Resurrecting complexity: the interplay of plasticity and rapid evolution in the multiple trait response to strong changes in predation pressure in the water flea Daphnia magna.

A resurrection ecology reconstruction of 14 morphological, life history and behavioural traits revealed that a natural Daphnia magna population rapidly tracked changes in fish predation by integrating phenotypic plasticity and widespread evolutionary changes both in mean trait values and in trait plasticity. Increased fish predation mainly generated rapid adaptive evolution of plasticity (especially in the presence of maladaptive ancestral plasticity) resulting in an important change in the magnitude and direction of the multivariate reaction norm. Subsequent relaxation of the fish predation pressure resulted in reversed phenotypic plasticity and mainly caused evolution of the trait means towards the ancestral pre-fish means. Relaxation from fish predation did, however, not result in a complete reversal to the ancestral fishless multivariate phenotype. Our study emphasises that the study population rapidly tracked environmental changes through a mosaic of plasticity, evolution of trait means and evolution of plasticity to generate integrated phenotypic changes in multiple traits.

[1]  R Gomulkiewicz,et al.  Adaptive phenotypic plasticity: consensus and controversy. , 1995, Trends in ecology & evolution.

[2]  Stuart R. Dennis,et al.  Phenotypic convergence along a gradient of predation risk , 2011, Proceedings of the Royal Society B: Biological Sciences.

[3]  W. Lampert,et al.  Exploitative competition in differently sized Daphnia species: a mechanistic explanation. , 1999 .

[4]  J. Conner QUANTITATIVE GENETIC APPROACHES TO EVOLUTIONARY CONSTRAINT: HOW USEFUL? , 2012, Evolution; international journal of organic evolution.

[5]  D. Post,et al.  Lake ecosystems: Rapid evolution revealed by dormant eggs , 1999, Nature.

[6]  R. Relyea MORPHOLOGICAL AND BEHAVIORAL PLASTICITY OF LARVAL ANURANS IN RESPONSE TO DIFFERENT PREDATORS , 2001 .

[7]  R. Tollrian,et al.  Morphological defences of invasive Daphnia lumholtzi protect against vertebrate and invertebrate predators , 2014 .

[8]  P. Gienapp,et al.  Climate change and evolution: disentangling environmental and genetic responses , 2008, Molecular ecology.

[9]  C. Schlichting,et al.  PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION , 2014, Evolution; international journal of organic evolution.

[10]  R. Lande Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation , 2009, Journal of evolutionary biology.

[11]  W. Gabriel,et al.  Optimal adult growth of Daphnia in a seasonal environment , 1993 .

[12]  David N. Reznick,et al.  Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments , 2007 .

[13]  A. Hendry,et al.  The evolution of phenotypic plasticity in response to anthropogenic disturbance , 2010 .

[14]  T. Mitchell-Olds,et al.  Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change , 2012, Proceedings of the Royal Society B: Biological Sciences.

[15]  D. Lodge,et al.  Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral , 2002 .

[16]  R. Tollrian,et al.  Alternative antipredator defences and genetic polymorphism in a pelagic predator–prey system , 1995, Nature.

[17]  B. Robinson Evolution of growth by genetic accommodation in Icelandic freshwater stickleback , 2013, Proceedings of the Royal Society B: Biological Sciences.

[18]  L. Rowe,et al.  THE EFFECTS OF PREDATION ON THE AGE AND SIZE OF MATURITY OF PREY , 1996, Evolution; international journal of organic evolution.

[19]  Dean C. Adams,et al.  A General Framework for the Analysis of Phenotypic Trajectories in Evolutionary Studies , 2009, Evolution; international journal of organic evolution.

[20]  A Forsman,et al.  Rethinking phenotypic plasticity and its consequences for individuals, populations and species , 2014, Heredity.

[21]  D. Adams,et al.  Analysis of two-state multivariate phenotypic change in ecological studies. , 2007, Ecology.

[22]  S. Dodson,et al.  Interactive effects of fish kairomone and light on Daphnia escape behavior , 1999 .

[23]  D. Blumstein,et al.  Relaxed selection in the wild. , 2009, Trends in ecology & evolution.

[24]  K. Moloney,et al.  Phenotypic plasticity of native vs. invasive purple loosestrife: a two-state multivariate approach. , 2007, Ecology.

[25]  L. De Meester,et al.  Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Mark van Kleunen,et al.  Constraints on the evolution of adaptive phenotypic plasticity in plants. , 2005, The New phytologist.

[27]  J. Gore,et al.  SLOWLY SWITCHING BETWEEN ENVIRONMENTS FACILITATES REVERSE EVOLUTION IN SMALL POPULATIONS , 2011, Evolution; international journal of organic evolution.

[28]  Alison Scoville,et al.  Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators , 2010, Proceedings of the National Academy of Sciences.

[29]  Andrew P Hendry,et al.  Climate change, adaptation, and phenotypic plasticity: the problem and the evidence , 2014, Evolutionary applications.

[30]  J. Colbourne,et al.  A millennial-scale chronicle of evolutionary responses to cultural eutrophication in Daphnia. , 2014, Ecology letters.

[31]  Jarrod D Hadfield,et al.  Differences in spawning date between populations of common frog reveal local adaptation , 2010, Proceedings of the National Academy of Sciences.

[32]  M. Pfrender,et al.  Rapid evolution in response to introduced predators I: rates and patterns of morphological and life-history trait divergence , 2007, BMC Evolutionary Biology.

[33]  Charles W Fox,et al.  Rapid Evolution of Egg Size in Captive Salmon , 2003, Science.

[34]  E. Werner,et al.  MECHANISMS CREATING COMMUNITY STRUCTURE ACROSS A FRESHWATER HABITAT GRADIENT , 1996 .

[35]  Christopher C. Wilmers,et al.  Human predators outpace other agents of trait change in the wild , 2009, Proceedings of the National Academy of Sciences.

[36]  G. Bell Fluctuating selection: the perpetual renewal of adaptation in variable environments , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  H. P. Riessen Costs of predator-induced morphological defences in Daphnia , 2012 .

[38]  H. P. Riessen,et al.  Predator-induced life history shifts in Daphnia : a synthesis of studies using meta-analysis , 1999 .

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

[40]  M. Boersma,et al.  Predator‐Mediated Plasticity in Morphology, Life History, and Behavior of Daphnia: The Uncoupling of Responses , 1998, The American Naturalist.