Nutritional ecology beyond the individual: a conceptual framework for integrating nutrition and social interactions

Over recent years, modelling approaches from nutritional ecology (known as Nutritional Geometry) have been increasingly used to describe how animals and some other organisms select foods and eat them in appropriate amounts in order to maintain a balanced nutritional state maximising fitness. These nutritional strategies profoundly affect the physiology, behaviour and performance of individuals, which in turn impact their social interactions within groups and societies. Here, we present a conceptual framework to study the role of nutrition as a major ecological factor influencing the development and maintenance of social life. We first illustrate some of the mechanisms by which nutritional differences among individuals mediate social interactions in a broad range of species and ecological contexts. We then explain how studying individual- and collective-level nutrition in a common conceptual framework derived from Nutritional Geometry can bring new fundamental insights into the mechanisms and evolution of social interactions, using a combination of simulation models and manipulative experiments.

[1]  T. Seeley,et al.  Collective decision-making in honey bees: how colonies choose among nectar sources , 1991, Behavioral Ecology and Sociobiology.

[2]  Pawel Romanczuk,et al.  Cannibalism can drive the evolution of behavioural phase polyphenism in locusts. , 2012, Ecology letters.

[3]  Pawel Romanczuk,et al.  Nutritional state and collective motion: from individuals to mass migration , 2011, Proceedings of the Royal Society B: Biological Sciences.

[4]  G. Amdam,et al.  A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies , 2007, Proceedings of the National Academy of Sciences.

[5]  D. Bignell,et al.  Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera , 2001, Insectes Sociaux.

[6]  Ilya R. Fischhoff,et al.  Social relationships and reproductive state influence leadership roles in movements of plains zebra, Equus burchellii , 2007, Animal Behaviour.

[7]  J. Cory,et al.  Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar , 2006, Proceedings of the Royal Society B: Biological Sciences.

[8]  Richard G Melvin,et al.  The ratio of macronutrients, not caloric intake, dictates cardiometabolic health, aging, and longevity in ad libitum-fed mice. , 2014, Cell metabolism.

[9]  David Raubenheimer,et al.  Geometric analysis of macronutrient selection in the adult domestic cat, Felis catus , 2011, Journal of Experimental Biology.

[10]  F. Popper,et al.  The Onset of the , 2006 .

[11]  Joseph J. Hale,et al.  From Disorder to Order in Marching Locusts , 2006, Science.

[12]  Iain D. Couzin.  Collective animal behaviour. , 1999 .

[13]  Linda Partridge,et al.  Quantification of Food Intake in Drosophila , 2009, PloS one.

[14]  L. Conradt,et al.  Consensus decision making in animals. , 2005, Trends in ecology & evolution.

[15]  J. Deneubourg,et al.  Collective Decision-Making and Foraging Patterns in Ants and Honeybees , 2008 .

[16]  M. Kamakura.  Royalactin induces queen differentiation in honeybees , 2011, Nature.

[17]  Stephen J. Simpson,et al.  Small‐scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust , 2000 .

[18]  David Raubenheimer,et al.  Nutrition, ecology and nutritional ecology: toward an integrated framework , 2009 .

[19]  J. Deneubourg,et al.  Collective foraging decision in a gregarious insect , 2010, Behavioral Ecology and Sociobiology.

[20]  M. Kaspari,et al.  A carbohydrate-rich diet increases social immunity in ants , 2014, Proceedings of the Royal Society B: Biological Sciences.

[21]  M. West-Eberhard.  Developmental plasticity and evolution , 2003 .

[22]  Robert E. Page,et al.  The developmental genetics and physiology of honeybee societies , 2010, Animal Behaviour.

[23]  Audrey Dussutour,et al.  Communal Nutrition in Ants , 2009, Current Biology.

[24]  Yael Lubin,et al.  Colony nutrition skews reproduction in a social spider , 2008 .

[25]  C. Chapman,et al.  Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein , 2011, Biology Letters.

[26]  H. Stanley,et al.  Optimizing the success of random searches , 1999, Nature.

[27]  S. Simpson,et al.  Can the protein costs of bacterial resistance be offset by altered feeding behaviour? , 2009, The Journal of animal ecology.

[28]  D J T Sumpter,et al.  The feeding dynamics of broiler chickens , 2007, Journal of The Royal Society Interface.

[29]  D. Sumpter,et al.  From nonlinearity to optimality: pheromone trail foraging by ants , 2003, Animal Behaviour.

[30]  Steven C. Cook,et al.  Colony-level macronutrient regulation in ants: mechanisms, hoarding and associated costs , 2010, Animal Behaviour.

[31]  Jens Krause,et al.  Front Individuals Lead in Shoals of Three-Spined Sticklebacks (Gasterosteus Aculeatus) and Juvenile Roach (Rutilus Rutilus) , 1993 .

[32]  Susanne Hertz,et al.  Principles Of Social Evolution , 2016 .

[33]  A. Dussutour,et al.  Ant workers die young and colonies collapse when fed a high-protein diet , 2012, Proceedings of the Royal Society B: Biological Sciences.

[34]  J. H. Hunt,et al.  Nourishment And Evolution In Insect Societies , 1994 .

[35]  Jean-Louis Deneubourg,et al.  Feeding and Stocking Up: Radio-Labelled Food Reveals Exchange Patterns in Ants , 2009, PloS one.

[36]  S. Behmer.  Insect herbivore nutrient regulation. , 2009, Annual review of entomology.

[37]  I. Couzin,et al.  Collective behavior in cancer cell populations , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[38]  A. Pérez-Escudero,et al.  idTracker: tracking individuals in a group by automatic identification of unmarked animals , 2014, Nature Methods.

[39]  C. Grüter,et al.  Insights from insects about adaptive social information use. , 2014, Trends in ecology & evolution.

[40]  J. Krause,et al.  Relationship between the position preference and nutritional state of individuals in schools of juvenile roach (Rutilus rutilus) , 1992, Behavioral Ecology and Sociobiology.

[41]  Chris C. R. Smith,et al.  The trophic ecology of castes in harvester ant colonies , 2010 .

[42]  Robert E. Cohen,et al.  The Onset of Collective Behavior in Social Amoebae , 2011 .

[43]  D. Sumpter.  Collective Animal Behavior , 2010 .

[44]  I. Couzin,et al.  “Leading According to Need” in Self‐Organizing Groups , 2009, The American Naturalist.

[45]  Paul J. B. Hart,et al.  Quorum decision-making facilitates information transfer in fish shoals , 2008, Proceedings of the National Academy of Sciences.

[46]  A Griffin,et al.  Cooperation, control, and concession in meerkat groups. , 2001, Science.

[47]  M. Quesada,et al.  A quantitative review of pollination syndromes: do floral traits predict effective pollinators? , 2014, Ecology letters.

[48]  E. Despland,et al.  Group leadership depends on energetic state in a nomadic collective foraging caterpillar , 2011, Behavioral Ecology and Sociobiology.

[49]  I. Couzin,et al.  Self-Organization and Collective Behavior in Vertebrates , 2003 .

[50]  A. Crespi,et al.  Tracking Individuals Shows Spatial Fidelity Is a Key Regulator of Ant Social Organization , 2013, Science.

[51]  R. R. Krausz.  Living in Groups , 2013 .

[52]  Stephen J. Simpson,et al.  Predator Percolation, Insect Outbreaks, and Phase Polyphenism , 2009, Current Biology.

[53]  Robert E. Page,et al.  Complex social behaviour derived from maternal reproductive traits , 2006, Nature.

[54]  I. Couzin,et al.  An evolutionary framework for studying mechanisms of social behavior. , 2014, Trends in ecology & evolution.

[55]  D. Gordon.  The Ecology of Collective Behavior , 2014, PLoS biology.

[56]  A. J. Moore,et al.  Social Behaviour: Genes, Ecology and Evolution , 2010 .

[57]  Sean A. Rands,et al.  Spontaneous emergence of leaders and followers in foraging pairs , 2003, Nature.

[58]  S. Levin.  THE PROBLEM OF PATTERN AND SCALE IN ECOLOGY , 1992 .

[59]  Nick J. Royle,et al.  Nutrition during sexual maturation affects competitive ability but not reproductive productivity in burying beetles , 2013 .

[60]  D. Holway,et al.  Linking nutrition and behavioural dominance: carbohydrate scarcity limits aggression and activity in Argentine ants , 2007, Proceedings of the Royal Society B: Biological Sciences.

[61]  I. Couzin,et al.  Cannibal crickets on a forced march for protein and salt. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Michael A. Cant,et al.  Resource limitation moderates the adaptive suppression of subordinate breeding in a cooperatively breeding mongoose , 2012 .

[63]  Thomas Schlegel,et al.  Stop Signals Provide Cross Inhibition in Collective Decision-making , 2022 .

[64]  S. J. Simpson,et al.  Individual differences influence collective behaviour in social caterpillars , 2008, Animal Behaviour.

[65]  Pier P. Paoli,et al.  Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age , 2014, Amino Acids.

[66]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[67]  G. Holton.  Sociobiology: the new synthesis? , 1977, Newsletter on science, technology & human values.

[68]  D C Krakauer,et al.  Spatial scales of desert locust gregarization. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Richard J. Gill,et al.  Combined pesticide exposure severely affects individual- and colony-level traits in bees , 2012, Nature.

[70]  José Halloy,et al.  Collegial decision making based on social amplification leads to optimal group formation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[71]  T. Valone,et al.  Public Information: From Nosy Neighbors to Cultural Evolution , 2004, Science.

[72]  G. Bell.  Experimental evolution , 2008, Heredity.

[73]  T. Caraco,et al.  Social Foraging Theory , 2018 .

[74]  M. Sokolowski,et al.  Social Interactions in “Simple” Model Systems , 2010, Neuron.

[75]  David Raubenheimer,et al.  Lifespan and reproduction in Drosophila: New insights from nutritional geometry , 2008, Proceedings of the National Academy of Sciences.

[76]  P. Gowaty.  Developmental Plasticity and Evolution Mary Jane West-Eberhard , 2005, Animal Behaviour.

[77]  S. Levin.  The problem of pattern and scale in ecology , 1992 .

[78]  R. Sibly,et al.  Optimal foraging when regulating intake of multiple nutrients , 2004, Animal Behaviour.

[79]  J. Elser,et al.  Obligate herbivory in an ancestrally carnivorous lineage: the giant panda and bamboo from the perspective of nutritional geometry , 2015 .

[80]  A. Dussutour,et al.  Key Factors for the Emergence of Collective Decision in Invertebrates , 2012, Front. Neurosci..

[81]  R. Shine,et al.  Why be a cannibal? The benefits to cane toad, Rhinella marina [=Bufo marinus], tadpoles of consuming conspecific eggs , 2011, Animal Behaviour.

[82]  E. Wilson,et al.  The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies , 2008 .

[83]  J. Deneubourg,et al.  Allelomimetic synchronization in Merino sheep , 2007, Animal Behaviour.

[84]  F. D..  The Social Insects: their Origin and Evolution , 1928, Nature.

[85]  R. Kucharski,et al.  Nutritional Control of Reproductive Status in Honeybees via DNA Methylation , 2008, Science.

[86]  T. Seeley.  The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies , 1995 .

[87]  Guy Theraulaz,et al.  Mathematical model of self-organizing hierarchies in animal societies , 1996 .

[88]  Tobias Otte,et al.  Starving the competition: a proximate cause of reproductive skew in burying beetles (Nicrophorus vespilloides) , 2008, Proceedings of the Royal Society B: Biological Sciences.

[89]  David Raubenheimer,et al.  The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity , 2012 .

[90]  M. Purugganan,et al.  The cooperative amoeba: Dictyostelium as a model for social evolution. , 2011, Trends in genetics : TIG.

[91]  Mathieu Lihoreau,et al.  Recent advances in the integrative nutrition of arthropods. , 2015, Annual review of entomology.

[92]  A. Reynolds,et al.  Radar Tracking and Motion-Sensitive Cameras on Flowers Reveal the Development of Pollinator Multi-Destination Routes over Large Spatial Scales , 2012, PLoS biology.

[93]  Daniel A. Ashlock,et al.  Evolutionary computation for modeling and optimization , 2005 .

[94]  Michael H. Dickinson,et al.  Automated monitoring and quantitative analysis of feeding behaviour in Drosophila , 2014, Nature Communications.

[95]  I. Couzin.  Collective cognition in animal groups , 2009, Trends in Cognitive Sciences.

[96]  Laurent Keller,et al.  Nature versus nurture in social insect caste differentiation. , 2010, Trends in ecology & evolution.

[97]  R. Morse.  The Dance Language and Orientation of Bees , 1994 .

[98]  David Raubenheimer,et al.  Match and mismatch: conservation physiology, nutritional ecology and the timescales of biological adaptation , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[99]  V. Isaeva.  Self-organization in biological systems , 2012, Biology Bulletin.

[100]  D. Aanen,et al.  High Symbiont Relatedness Stabilizes Mutualistic Cooperation in Fungus-Growing Termites , 2009, Science.

[101]  J. Deneubourg,et al.  Self-organized shortcuts in the Argentine ant , 1989, Naturwissenschaften.

[102]  Doreen Schweizer,et al.  Social Behaviour Genes Ecology And Evolution , 2016 .

[103]  Michael A Charleston,et al.  Modelling nutrition across organizational levels: from individuals to superorganisms. , 2014, Journal of insect physiology.

[104]  Diana E. Wheeler,et al.  Developmental and Physiological Determinants of Caste in Social Hymenoptera: Evolutionary Implications , 1986, The American Naturalist.