution , 2016, Nature.

[6]  A. Hoffmann,et al.  Limits to the adaptive potential of small populations , 2006 .

[7]  D. Roff,et al.  Do bottlenecks increase additive genetic variance? , 2011, Conservation Genetics.

[8]  Alan Hodgkinson,et al.  Variation in the mutation rate across mammalian genomes , 2011, Nature Reviews Genetics.

[9]  J. Stinchcombe,et al.  How much do genetic covariances alter the rate of adaptation? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[10]  Y. Wurm,et al.  Convergent Genetic Architecture Underlies Social Organization in Ants , 2014, Current Biology.

[11]  R. Lande.  QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY , 1979, Evolution; international journal of organic evolution.

[12]  Parental effects and the evolution of phenotypic memory , 2016, Journal of evolutionary biology.

[13]  W. Stephan.  Signatures of positive selection: from selective sweeps at individual loci to subtle allele frequency changes in polygenic adaptation , 2016, Molecular ecology.

[14]  R. Lanfear,et al.  Exploring the Relationships between Mutation Rates, Life History, Genome Size, Environment, and Species Richness in Flowering Plants , 2015, The American Naturalist.

[15]  E. H. Bryant,et al.  The Effect of an Experimental Bottleneck upon Quantitative Genetic Variation in the Housefly. , 1986, Genetics.

[16]  A. MacColl.  The ecological causes of evolution. , 2011, Trends in ecology & evolution.

[17]  C. Both.  Flexibility of Timing of Avian Migration to Climate Change Masked by Environmental Constraints En Route , 2010, Current Biology.

[18]  D. Haig,et al.  Specialists and generalists: the sexual ecology of the genome. , 2014, Cold Spring Harbor perspectives in biology.

[19]  M. Whitlock,et al.  EFFECTS OF MIGRATION ON THE GENETIC COVARIANCE MATRIX , 2007, Evolution; international journal of organic evolution.

[20]  Jeff Gore,et al.  A SLOWLY EVOLVING HOST MOVES FIRST IN SYMBIOTIC INTERACTIONS , 2011, Evolution; international journal of organic evolution.

[21]  S. Diamond,et al.  The spatial patterns of directional phenotypic selection. , 2013, Ecology letters.

[22]  A. Agrawal,et al.  Transgenerational defense induction and epigenetic inheritance in plants. , 2012, Trends in ecology & evolution.

[23]  R. Frankham,et al.  HOW CLOSELY CORRELATED ARE MOLECULAR AND QUANTITATIVE MEASURES OF GENETIC VARIATION? A META‐ANALYSIS , 2001, Evolution; international journal of organic evolution.

[24]  H. Kokko,et al.  Relaxed selection when you least expect it: why declining bird populations might fail to respond to phenological mismatches , 2015 .

[25]  T. Day,et al.  Nongenetic Inheritance and Its Evolutionary Implications , 2009 .

[26]  S. Lien,et al.  Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon , 2015, Nature.

[27]  E. Brodie,et al.  Historical Contingency in a Multigene Family Facilitates Adaptive Evolution of Toxin Resistance , 2016, Current Biology.

[28]  James M. Cheverud,et al.  GENETIC VARIATION IN PLEIOTROPY: DIFFERENTIAL EPISTASIS AS A SOURCE OF VARIATION IN THE ALLOMETRIC RELATIONSHIP BETWEEN LONG BONE LENGTHS AND BODY WEIGHT , 2007, Evolution; international journal of organic evolution.

[29]  Thomas E. Juenger,et al.  Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment , 2013 .

[30]  K. Koelle,et al.  Navigating the Devious Course of Evolution: The Importance of Mechanistic Models for Identifying Eco-Evolutionary Dynamics in Nature , 2013, The American Naturalist.

[31]  R. Lewontin,et al.  The Genetic Basis of Evolutionary Change , 2022 .

[32]  J. Wingfield,et al.  A supergene determines highly divergent male reproductive morphs in the ruff , 2015, Nature Genetics.

[33]  P. Grant,et al.  Demographic routes to variability and regulation in bird populations , 2016, Nature Communications.

[34]  V. Le Corre,et al.  Genetic variability at neutral markers, quantitative trait land trait in a subdivided population under selection. , 2003, Genetics.

[35]  E. Armbrust,et al.  Genome size differentiates co-occurring populations of the planktonic diatom Ditylum brightwellii (Bacillariophyta) , 2010, BMC Evolutionary Biology.

[36]  Pall I. Olason,et al.  Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers , 2015, Genome research.

[37]  Julie R. Etterson,et al.  Transgenerational Plasticity Is Adaptive in the Wild , 2007, Science.

[38]  M. Kirkpatrick,et al.  Chromosome inversions, adaptive cassettes and the evolution of species' ranges , 2015, Molecular ecology.

[39]  K. Wright,et al.  Indirect Evolution of Hybrid Lethality Due to Linkage with Selected Locus in Mimulus guttatus , 2013, PLoS biology.

[40]  J. Hofbauer,et al.  The adaptive advantage of phenotypic memory in changing environments. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[41]  L. Keller,et al.  A Y-like social chromosome causes alternative colony organization in fire ants , 2013, Nature.

[42]  C. Biémont.  A Brief History of the Status of Transposable Elements: from Junk Dna to Major Players in Evolution Transposable Elements as Components of Genetic Diversity , 2022 .

[43]  Benjamin A. Logsdon,et al.  Neutral Evolution of Multiple Quantitative Characters: A Genealogical Approach , 2007, Genetics.

[44]  Annalise B. Paaby,et al.  Cryptic genetic variation: evolution's hidden substrate , 2014, Nature Reviews Genetics.

[45]  B. Walsh,et al.  Abundant Genetic Variation + Strong Selection = Multivariate Genetic Constraints: A Geometric View of Adaptation , 2009 .

[46]  J. Mezey,et al.  Comparing G matrices: are common principal components informative? , 2003, Genetics.

[47]  G. Sella,et al.  Interpreting the Dependence of Mutation Rates on Age and Time , 2015, PLoS biology.

[48]  J. Minárovits,et al.  Epigenetic Regulation. , 2016, Advances in experimental medicine and biology.

[49]  C. Petropoulos,et al.  Epistasis and Pleiotropy Affect the Modularity of the Genotype–Phenotype Map of Cross-Resistance in HIV-1 , 2016, Molecular biology and evolution.

[50]  Maria Romano,et al.  Climate warming, ecological mismatch at arrival and population decline in migratory birds , 2011, Proceedings of the Royal Society B: Biological Sciences.

[51]  M. Feldman,et al.  GENETIC VARIATION AND THE EVOLUTION OF EPIGENETIC REGULATION , 2014, Evolution; international journal of organic evolution.

[52]  Marcel E Visser,et al.  Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? , 2009, The Journal of animal ecology.

[53]  E. Brodie,et al.  Environmental effects on the structure of the G‐matrix , 2015, Evolution; international journal of organic evolution.

[54]  Paul A Hohenlohe,et al.  Trait dimensionality explains widespread variation in local adaptation , 2015, Proceedings of the Royal Society B: Biological Sciences.

[55]  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.

[56]  Sonia Kéfi,et al.  Evolution of Local Facilitation in Arid Ecosystems , 2008, The American Naturalist.

[57]  M. Quail,et al.  The industrial melanism mutation in British peppered moths is a transposable element , 2016, Nature.

[58]  G. Coop,et al.  A Population Genetic Signal of Polygenic Adaptation , 2013, PLoS genetics.

[59]  H. Wichman,et al.  Evolutionary Feedback Mediated through Population Density, Illustrated with Viruses in Chemostats , 2005, The American Naturalist.

[60]  L. Kruuk,et al.  The danger of applying the breeder's equation in observational studies of natural populations , 2010, Journal of evolutionary biology.

[61]  H. Ellegren,et al.  Determinants of genetic diversity , 2016, Nature Reviews Genetics.

[62]  G. Wagner,et al.  The pleiotropic structure of the genotype–phenotype map: the evolvability of complex organisms , 2011, Nature Reviews Genetics.

[63]  James Mallet,et al.  A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies , 2006, PLoS biology.

[64]  A. Hendry,et al.  Eco-evolutionary dynamics , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[65]  Tobias Uller,et al.  Developmental plasticity and the evolution of parental effects. , 2008, Trends in ecology & evolution.

[66]  R. Whitlock.  Relationships between adaptive and neutral genetic diversity and ecological structure and functioning: a meta-analysis , 2014, The Journal of ecology.

[67]  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.

[68]  M. Skinner.  Environmental Epigenetics , 2015, Environmental epigenetics.

[69]  A. Ives,et al.  Rapid evolution, seasonality, and the termination of parasite epidemics. , 2009, Ecology.

[70]  B. Grant,et al.  A beak size locus in Darwin’s finches facilitated character displacement during a drought , 2016, Science.

[71]  R. Petit,et al.  Sex-biased dispersal promotes adaptive parental effects , 2010, BMC Evolutionary Biology.

[72]  R. Hoyle,et al.  When to rely on maternal effects and when on phenotypic plasticity? , 2015, Evolution; international journal of organic evolution.

[73]  S. Sultan,et al.  HOW STABLE ‘SHOULD’ EPIGENETIC MODIFICATIONS BE? INSIGHTS FROM ADAPTIVE PLASTICITY AND BET HEDGING , 2014, Evolution; international journal of organic evolution.

[74]  W. G. Hill,et al.  The effect of linkage on limits to artificial selection. , 1966, Genetical research.

[75]  Jay L. Lush,et al.  Animal Breeding Plans , 2008 .

[76]  Sasha R. X. Dall,et al.  The evolution of unconditional strategies via the 'multiplier effect'. , 2011, Ecology letters.

[77]  D. H. Reed,et al.  Inbreeding and extinction: Effects of rate of inbreeding , 2003, Conservation Genetics.

[78]  M. Lynch.  Mutation and Human Exceptionalism: Our Future Genetic Load , 2016, Genetics.

[79]  R. Hoyle,et al.  The benefits of maternal effects in novel and in stable environments , 2012, Journal of The Royal Society Interface.

[80]  H. Spencer,et al.  The adaptive invasion of epialleles in a heterogeneous environment. , 2013, Theoretical population biology.

[81]  Brian Charlesworth,et al.  The Effects of Deleterious Mutations on Evolution at Linked Sites , 2012, Genetics.

[82]  A. Hoffmann,et al.  Low Potential for Climatic Stress Adaptation in a Rainforest Drosophila Species , 2003, Science.

[83]  P M Visscher,et al.  A Localized Negative Genetic Correlation Constrains Microevolution of Coat Color in Wild Sheep , 2008, Science.

[84]  L. Duret,et al.  Comparative population genomics in animals uncovers the determinants of genetic diversity , 2014, Nature.

[85]  S. J. Arnold,et al.  STABILITY OF THE G‐MATRIX IN A POPULATION EXPERIENCING PLEIOTROPIC MUTATION, STABILIZING SELECTION, AND GENETIC DRIFT , 2003, Evolution; international journal of organic evolution.

[86]  Jianzhi Zhang,et al.  Genomic patterns of pleiotropy and the evolution of complexity , 2010, Proceedings of the National Academy of Sciences.

[87]  A. Hoffmann,et al.  Population Bottlenecks Increase Additive Genetic Variance But Do Not Break a Selection Limit in Rain Forest Drosophila , 2008, Genetics.

[88]  A. Tack,et al.  Spatial eco-evolutionary feedback in plant-pathogen interactions , 2014, European Journal of Plant Pathology.

[89]  M. Murray,et al.  All that's gold does not glitter , 2002 .

[90]  S. Yeaman.  Genomic rearrangements and the evolution of clusters of locally adaptive loci , 2013, Proceedings of the National Academy of Sciences.

[91]  T. Ohta.  Population size and rate of evolution , 1972, Journal of Molecular Evolution.

[92]  Joel G. Kingsolver,et al.  Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions , 2012, Evolutionary Ecology.

[93]  S. Yeaman,et al.  Regional heterogeneity and gene flow maintain variance in a quantitative trait within populations of lodgepole pine , 2006, Proceedings of the Royal Society B: Biological Sciences.

[94]  J. M. Comeron,et al.  The Hill–Robertson effect: evolutionary consequences of weak selection and linkage in finite populations , 2008, Heredity.

[95]  A. Barbadilla,et al.  Adaptive Evolution Is Substantially Impeded by Hill–Robertson Interference in Drosophila , 2015, Molecular biology and evolution.

[96]  J. McNamara,et al.  The Evolution of Transgenerational Integration of Information in Heterogeneous Environments , 2015, The American Naturalist.

[97]  Elizabeth P. Murchison,et al.  Rapid evolutionary response to a transmissible cancer in Tasmanian devils , 2016, Nature Communications.

[98]  O. Seehausen,et al.  Does eutrophication-driven evolution change aquatic ecosystems? , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[99]  J. Crow.  The genetic basis of evolutionary change , 1975 .

[100]  S. Yeaman.  Local Adaptation by Alleles of Small Effect* , 2015, The American Naturalist.

[101]  D. Houle,et al.  Measuring and comparing evolvability and constraint in multivariate characters , 2008, Journal of evolutionary biology.

[102]  R. Lande,et al.  Genetic Variation and Phenotypic Evolution During Allopatric Speciation , 1980, The American Naturalist.