Opportunistic datasets perform poorly in Ecological Niche Modelling: a case study from a polymorphic lizard

ABSTRACT Context. Among processes involved in colour polymorphism, geographic variation in morph composition and frequency has been attracting interest since it reflects morph local adaptation. A recent study in the Pyrenees associated the pattern of geographic variation in morph frequency of the common wall lizard with the divergence in climatic niches, supporting the hypothesis that morphs represent alternative local climatic adaptations. However, the Pyrenees represent only a small portion of the species range. Aims. We modelled the ecological niches of Italian morphs using the same procedure adopted for the Pyrenees to check whether the effects detected at local scales (i.e. the Pyrenees) were repeatable at regional scales (i.e. Italy). This generalisation is needed to investigate how natural selection maintains locally adapted polymorphisms. Methods. We classified each locality (120 populations) according to the presence/absence of morphs, and independent Ecological Niche Models (ENMs) against the same background were fitted. Receiver Operating Curves accounting for sampling biases, equivalency and similarity tests were used to check and compare models accounting for spatial distribution of data. Key results. Morph-specific ENMs did not reproduce any of the patterns detected in the Pyrenees. Any difference among morphs disappeared after controlling for morph spatial distribution. Since occurrence points of the rarest morphs were a subsample of the occurrence points of the most common morph, it is not possible to separate the effects of true ecological differences among morphs from the effects of the spatial distribution patterns of morph occurrence. Conclusions. Using presence data not specifically collected for ENM comparisons does not allow reliable assessments of morph niche segregation. Our analysis points out the need to be very cautious in ecological interpretations of ENMs built on presence/background or presence-only data when occurrences are spatially nested. Implications. When dealing with data not specifically collected according to a targeted design, it is not legitimate to compare ENMs with completely nested occurrence points, because this approach can not exclude the possibility that ENM differences were the result of a spatial subsampling. This type of bias is probably largely underestimated, and it may lead to serious misinterpretations as shown in this study.

[1]  R. Sacchi,et al.  Morph-specific seasonal variation of aggressive behaviour in a polymorphic lizard species , 2020, PeerJ.

[2]  R. Halvorsen,et al.  Bunching up the background betters bias in species distribution models , 2019, Ecography.

[3]  R. Sacchi,et al.  Morph-specific protein patterns in the femoral gland secretions of a colour polymorphic lizard , 2019, Scientific Reports.

[4]  T. Uller,et al.  Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard , 2018, Proceedings of the National Academy of Sciences.

[5]  J. Lenoir,et al.  Incorporating microclimate into species distribution models , 2018, Ecography.

[6]  N. Sillero,et al.  Climate suggests environment‐dependent selection on lizard colour morphs , 2018, Journal of Biogeography.

[7]  M. Carretero,et al.  Partial divergence in microhabitat use suggests environmental-dependent selection on a colour polymorphic lizard , 2018, Behavioral Ecology and Sociobiology.

[8]  R. Froissart,et al.  Experimental demonstration of the impact of hard and soft selection regimes on polymorphism maintenance in spatially heterogeneous environments † , 2018, Evolution; international journal of organic evolution.

[9]  J. Paterson,et al.  Male throat colour polymorphism is related to differences in space use and in habitat selection in tree lizards , 2018, Journal of Zoology.

[10]  B. Sinervo,et al.  Evolutionary games, climate and the generation of diversity , 2017, PLoS ONE.

[11]  R. Sacchi,et al.  Effects of Colour Morph and Temperature on Immunity in Males and Females of the Common Wall Lizard , 2017, Evolutionary Biology.

[12]  E. Svensson.  Back to basics: using colour polymorphisms to study evolutionary processes , 2017, Molecular ecology.

[13]  E. Font,et al.  Intensity of male‐male competition predicts morph diversity in a color polymorphic lizard , 2017, Evolution; international journal of organic evolution.

[14]  Matthew E. Aiello-Lammens,et al.  Improving niche and range estimates with Maxent and point process models by integrating spatially explicit information , 2016 .

[15]  R. Sacchi,et al.  Common Wall Lizard Females (Podarcis muralis) do not Actively Choose Males Based on their Colour Morph , 2015 .

[16]  M. Wand.  Functions for Kernel Smoothing Supporting Wand & Jones (1995) , 2015 .

[17]  S. Nielsen,et al.  Accounting for spatially biased sampling effort in presence‐only species distribution modelling , 2015 .

[18]  Brendan A. Wintle,et al.  Is my species distribution model fit for purpose? Matching data and models to applications , 2015 .

[19]  D. Stuart-Fox,et al.  Geographic variation in animal colour polymorphisms and its role in speciation , 2014, Biological reviews of the Cambridge Philosophical Society.

[20]  M. Wellenreuther,et al.  Sexual selection and genetic colour polymorphisms in animals , 2014, Molecular ecology.

[21]  David I. Warton,et al.  Topoclimate versus macroclimate: how does climate mapping methodology affect species distribution models and climate change projections? , 2014 .

[22]  T. Hastie,et al.  Bias correction in species distribution models: pooling survey and collection data for multiple species , 2014, Methods in ecology and evolution.

[23]  R. Sacchi,et al.  Chemical polymorphism in male femoral gland secretions matches polymorphic coloration in common wall lizards (Podarcis muralis) , 2014, Chemoecology.

[24]  David I. Warton,et al.  Model-Based Control of Observer Bias for the Analysis of Presence-Only Data in Ecology , 2013, PloS one.

[25]  R. Sacchi,et al.  Colour variation in the polymorphic common wall lizard (Podarcis muralis): An analysis using the RGB colour system , 2013 .

[26]  R. Sacchi,et al.  Homeward bound: factors affecting homing ability in a polymorphic lizard , 2013 .

[27]  R. Sacchi,et al.  Colour Polymorphism and Alternative Breeding Strategies: Effects of Parent’s Colour Morph on Fitness Traits in the Common Wall Lizard , 2013, Evolutionary Biology.

[28]  R. Sacchi,et al.  Studying the reproductive biology of the common wall lizard using ultrasonography , 2012 .

[29]  R. Hijmans,et al.  Cross-validation of species distribution models: removing spatial sorting bias and calibration with a null model. , 2012, Ecology.

[30]  Robert P. Anderson,et al.  Ecological Niches and Geographic Distributions , 2011 .

[31]  S. Dobrowski,et al.  Modeling plant ranges over 75 years of climate change in California, USA: temporal transferability and species traits , 2011 .

[32]  N. Sillero.  What does ecological modelling model? A proposed classification of ecological niche models based on their underlying methods , 2011 .

[33]  M. Ożgo.  Rapid evolution in unstable habitats: a success story of the polymorphic land snail Cepaea nemoralis (Gastropoda: Pulmonata) , 2011 .

[34]  M. Pierotti,et al.  Colour polymorphism and correlated characters: genetic mechanisms and evolution , 2010, Molecular ecology.

[35]  B. Hansson,et al.  Island biology and morphological divergence of the Skyros wall lizard Podarcis gaigeae: a combined role for local selection and genetic drift on color morph frequency divergence? , 2010, BMC Evolutionary Biology.

[36]  M. Giovannotti,et al.  Mitochondrial DNA sequence analysis reveals multiple Pleistocene glacial refugia for Podarcis muralis (Laurenti, 1768) in the Italian Peninsula , 2010 .

[37]  Richard E. Glor,et al.  ENMTools: a toolbox for comparative studies of environmental niche models , 2010 .

[38]  W. Godsoe.  Regional variation exaggerates ecological divergence in niche models. , 2010, Systematic biology.

[39]  Alison R. Davis,et al.  Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation , 2010, Proceedings of the National Academy of Sciences.

[40]  S. Griffith,et al.  The historical frequency of head-colour morphs in the Gouldian Finch (Erythrura gouldiae) , 2009 .

[41]  R. Sacchi,et al.  Male-male combats in a polymorphic lizard: residency and size, but not color, affect fighting rules and contest outcome. , 2009, Aggressive behavior.

[42]  M. Turelli,et al.  Environmental Niche Equivalency versus Conservatism: Quantitative Approaches to Niche Evolution , 2008, Evolution; international journal of organic evolution.

[43]  A. Forsman,et al.  Associations of variable coloration with niche breadth and conservation status among Australian reptiles. , 2008, Ecology.

[44]  R. Sacchi,et al.  Microgeographic variation of colour morph frequency and biometry of common wall lizards , 2007 .

[45]  T. Uller,et al.  Mating system variation and morph fluctuations in a polymorphic lizard , 2007, Molecular ecology.

[46]  N. Raes,et al.  A null‐model for significance testing of presence‐only species distribution models , 2007 .

[47]  A. Herrel,et al.  Morphology, performance, behavior and ecology of three color morphs in males of the lizard Podarcis melisellensis. , 2007, Integrative and comparative biology.

[48]  J. Mckinnon,et al.  Linking color polymorphism maintenance and speciation. , 2007, Trends in ecology & evolution.

[49]  B. Sinervo,et al.  The Developmental, Physiological, Neural, and Genetical Causes and Consequences of Frequency-Dependent Selection in the Wild , 2006 .

[50]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[51]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[52]  T. Dawson,et al.  Selecting thresholds of occurrence in the prediction of species distributions , 2005 .

[53]  Alexandra Roulin.  The evolution, maintenance and adaptive function of genetic colour polymorphism in birds , 2004, Biological reviews of the Cambridge Philosophical Society.

[54]  P. Galeotti,et al.  The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors , 2004 .

[55]  B. Sinervo,et al.  Spatial Scale and Temporal Component of Selection in Side‐Blotched Lizards , 2004, The American Naturalist.

[56]  M. Fasola,et al.  Colour polymorphism in birds: causes and functions , 2003, Journal of evolutionary biology.

[57]  B. Sinervo,et al.  Density-dependent competition and selection on immune function in genetic lizard morphs , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  B. Sinervo,et al.  SOCIAL CAUSES OF CORRELATIONAL SELECTION AND THE RESOLUTION OF A HERITABLE THROAT COLOR POLYMORPHISM IN A LIZARD , 2001, Evolution; international journal of organic evolution.

[59]  W. Ponder,et al.  Evaluation of Museum Collection Data for Use in Biodiversity Assessment , 2001 .

[60]  B. Sinervo,et al.  The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between the sexes. , 2001, The Journal of heredity.

[61]  B. Sinervo,et al.  Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Antoine Guisan,et al.  Predictive habitat distribution models in ecology , 2000 .

[63]  Barry Sinervo,et al.  Testosterone, Endurance, and Darwinian Fitness: Natural and Sexual Selection on the Physiological Bases of Alternative Male Behaviors in Side-Blotched Lizards , 2000, Hormones and Behavior.

[64]  P. Mariottini,et al.  Molecular biogeography of the Mediterranean lizards Podarcis Wagler, 1830 and Teira Gray, 1838 (Reptilia, Lacertidae) , 2000 .

[65]  B. Sinervo,et al.  The rock–paper–scissors game and the evolution of alternative male strategies , 1996, Nature.

[66]  John Maynard Smith,et al.  The games lizards play , 1996, Nature.

[67]  R. Knapp,et al.  Hormonal Responses to Aggression Vary in Different Types of Agonistic Encounters in Male Tree Lizards, Urosaurus ornatus , 1995, Hormones and Behavior.

[68]  G. C. Carpenter.  The Ontogeny of a Variable Social Badge: Throat Color Development in Tree Lizards (Urosaurus ornatus) , 1995 .

[69]  I. Moore,et al.  Social, environmental and genetic factors in the ontogeny of phenotypic differentiation in a lizard with alternative male reproductive strategies , 1993, Behavioral Ecology and Sociobiology.

[70]  G. Arnqvist.  SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER, GERRIS ODONTOGASTER , 1992, Evolution; international journal of organic evolution.

[71]  C. W. Thompson,et al.  Throat colour reliably signals status in male tree lizards, Urosaurus ornatus , 1991, Animal Behaviour.

[72]  M. Moore,et al.  Syntopic Occurrence of Multiple Dewlap Color Morphs in Male Tree Lizards, Urosaurus ornatus , 1991 .

[73]  M. West-Eberhard,et al.  Alternative adaptations, speciation, and phylogeny (A Review). , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[74]  E. Hover.  Differences in Aggressive Behavior Between Two Throat Color Morphs in a Lizard, Urosaurus ornatus , 1985 .

[75]  T. Schoener.  The Anolis Lizards of Bimini: Resource Partitioning in a Complex Fauna , 1968 .

[76]  J. Huxley.  Morphism in birds , 1955 .

[77]  M. Kearney,et al.  Advances in Monitoring and Modelling Climate at Ecologically Relevant Scales , 2018 .

[78]  E. Font,et al.  The role of male coloration in the outcome of staged contests in the European common wall lizard (Podarcis muralis) , 2016 .

[79]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[80]  C. Corti,et al.  Genetic variability in mainland and insular populations of Podarcis muralis (Reptilia: Lacertidae) , 2010 .

[81]  Steven J. Phillips,et al.  Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. , 2009, Ecological applications : a publication of the Ecological Society of America.

[82]  M Chévremont,et al.  Mitochondrial DNA , 2009, Encyclopedia of Biometrics.

[83]  A. Forsman,et al.  Variable coloration is associated with more northerly geographic range limits and larger range sizes in North American lizards and snakes , 2008 .

[84]  Gerris Odontogaster.  SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER, , 1992 .

[85]  M. Cheylan.  Variabilité phénotypique du lézard des murailles Podarcis muralis sur les îles de la côte provençale, France , 1988, Revue d'Écologie (La Terre et La Vie).