InSTREAM-Gen: Modelling eco-evolutionary dynamics of trout populations under anthropogenic environmental change

Current rates of environmental change are exceeding the capacity of many populations to adapt to new conditions and thus avoid demographic collapse and ultimate extinction. In particular, cold-water freshwater fish species are predicted to experience strong selective pressure from climate change and a wide range of interacting anthropogenic stressors in the near future. To implement effective management and conservation measures, it is crucial to quantify the maximum rate of change that cold-water freshwater fish populations can withstand. Here, we present a spatially explicit eco-genetic individual-based model, inSTREAM-Gen, to predict the eco-evolutionary dynamics of stream-dwelling trout under anthropogenic environmental change. The model builds on a well-tested demographic model, which includes submodels of river dynamics, bioenergetics, and adaptive habitat selection, with a new genetic module that allows exploration of genetic and life-history adaptations to new environments. The genetic module models the transmission of two key traits, size at emergence and maturity size threshold. We parameterized the model for a brown trout (Salmo trutta L.) population at the warmest edge of its range to validate it and analyze its sensitivity to parameters under contrasting thermal profiles. To illustrate potential applications of the model, we analyzed the population's demographic and evolutionary dynamics under scenarios of (1) climate change-induced warming, and (2) warming plus flow reduction resulting from climate and land use change, compared to (3) a baseline of no environmental change. The model predicted severe declines in density and biomass under climate warming. These declines were lower than expected at range margins because of evolution towards smaller size at both emergence and maturation compared to the natural evolution under the baseline conditions. Despite stronger evolutionary responses, declining rates were substantially larger under the combined warming and flow reduction scenario, leading to a high probability of population extinction over contemporary time frames. Therefore, adaptive responses could not prevent extinction under high rates of environmental change. Our model demonstrates critical elements of next generation ecological modelling aiming at predictions in a changing world as it accounts for spatial and temporal resource heterogeneity, while merging individual behaviour and bioenergetics with microevolutionary adaptations.

[1]  S. Railsback,et al.  Feeding modes in stream salmonid population models: is drift feeding the whole story? , 2013, Environmental Biology of Fishes.

[2]  S. Einum,et al.  Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  B. Jonsson,et al.  A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. , 2009, Journal of fish biology.

[4]  N. Barton,et al.  Multifactorial genetics: Understanding quantitative genetic variation , 2002, Nature Reviews Genetics.

[5]  Steven F. Railsback,et al.  InSTREAM: the individual-based stream trout research and environmental assessment model , 2009 .

[6]  Sylvia R. Esterby,et al.  Review of methods for the detection and estimation of trends with emphasis on water quality applications , 1996 .

[7]  D. Ayllón,et al.  Modelling brown trout spatial requirements through physical habitat simulations , 2010 .

[8]  Uta Berger,et al.  Making Predictions in a Changing World: The Benefits of Individual-Based Ecology , 2014, Bioscience.

[9]  Peter Kareiva,et al.  U.S. Natural Resources and Climate Change: Concepts and Approaches for Management Adaptation , 2009, Environmental management.

[10]  E. Meir,et al.  Time to Evolve? Potential Evolutionary Responses of Fraser River Sockeye Salmon to Climate Change and Effects on Persistence , 2011, PloS one.

[11]  Christina L. Tague,et al.  RHESSys: Regional Hydro-Ecologic Simulation System—An Object- Oriented Approach to Spatially Distributed Modeling of Carbon, Water, and Nutrient Cycling , 2004 .

[12]  J. Fremlin Predicting Population , 1972, Nature.

[13]  Philippe Baret,et al.  Simulating brown trout demogenetics in a river/nursery brook system: The individual-based model DemGenTrout , 2013 .

[14]  R. Lande,et al.  Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory , 2010, PLoS biology.

[15]  Max D. Morris,et al.  Factorial sampling plans for preliminary computational experiments , 1991 .

[16]  J. Rosenfeld Modelling the effects of habitat on self-thinning, energy equivalence, and optimal habitat structure for juvenile trout , 2014 .

[17]  R. Hirsch,et al.  Techniques of trend analysis for monthly water quality data , 1982 .

[18]  U. Dieckmann,et al.  Demographic and Evolutionary Consequences of Selective Mortality: Predictions from an Eco-Genetic Model for Smallmouth Bass , 2007 .

[19]  Jason Lowe,et al.  Quantifying the benefit of early climate change mitigation in avoiding biodiversity loss , 2013 .

[20]  J. M. Elliott Numerical changes and population regulation in young migratory trout Salmo trutta in a Lake District stream, 1966-83 , 1984 .

[21]  D. Ayllón,et al.  Thermal Carrying Capacity for a Thermally-Sensitive Species at the Warmest Edge of Its Range , 2013, PloS one.

[22]  Jennifer L. Hill,et al.  An Energetic Model of Microhabitat Use for Rainbow Trout and Rosyside Dace , 1993 .

[23]  Nicholas F. Hughes,et al.  Selection of Positions by Drift-Feeding Salmonids in Dominance Hierarchies: Model and Test for Arctic Grayling (Thymallus arcticus) in Subarctic Mountain Streams, Interior Alaska , 1992 .

[24]  U. Sommer,et al.  Global warming benefits the small in aquatic ecosystems , 2009, Proceedings of the National Academy of Sciences.

[25]  T. Höök,et al.  Eco-genetic model to explore fishing-induced ecological and evolutionary effects on growth and maturation schedules , 2009, Evolutionary applications.

[26]  Freshwater resources , 2022 .

[27]  Cyril Piou,et al.  Contrasting effects of climate change in continental vs. oceanic environments on population persistence and microevolution of Atlantic salmon , 2013, Global change biology.

[28]  S. Yue,et al.  The Mann-Kendall Test Modified by Effective Sample Size to Detect Trend in Serially Correlated Hydrological Series , 2004 .

[29]  D. Tallmon,et al.  Genetic change for earlier migration timing in a pink salmon population , 2012, Proceedings of the Royal Society B: Biological Sciences.

[30]  J. Post,et al.  Rapid depletion of genotypes with fast growth and bold personality traits from harvested fish populations , 2008, Proceedings of the National Academy of Sciences.

[31]  M. R. Evans,et al.  Modelling ecological systems in a changing world , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  Michael Frankfurter,et al.  Statistical Methods For Environmental Pollution Monitoring , 2016 .

[33]  Steven F Railsback,et al.  Trait-mediated trophic interactions: is foraging theory keeping up? , 2013, Trends in ecology & evolution.

[34]  Laëtitia Buisson,et al.  Climate‐induced changes in the distribution of freshwater fish: observed and predicted trends , 2013 .

[35]  Keith Brander,et al.  Quantitative approaches in climate change ecology , 2011, Global Change Biology.

[36]  S. Railsback,et al.  Contrast of Degraded and Restored Stream Habitat Using an Individual-Based Salmon Model , 2013 .

[37]  P. Baret,et al.  A review of ecological models for brown trout: towards a new demogenetic model , 2011 .

[38]  H. B. Mann Nonparametric Tests Against Trend , 1945 .

[39]  Michele Bellingeri,et al.  Consequences of extreme events on population persistence and evolution of a quantitative trait , 2012, Ecol. Informatics.

[40]  S. Leal Genetics and Analysis of Quantitative Traits , 2001 .

[41]  Volker Grimm,et al.  Using pattern-oriented modeling for revealing hidden information: a key for reconciling ecological theory and application , 2003 .

[42]  U. Dieckmann,et al.  The impact of fishing-induced mortality on the evolution of alternative life-history tactics in brook charr , 2008, Evolutionary applications.

[43]  M. Esteve,et al.  Observations of Spawning Behaviour in Salmoninae: Salmo, Oncorhynchus and Salvelinus , 2005, Reviews in Fish Biology and Fisheries.

[44]  R. O. Gilbert Statistical Methods for Environmental Pollution Monitoring , 1987 .

[45]  R. Huey,et al.  Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon , 2008, Evolutionary applications.

[46]  Andreas Focks,et al.  Towards better modelling and decision support: Documenting model development, testing, and analysis using TRACE , 2014 .

[47]  Uta Berger,et al.  Pattern-Oriented Modeling of Agent-Based Complex Systems: Lessons from Ecology , 2005, Science.

[48]  D. Ayllón,et al.  Ontogenetic and spatial variations in brown trout habitat selection , 2010 .

[49]  Successes, failures, and opportunities in the practical application of drift-foraging models , 2014, Environmental Biology of Fishes.

[50]  S. Vincenzi Extinction risk and eco-evolutionary dynamics in a variable environment with increasing frequency of extreme events , 2014, Journal of The Royal Society Interface.

[51]  Andrea Saltelli,et al.  An effective screening design for sensitivity analysis of large models , 2007, Environ. Model. Softw..

[52]  Volker Grimm,et al.  Ecological models supporting environmental decision making: a strategy for the future. , 2010, Trends in ecology & evolution.

[53]  Scott J. Goetz,et al.  Terrestrial and Inland Water Systems , 2014 .

[54]  Volker Grimm,et al.  Merging validation and evaluation of ecological models to ‘evaludation’: A review of terminology and a practical approach , 2014 .

[55]  H. Jager Individual variation in life history characteristics can influence extinction risk , 2001 .

[56]  Steven F. Railsback,et al.  Movement rules for individual-based models of stream fish , 1999 .

[57]  Latitude and altitude differentially shape life history trajectories between the sexes in non-anadromous brown trout , 2014, Evolutionary Ecology.

[58]  Tamara C. Grand,et al.  Physiological Ecology Meets the Ideal-free Distribution: Predicting the Distribution of Size-structured Fish Populations Across Temperature Gradients , 2000, Environmental Biology of Fishes.

[59]  Winfried Kurth,et al.  Facilitating Parameter Estimation and Sensitivity Analysis of Agent-Based Models: A Cookbook Using NetLogo and 'R' , 2014, J. Artif. Soc. Soc. Simul..

[60]  D. Schluter,et al.  Adaptation from standing genetic variation. , 2008, Trends in ecology & evolution.

[61]  Tomasz Wyszomirski,et al.  Modelling the role of social behavior in the persistence of the alpine marmot Marmota marmota , 2003 .

[62]  M. Mangel,et al.  Selective consequences of catastrophes for growth rates in a stream-dwelling salmonid , 2012, Oecologia.

[63]  J. Hutchings,et al.  Plastic and evolutionary responses to climate change in fish , 2014, Evolutionary applications.

[64]  D. Ayllón,et al.  Global warming threatens the persistence of Mediterranean brown trout , 2012 .

[65]  Steven F. Railsback,et al.  ANALYSIS OF HABITAT‐SELECTION RULES USING ANINDIVIDUAL‐BASED MODEL , 2002 .

[66]  S. Carlson,et al.  A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change , 2008, Evolutionary applications.

[67]  D. Ayllón,et al.  Modelling carrying capacity dynamics for the conservation and management of territorial salmonids , 2012 .

[68]  Richard J. Beckman,et al.  A Comparison of Three Methods for Selecting Values of Input Variables in the Analysis of Output From a Computer Code , 2000, Technometrics.

[69]  M. D. McKay,et al.  A comparison of three methods for selecting values of input variables in the analysis of output from a computer code , 2000 .

[70]  Birgit Müller,et al.  A standard protocol for describing individual-based and agent-based models , 2006 .

[71]  L. Crozier,et al.  Using Time Series Analysis to Characterize Evolutionary and Plastic Responses to Environmental Change: A Case Study of a Shift toward Earlier Migration Date in Sockeye Salmon , 2011, The American Naturalist.

[72]  Steven F. Railsback,et al.  Tests of Theory for Diel Variation in Salmonid Feeding Activity and Habitat Use , 2005 .

[73]  Steven F. Railsback,et al.  Individual-based modeling and ecology , 2005 .

[74]  B. Sheldon,et al.  Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations , 2013, PLoS biology.

[75]  J. Sanjay,et al.  Regional Climate Change Scenarios , 2017 .

[76]  Stewart J. Cohen,et al.  Climate Change 2014: Impacts,Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change , 2014 .

[77]  Cyril Piou,et al.  A demo-genetic individual-based model for Atlantic salmon populations: Model structure, parameterization and sensitivity , 2012 .

[78]  R. Nisbet,et al.  Predicting Population Dynamics from the Properties of Individuals: A Cross-Level Test of Dynamic Energy Budget Theory , 2013, The American Naturalist.

[79]  U. Dieckmann,et al.  Eco-genetic modeling of contemporary life-history evolution. , 2009, Ecological applications : a publication of the Ecological Society of America.

[80]  U. Dieckmann,et al.  Ecology: Managing Evolving Fish Stocks , 2007, Science.

[81]  Derek E. Lee,et al.  POPULATION‐LEVEL ANALYSIS AND VALIDATION OF AN INDIVIDUAL‐BASED CUTTHROAT TROUT MODEL , 2002 .

[82]  K. Fausch,et al.  Profitable stream positions for salmonids: relating specific growth rate to net energy gain , 1984 .

[83]  C. Azorín-Molina,et al.  Impact of climate and land use change on water availability and reservoir management: scenarios in the Upper Aragón River, Spanish Pyrenees. , 2014, The Science of the total environment.

[84]  L. Comte,et al.  Do stream fish track climate change? Assessing distribution shifts in recent decades , 2013 .

[85]  U. Netlogo Wilensky,et al.  Center for Connected Learning and Computer-Based Modeling , 1999 .

[86]  E. Garcia-Vazquez,et al.  Alternative mating strategies in Atlantic salmon and brown trout. , 2001, The Journal of heredity.

[87]  M. Mangel,et al.  Eco-evolutionary dynamics induced by massive mortality events. , 2014, Journal of fish biology.

[88]  B. Jonsson,et al.  Ecology of Atlantic Salmon and Brown Trout Habitat as a Template for Life Histories General Conclusions and Research Tasks , 2011 .

[89]  J. Gareth Polhill,et al.  The ODD protocol: A review and first update , 2010, Ecological Modelling.

[90]  David R. B. Stockwell,et al.  Forecasting the Effects of Global Warming on Biodiversity , 2007 .

[91]  Corey J A Bradshaw,et al.  Synergies among extinction drivers under global change. , 2008, Trends in ecology & evolution.