Density-dependent environments can select for extremes of body size

Body size variation is an enigma. We do not understand why species achieve the sizes they do, and this means we also do not understand the circumstances under which gigantism or dwarfism is selected. We develop size-structured integral projection models to explore evolution of body size and life history speed. We make few assumptions and keep models simple: all functions remain constant across models except for the one that describes development of body size with age. We set sexual maturity to occur when size attains 80% of the asymptotic size, which is typical of a large mammal, and allow negative density dependence to only affect either reproduction or juvenile survival. Fitness – the quantity that is maximized by adaptive evolution – is carrying capacity in our models, and we are consequently interested in how it changes with size at sexual maturity, and how this association varies with development rate. The simple models generate complex dynamics while providing insight into the circumstances when extremes of body size evolve. The direction of selection leading to either gigantism or dwarfism crucially depends on the proportion of the population that is sexually mature, which in turn depends on how the development function determines the survivorship schedule. The developmental trajectories consequently interact with size-specific survival or reproductive rates to determine the best life history and the optimal body size emerges from that interaction. These dynamics result in trade-offs between different components of the life history, with the form of the trade-off that emerges depending upon where in the life history density dependence operates most strongly. Empirical application of the approach we develop has potential to help explain the enigma of body size variation across the tree of life.

[1]  Julia A. Barthold,et al.  Demographic determinants of the phenotypic mother-offspring correlation , 2021 .

[2]  A. Dobson,et al.  Investigating the Dynamics of Elk Population Size and Body Mass in a Seasonal Environment Using a Mechanistic Integral Projection Model , 2020, The American Naturalist.

[3]  M. Czarnoleski,et al.  Coevolution of body size and metabolic rate in vertebrates: a life‐history perspective , 2020, Biological reviews of the Cambridge Philosophical Society.

[4]  S. Richards,et al.  Fish body sizes change with temperature but not all species shrink with warming , 2020, Nature Ecology & Evolution.

[5]  J. Gaillard,et al.  Life-history strategy varies with the strength of competition in a food-limited ungulate population. , 2020, Ecology letters.

[6]  S. Schreiber Positively and negatively autocorrelated environmental fluctuations have opposing effects on species coexistence , 2019, bioRxiv.

[7]  T. Coulson,et al.  The effect of insularity on avian growth rates and implications for insular body size evolution , 2019, Proceedings of the Royal Society B.

[8]  Tim Coulson,et al.  ENVIRONMENTAL PERTURBATIONS AND TRANSITIONS BETWEEN ECOLOGICAL AND EVOLUTIONARY EQUILIBRIA: AN ECO-EVOLUTIONARY FEEDBACK FRAMEWORK , 2019, bioRxiv.

[9]  D. R. Robertson,et al.  Fish reproductive-energy output increases disproportionately with body size , 2018, Science.

[10]  J. Goldbogen Physiological constraints on marine mammal body size , 2018, Proceedings of the National Academy of Sciences.

[11]  J. Gaillard,et al.  Causes and consequences of variation in offspring body mass: meta‐analyses in birds and mammals , 2018, Biological reviews of the Cambridge Philosophical Society.

[12]  J. Travis,et al.  Predicting coexistence in species with continuous ontogenetic niche shifts and competitive asymmetry. , 2017, Ecology.

[13]  R. Lande,et al.  Evolution of stochastic demography with life history tradeoffs in density-dependent age-structured populations , 2017, Proceedings of the National Academy of Sciences.

[14]  J. Travis,et al.  Predicting Coexistence in Species with Continuous Ontogenetic Niche Shifts and Competitive Asymmetry , 2017, bioRxiv.

[15]  Hal Caswell,et al.  Mechanistic description of population dynamics using dynamic energy budget theory incorporated into integral projection models , 2017 .

[16]  Julia A. Barthold,et al.  Modeling Adaptive and Non-adaptive Responses of Populations to Environmental Change , 2016, bioRxiv.

[17]  C. Ramsey,et al.  Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus) , 2016, Science.

[18]  Mark Rees,et al.  Data-driven Modelling of Structured Populations: A Practical Guide to the Integral Projection Model , 2016 .

[19]  D. Reznick,et al.  The effects of asymmetric competition on the life history of Trinidadian guppies , 2016, Ecology letters.

[20]  Stephen P. Ellner,et al.  Data-driven modelling of structured populations , 2016 .

[21]  Kathrin Abendroth,et al.  Evolution In Age Structured Populations , 2016 .

[22]  Shripad Tuljapurkar,et al.  Measuring selective constraint on fertility in human life histories , 2015, Proceedings of the National Academy of Sciences.

[23]  S. Engen,et al.  The concept of fitness in fluctuating environments. , 2015, Trends in ecology & evolution.

[24]  Joel Kingsolver,et al.  Evolutionary Change in Continuous Reaction Norms , 2014, The American Naturalist.

[25]  D. Reznick,et al.  Do Eco-Evo Feedbacks Help Us Understand Nature? Answers From Studies of the Trinidadian Guppy , 2014 .

[26]  Jean-Michel Gaillard,et al.  Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology , 2013, Ageing Research Reviews.

[27]  U. Steiner,et al.  Trading stages: Life expectancies in structured populations , 2012, Experimental Gerontology.

[28]  Tim Coulson,et al.  Integral projections models, their construction and use in posing hypotheses in ecology , 2012 .

[29]  T. Anker‐Nilssen,et al.  Exploring causal pathways in demographic parameter variation: path analysis of mark–recapture data , 2012 .

[30]  Si Tang,et al.  Stability criteria for complex ecosystems , 2011, Nature.

[31]  T. Clutton‐Brock,et al.  Lifetime growth in wild meerkats: incorporating life history and environmental factors into a standard growth model , 2011, Oecologia.

[32]  R. Covas Evolution of reproductive life histories in island birds worldwide , 2012, Proceedings of the Royal Society B: Biological Sciences.

[33]  Tim Coulson,et al.  Modeling Effects of Environmental Change on Wolf Population Dynamics, Trait Evolution, and Life History , 2011, Science.

[34]  H. Gunga,et al.  Biology of the sauropod dinosaurs: the evolution of gigantism , 2011, Biological reviews of the Cambridge Philosophical Society.

[35]  Shripad Tuljapurkar,et al.  Using evolutionary demography to link life history theory, quantitative genetics and population ecology , 2010, The Journal of animal ecology.

[36]  R. Freckleton,et al.  Testing the Janzen-Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree. , 2010, Ecology letters.

[37]  Stephen P Ellner,et al.  Coexistence of perennial plants: an embarrassment of niches. , 2010, Ecology letters.

[38]  Arpat Ozgul,et al.  The Dynamics of Phenotypic Change and the Shrinking Sheep of St. Kilda , 2009, Science.

[39]  J. Gaillard,et al.  From stochastic environments to life histories and back , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Bernt-Erik Sæther,et al.  An evolutionary maximum principle for density-dependent population dynamics in a fluctuating environment , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  T. White The role of food, weather and climate in limiting the abundance of animals , 2008, Biological reviews of the Cambridge Philosophical Society.

[42]  M. Rees,et al.  Evolution of flowering decisions in a stochastic, density-dependent environment , 2008, Proceedings of the National Academy of Sciences.

[43]  J. Gaillard,et al.  Senescence rates are determined by ranking on the fast-slow life-history continuum. , 2008, Ecology letters.

[44]  R. Major,et al.  The contribution of artificial nest experiments to understanding avian reproductive success: a review of methods and conclusions , 2008 .

[45]  Benjamin M Bolker,et al.  Trait-mediated interactions: influence of prey size, density and experience. , 2008, The Journal of animal ecology.

[46]  Shai Meiri,et al.  THE ISLAND RULE IN LARGE MAMMALS: PALEONTOLOGY MEETS ECOLOGY , 2006, Evolution; international journal of organic evolution.

[47]  U. Dieckmann,et al.  The adaptive dynamics of function-valued traits. , 2006, Journal of theoretical biology.

[48]  Sasha R. X. Dall,et al.  Estimating individual contributions to population growth: evolutionary fitness in ecological time , 2006, Proceedings of the Royal Society B: Biological Sciences.

[49]  Mark V. Lomolino,et al.  Body size evolution in insular vertebrates: generality of the island rule , 2005 .

[50]  Bas Kooijman,et al.  Dynamic Energy Budget Theory for Metabolic Organisation , 2005 .

[51]  D. Bellwood,et al.  Shortest recorded vertebrate lifespan found in a coral reef fish , 2005, Current Biology.

[52]  T. Clutton‐Brock,et al.  Predictors of reproductive cost in female Soay sheep , 2005 .

[53]  M. Benton,et al.  The evolution of large size: how does Cope's Rule work? , 2005, Trends in ecology & evolution.

[54]  H. J. Walker,et al.  The World's Smallest Vertebrate, Schindleria brevipinguis, A New Paedomorphic Species in the Family Schindleriidae (Perciformes: Gobioidei) , 2004 .

[55]  Geoffrey B. West,et al.  The predominance of quarter-power scaling in biology , 2004 .

[56]  Stephen P. Ellner,et al.  Evolution of size–dependent flowering in a variable environment: construction and analysis of a stochastic integral projection model , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  R. Wootton The evolution of life histories: Theory and analysis , 1993, Reviews in Fish Biology and Fisheries.

[58]  L. Kruuk,et al.  Explaining stasis: microevolutionary studies in natural populations , 2004, Genetica.

[59]  S. Ellner,et al.  Rapid evolution drives ecological dynamics in a predator–prey system , 2003, Nature.

[60]  J. Gaillard,et al.  Causes of sex‐biased adult survival in ungulates: sexual size dimorphism, mating tactic or environment harshness? , 2003 .

[61]  S. Clegg,et al.  The ‘island rule’ in birds: medium body size and its ecological explanation , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  L. Rowe,et al.  Developmental Thresholds and the Evolution of Reaction Norms for Age and Size at Life‐History Transitions , 2002, The American Naturalist.

[63]  U. Dieckmann,et al.  Evolutionary Optimisation Models and Matrix Games in the Unified Perspective of Adaptive Dynamics , 2002 .

[64]  N. Owen‐Smith,et al.  A metaphysiological modelling approach to stability in herbivore–vegetation systems , 2002 .

[65]  D. O. Logofet Matrix Population Models: Construction, Analysis, and Interpretation , 2002 .

[66]  J. M. Hoekstra,et al.  The Strength of Phenotypic Selection in Natural Populations , 2001, The American Naturalist.

[67]  E. Nol,et al.  LANDSCAPE AND FRAGMENT SIZE EFFECTS ON REPRODUCTIVE SUCCESS OF FOREST‐BREEDING BIRDS IN ONTARIO , 2000 .

[68]  J. Gaillard,et al.  Temporal Variation in Fitness Components and Population Dynamics of Large Herbivores , 2000 .

[69]  P. Chesson Mechanisms of Maintenance of Species Diversity , 2000 .

[70]  Alan Grafen,et al.  Formal Darwinism, the individual–as–maximizing–agent analogy and bet–hedging , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[71]  P. Turchin Population regulation : a synthetic view , 1999 .

[72]  T. Takada,et al.  Theorems on the invasion process in stage-structured populations with density-dependent dynamics , 1998 .

[73]  J. Gaillard,et al.  Variation in growth form and precocity at birth in eutherian mammals , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  James H. Brown,et al.  A General Model for the Origin of Allometric Scaling Laws in Biology , 1997, Science.

[75]  A. Grant Selection pressures on vital rates in density–dependent populations , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  J. Weiner,et al.  Interspecific Allometries Are by-Products of Body Size Optimization , 1997, The American Naturalist.

[77]  P. Taylor,et al.  Von Bertalanffy's Growth Equation Should Not Be Used to Model Age and Size at Maturity , 1997, The American Naturalist.

[78]  Hal Caswell,et al.  Estimation of Individual Fitness from Life-History Data , 1996, The American Naturalist.

[79]  Odo Diekmann,et al.  On evolutionarily stable life histories, optimization and the need to be specific about density dependence , 1995 .

[80]  F. Gulland,et al.  Ecology of Infectious Diseases in Natural Populations: Impact of Infectious Diseases on Wild Animal Populations: a Review , 1995 .

[81]  E. Charnov,et al.  A trade-off-invariant life-history rule for optimal offspring size , 1995, Nature.

[82]  T. Takada,et al.  An analysis of life history evolution in terms of the density-dependent Lefkovitch matrix model. , 1992, Mathematical biosciences.

[83]  D. Seip Factors limiting woodland caribou populations and their interrelationships with wolves and moose in southeastern British Columbia , 1992 .

[84]  J. Kozłowski Optimal allocation of resources to growth and reproduction: Implications for age and size at maturity. , 1992, Trends in ecology & evolution.

[85]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[86]  John A. Endler,et al.  Experimentally induced life-history evolution in a natural population , 1990, Nature.

[87]  Shripad Tuljapurkar,et al.  Population Dynamics in Variable Environments , 1990 .

[88]  D. Winkler,et al.  Offspring Size and Number: A Life History Model Linking Effort Per Offspring and Total Effort , 1987, The American Naturalist.

[89]  J. Hofbauer,et al.  Coexistence for systems governed by difference equations of Lotka-Volterra type , 1987, Journal of mathematical biology.

[90]  G. Parker,et al.  Optimal Egg Size and Clutch Size: Effects of Environment and Maternal Phenotype , 1986, The American Naturalist.

[91]  M. Hassell,et al.  Detecting density dependence. , 1986, Trends in ecology & evolution.

[92]  S. Stearns,et al.  THE EVOLUTION OF PHENOTYPIC PLASTICITY IN LIFE‐HISTORY TRAITS: PREDICTIONS OF REACTION NORMS FOR AGE AND SIZE AT MATURITY , 1986, Evolution; international journal of organic evolution.

[93]  R. Armstrong Resource Competition and Community Structure.David Tilman , 1984 .

[94]  D. Tilman Resource Competition and Community Structure. (MPB-17), Volume 17 , 2020 .

[95]  D. Reznick THE IMPACT OF PREDATION ON LIFE HISTORY EVOLUTION IN TRINIDADIAN GUPPIES: GENETIC BASIS OF OBSERVED LIFE HISTORY PATTERNS , 1982, Evolution; international journal of organic evolution.

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

[97]  D. Reznick THE IMPACT OF PREDATION ON LIFE HISTORY EVOLUTION IN , 1982 .

[98]  R. Law Optimal Life Histories Under Age-Specific Predation , 1979, The American Naturalist.

[99]  S. Stearns THE EVOLUTION OF LIFE * : . 4120 HISTORY TRAITS : A Critique of the Theory and a Review of the Data , 2008 .

[100]  B. Charlesworth Selection in populations with overlapping generations. VI. Rates of change of gene frequency and population growth rate. , 1974, Theoretical population biology.

[101]  Christopher C. Smith,et al.  The Optimal Balance between Size and Number of Offspring , 1974, The American Naturalist.

[102]  B. Charlesworth Selection in Populations with Overlapping Generations. V. Natural Selection and Life Histories , 1973, The American Naturalist.

[103]  B. McNab,et al.  On the Ecological Significance of Bergmann's Rule , 1971 .

[104]  R H Macarthur,et al.  SOME GENERALIZED THEOREMS OF NATURAL SELECTION. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

[105]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.