More than a flying syringe: Using functional traits in vector borne disease research

Vectors are responsible for the transmission of many important endemic and emerging diseases. The functional traits of these animals have important consequences for pathogen transmission, but also for fitness and population dynamics of the vectors themselves. Increasing empirical evidence suggests that vector traits vary significantly at time scales relevant to transmission dynamics. Currently, an understanding of how this variation in key traits impacts transmission is hindered by a lack of empirical data as well theoretical methods as for mechanistically incorporating traits into transmission models. Here, we present a framework for incorporating both intrinsic and environment-driven variation in vector traits into empirical and theoretical vector-borne disease research. This framework mechanistically captures the effect of trait variation on vector fitness, the correlation between vector traits, and how these together determine transmission dynamics. We illustrate how trait-based vector-borne disease modelling can make novel predictions, and identify key steps and challenges in the construction, empirical parameterization and validation of such models. Perhaps most importantly, this framework can also be used to prioritize data collection efforts.

[1]  P. Amarasekare,et al.  The intrinsic growth rate as a predictor of population viability under climate warming. , 2013, The Journal of animal ecology.

[2]  C. Murdock,et al.  Larval food quantity affects the capacity of adult mosquitoes to transmit human malaria , 2016, Proceedings of the Royal Society B: Biological Sciences.

[3]  N. Uygun,et al.  Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Hom., Aphididae) reared on Gossypium hirsutum L. , 1999 .

[4]  S. Lal,et al.  Epidemiology and control of malaria , 1999, Indian journal of pediatrics.

[5]  Libo Sun,et al.  Parameter inference and model selection in deterministic and stochastic dynamical models via approximate Bayesian computation: modeling a wildlife epidemic , 2014, 1409.7715.

[6]  Jerald B. Johnson,et al.  Model selection in ecology and evolution. , 2004, Trends in ecology & evolution.

[7]  J. Buonaccorsi,et al.  Analysis of Survival of Young and Old Aedes aegypti (Diptera: Culicidae) from Puerto Rico and Thailand , 2001, Journal of medical entomology.

[8]  Thomas Caraco,et al.  Stage‐Structured Infection Transmission and a Spatial Epidemic: A Model for Lyme Disease , 2002, The American Naturalist.

[9]  S W Lindsay,et al.  Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae) , 2003, Bulletin of Entomological Research.

[10]  T. Raffel,et al.  Thermal Performance Curves and the Metabolic Theory of Ecology—A Practical Guide to Models and Experiments for Parasitologists , 2017, Journal of Parasitology.

[11]  Daniel P Weikel,et al.  Phenomenological forecasting of disease incidence using heteroskedastic Gaussian processes: a dengue case study , 2017, 1702.00261.

[12]  N Thompson Hobbs,et al.  Data–model fusion to better understand emerging pathogens and improve infectious disease forecasting , 2011, Ecological applications : a publication of the Ecological Society of America.

[13]  V. Savage,et al.  From Metabolic Constraints on Individuals to the Dynamics of Ecosystems , 2015 .

[14]  Lynn B. Martin,et al.  Extreme Competence: Keystone Hosts of Infections , 2019, Trends in Ecology & Evolution.

[15]  P. Hotez,et al.  Global economic burden of Chagas disease: a computational simulation model. , 2013, The Lancet. Infectious diseases.

[16]  Nicolas Bacaër,et al.  Growth rate and basic reproduction number for population models with a simple periodic factor. , 2007, Mathematical biosciences.

[17]  K. Paaijmans,et al.  Mapping the Distribution of Malaria: Current Approaches and Future Directions , 2015 .

[18]  N. Durand,et al.  Functional Development of the Octenol Response in Aedes aegypti , 2013, Front. Physiol..

[19]  Anthony J. Wilson,et al.  Bluetongue in Europe: past, present and future , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  N. Gerardo,et al.  The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid, Acyrthosiphon pisum , 2013, Applied and Environmental Microbiology.

[21]  Lauren J. Cator,et al.  Fitness consequences of altered feeding behavior in immune-challenged mosquitoes , 2016, Parasites & Vectors.

[22]  C. J. McGrath,et al.  Effect of exchange rate return on volatility spill-over across trading regions , 2012 .

[23]  J. Holt,et al.  Epidemiology of insect‐transmitted plant viruses: modelling disease dynamics and control interventions , 2004 .

[24]  S. Long,et al.  Free-air Carbon Dioxide Enrichment (FACE) in Global Change Research: A Review , 1999 .

[25]  D. White Epidemiology of Lyme disease. , 1991, The Canadian journal of infectious diseases = Journal canadien des maladies infectieuses.

[26]  Leslie A. Real,et al.  Vector Preference and Disease Dynamics: A Study of Barley Yellow Dwarf Virus , 1995 .

[27]  P. Michel,et al.  A systematic, realist review of zooprophylaxis for malaria control , 2015, Malaria Journal.

[28]  M. Daugherty,et al.  Temporal progression of 'Candidatus Liberibacter asiaticus' infection in citrus and acquisition efficiency by Diaphorina citri. , 2014, Phytopathology.

[29]  Nicolas Bacaër,et al.  On the biological interpretation of a definition for the parameter R0 in periodic population models , 2012, Journal of mathematical biology.

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

[31]  James O. Berger,et al.  Using Statistical and Computer Models to Quantify Volcanic Hazards , 2009, Technometrics.

[32]  L. Madden,et al.  Effects of Temperature and Vector Age on Transmission of Two Ohio Strains of Aster Yellows Phytoplasma by the Aster Leafhopper (Homoptera: Cicadellidae) , 1996 .

[33]  Deepa Agashe The Stabilizing Effect of Intraspecific Genetic Variation on Population Dynamics in Novel and Ancestral Habitats , 2009, The American Naturalist.

[34]  S. Schreiber,et al.  Why intraspecific trait variation matters in community ecology. , 2011, Trends in ecology & evolution.

[35]  C. J. Otter,et al.  Effects of age, sex and hunger on the antennal olfactory sensitivity of tsetse flies , 1991 .

[36]  David L. Smith,et al.  Vectorial capacity and vector control: reconsidering sensitivity to parameters for malaria elimination , 2016, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[37]  Takehiko Yamanaka,et al.  Model analysis for plant disease dynamics co-mediated by herbivory and herbivore-borne phytopathogens , 2012, Biology Letters.

[38]  K. Paaijmans,et al.  The Effect of Temperature on Anopheles Mosquito Population Dynamics and the Potential for Malaria Transmission , 2013, PloS one.

[39]  R. Gomulkiewicz Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology : Eric L. Charnov Oxford Series in Ecology and Evolution, Oxford University Press, Oxford, United Kingdom, 1993, 167 pp., $19.95 (paper), $37.50 (cloth). , 1994 .

[40]  Giovanini Evelim Coelho,et al.  Zika virus in the Americas: Early epidemiological and genetic findings , 2016, Science.

[41]  A. Dell,et al.  Scaling-up Trait Variation from Individuals to Ecosystems , 2015 .

[42]  Mevin B. Hooten,et al.  A guide to Bayesian model selection for ecologists , 2015 .

[43]  Paul E. Parham,et al.  Modeling the Effects of Weather and Climate Change on Malaria Transmission , 2009, Environmental health perspectives.

[44]  Mick G. Roberts,et al.  THRESHOLD QUANTITIES FOR INFECTIOUS DISEASES IN PERIODIC ENVIRONMENTS , 1995 .

[45]  J Norberg,et al.  Phenotypic diversity and ecosystem functioning in changing environments: A theoretical framework , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[46]  J. Blanchard,et al.  A bioenergetic framework for the temperature dependence of trophic interactions. , 2014, Ecology letters.

[47]  Anatoliy I. Yashin,et al.  An Age-Structured Extension to the Vectorial Capacity Model , 2012, PloS one.

[48]  S. Moore,et al.  Plant-based insect repellents: a review of their efficacy, development and testing , 2011, Malaria Journal.

[49]  Wayne M Getz,et al.  Making ecological models adequate. , 2018, Ecology letters.

[50]  Nicolas Bacaër,et al.  The epidemic threshold of vector-borne diseases with seasonality , 2006, Journal of mathematical biology.

[51]  S. Lavorel,et al.  Incorporating plant functional diversity effects in ecosystem service assessments , 2007, Proceedings of the National Academy of Sciences.

[52]  C. Dye,et al.  Population dynamics of mosquito-borne disease: effects of flies which bite some people more frequently than others. , 1986, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[53]  T. Scott,et al.  Age and body size effects on blood meal size and multiple blood feeding by Aedes aegypti (Diptera: Culicidae). , 1995, Journal of medical entomology.

[54]  V. Savage,et al.  Improved approximations to scaling relationships for species, populations, and ecosystems across latitudinal and elevational gradients. , 2004, Journal of theoretical biology.

[55]  K. Paaijmans,et al.  Understanding uncertainty in temperature effects on vector-borne disease: a Bayesian approach. , 2013, Ecology.

[56]  T. Scott,et al.  Age-Dependent Survival of the Dengue Vector Aedes aegypti (Diptera: Culicidae) Demonstrated by Simultaneous Release–Recapture of Different Age Cohorts , 2008, Journal of medical entomology.

[57]  W. Takken,et al.  Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi , 2013, Parasites & Vectors.

[58]  David L. Smith,et al.  Ross, Macdonald, and a Theory for the Dynamics and Control of Mosquito-Transmitted Pathogens , 2012, PLoS pathogens.

[59]  J. K. Nayar,et al.  A comparative study of flight performance and fuel utilization as a function of age in females of Florida mosquitoes. , 1973, Journal of insect physiology.

[60]  L. F. Chaves,et al.  Increased Adult Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) Abundance in a Dengue Transmission Hotspot, Compared to a Coldspot, within Kaohsiung City, Taiwan , 2018, Insects.

[61]  John C. Carlson,et al.  A simulation model of African Anopheles ecology and population dynamics for the analysis of malaria transmission , 2004, Malaria Journal.

[62]  David M. Hartley,et al.  A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010 , 2013, Journal of The Royal Society Interface.

[63]  L. Cator,et al.  Immunity, host physiology, and behaviour in infected vectors. , 2017, Current opinion in insect science.

[64]  Van M. Savagea Improved approximations to scaling relationships for species , populations , and ecosystems across latitudinal and elevational gradients , 2004 .

[65]  T. Lefèvre,et al.  Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. , 2008, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[66]  Felicia Keesing,et al.  The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[67]  J. Teevan Influence of temperature , 2007 .

[68]  Leah R. Johnson,et al.  Bayesian inference for bioenergetic models , 2013 .

[69]  Andrew J. Tatem,et al.  Recasting the theory of mosquito-borne pathogen transmission dynamics and control , 2014, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[70]  Y. Toquenaga,et al.  Genetic variation can promote system persistence in an experimental host-parasitoid system , 2003, Population Ecology.

[71]  Alexis Lawrence Romanoff,et al.  Influence of temperature , 1938 .

[72]  P. Mellor,et al.  Vector competence of South African Culicoides species for bluetongue virus serotype 1 (BTV‐1) with special reference to the effect of temperature on the rate of virus replication in C. imicola and C. bolitinos , 2002, Medical and veterinary entomology.

[73]  Weihua Li,et al.  Effect of temperature on the transmission characteristics of high-torque magnetorheological brakes , 2019, Smart Materials and Structures.

[74]  A. Rolando,et al.  Evidence for Male Horn Dimorphism and Related Pronotal Shape Variation in Copris lunaris (Linnaeus, 1758) (Coleoptera: Scarabaeidae, Coprini) , 2018, Insects.

[75]  C. Webb,et al.  Scaling from Traits to Ecosystems: Developing a General Trait Driver Theory via Integrating Trait-Based and Metabolic Scaling Theories , 2015, 1502.06629.

[76]  Roy M. Anderson,et al.  The Population Dynamics of Microparasites and Their Invertebrate Hosts , 1981 .

[77]  Enrique Alonso García,et al.  Towards global data products of Essential Biodiversity Variables on species traits , 2018, Nature Ecology & Evolution.

[78]  L. Kramer,et al.  Effect of temperature of extrinsic incubation on the vector competence of Culex tarsalis for western equine encephalomyelitis virus. , 1983, The American journal of tropical medicine and hygiene.

[79]  M. Guzmán,et al.  The epidemiology of dengue in the americas over the last three decades: a worrisome reality. , 2010, The American journal of tropical medicine and hygiene.

[80]  G. Dayan,et al.  The history of dengue outbreaks in the Americas. , 2012, The American journal of tropical medicine and hygiene.

[81]  L. F. Chaves,et al.  Uranotaenia novobscura ryukyuana (Diptera: Culicidae) Population Dynamics are Denso-Dependent and Autonomous from Weather Fluctuations , 2014 .

[82]  Michael D. Collins,et al.  Supporting Online Material Materials and Methods Figs. S1 to S3 Tables S1 and S2 References Plant Genotypic Diversity Predicts Community Structure and Governs an Ecosystem Process , 2022 .

[83]  S. Gandon,et al.  Plasmodium infection decreases fecundity and increases survival of mosquitoes , 2012, Proceedings of the Royal Society B: Biological Sciences.

[84]  V. Savage,et al.  Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. , 2014, The Journal of animal ecology.

[85]  T. Lefèvre,et al.  Rethinking the extrinsic incubation period of malaria parasites , 2018, Parasites & Vectors.

[86]  J. Koella Malaria as a manipulator , 2005, Behavioural Processes.

[87]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[88]  R. May,et al.  Population biology of infectious diseases: Part I , 1979, Nature.

[89]  D. Haydon Models for Ecological Data: An Introduction , 2008 .

[90]  V. Savage,et al.  A Framework for Elucidating the Temperature Dependence of Fitness , 2011, The American Naturalist.

[91]  Leah R Johnson,et al.  Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models , 2017, PLoS neglected tropical diseases.

[92]  Bernard Moulin,et al.  Introduction to Analyzing and Modeling Spatial and Temporal Dynamics of Infectious Diseases , 2015 .

[93]  C. Carbone,et al.  Foraging constraints reverse the scaling of activity time in carnivores , 2018, Nature Ecology & Evolution.

[94]  Zihua Zhao,et al.  Using the loess method to describe the effect of temperature on development rate , 2017 .

[95]  J. Koella,et al.  Maternal environment shapes the life history and susceptibility to malaria of Anopheles gambiae mosquitoes , 2011, Malaria Journal.

[96]  B. Enquist,et al.  Rebuilding community ecology from functional traits. , 2006, Trends in ecology & evolution.

[97]  James Harle,et al.  Potential consequences of climate change for primary production and fish production in large marine ecosystems , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[98]  Jennifer A Hoeting,et al.  A structured and dynamic framework to advance traits-based theory and prediction in ecology. , 2010, Ecology letters.

[99]  T. Lefèvre,et al.  Evidence for carry-over effects of predator exposure on pathogen transmission potential , 2015, Proceedings of the Royal Society B: Biological Sciences.

[100]  K. Paaijmans,et al.  Optimal temperature for malaria transmission is dramatically lower than previously predicted. , 2013, Ecology letters.

[101]  A. Graham,et al.  Opportunities and challenges of Integral Projection Models for modelling host–parasite dynamics , 2015, Journal of Animal Ecology.

[102]  P. E. Kopp,et al.  Superspreading and the effect of individual variation on disease emergence , 2005, Nature.

[103]  B. M. Christensen,et al.  Age‐associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers , 2004, Cellular microbiology.

[104]  Jane-Ling Wang,et al.  Mosquitoes do senesce: departure from the paradigm of constant mortality. , 2007, The American journal of tropical medicine and hygiene.

[105]  Samraat Pawar,et al.  Dimensionality of consumer search space drives trophic interaction strengths , 2012, Nature.

[106]  A. Nappi,et al.  Melanization immune responses in mosquito vectors. , 2005, Trends in parasitology.

[107]  C. Albuquerque,et al.  Impact of small variations in temperature and humidity on the reproductive activity and survival of Aedes aegypti (Diptera, Culicidae) , 2010 .

[108]  H. Delatte,et al.  Influence of Temperature on Immature Development, Survival, Longevity, Fecundity, and Gonotrophic Cycles of Aedes albopictus, Vector of Chikungunya and Dengue in the Indian Ocean , 2009, Journal of medical entomology.

[109]  L. R. Petersen,et al.  Zika Virus. , 2016, The New England journal of medicine.

[110]  V. Savage,et al.  Systematic variation in the temperature dependence of physiological and ecological traits , 2011, Proceedings of the National Academy of Sciences.

[111]  A. Dobson,et al.  Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics. , 2013, Ecology letters.

[112]  D. Kirk,et al.  Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics , 2018, PLoS biology.

[113]  S. Bellan The Importance of Age Dependent Mortality and the Extrinsic Incubation Period in Models of Mosquito-Borne Disease Transmission and Control , 2010, PloS one.

[114]  Giulio A. De Leo,et al.  Allometry and simple epidemic models for microparasites , 1996, Nature.

[115]  R. May,et al.  Population biology of infectious diseases: Part II , 1979, Nature.

[116]  G. D. Paterson,et al.  THE ANALYSIS OF MORTALITY AND SURVIVAL RATES IN WILD POPULATION OF MOSQUITOES , 1981 .

[117]  Michael J. Turell,et al.  Effect of Environmental Temperature on the Ability of Culex pipiens (Diptera: Culicidae) to Transmit West Nile Virus , 2002, Journal of medical entomology.

[118]  M. Service,et al.  Size variation and reproductive success in the mosquito Aedes cantans , 1994, Medical and veterinary entomology.

[119]  R. May,et al.  Modelling vaccination strategies against foot-and-mouth disease , 2003, Nature.

[120]  Nicolas Bacaër Approximation of the Basic Reproduction Number R0 for Vector-Borne Diseases with a Periodic Vector Population , 2007, Bulletin of mathematical biology.

[121]  L. P. Lounibos,et al.  Age-dependent bloodfeeding of Aedes aegypti and Aedes albopictus on artificial and living hosts. , 2003, Journal of the American Mosquito Control Association.

[122]  P. Kindlmann,et al.  INSECT PREDATOR-PREY DYNAMICS AND THE BIOLOGICAL CONTROL OF APHIDS BY LADYBIRDS , 2003 .

[123]  T. Baker,et al.  ‘Manipulation’ without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites , 2013, Proceedings of the Royal Society B: Biological Sciences.

[124]  Kate E. Jones,et al.  Impacts of biodiversity on the emergence and transmission of infectious diseases , 2010, Nature.

[125]  L. Johnson,et al.  Mathematical models are a powerful method to understand and control the spread of Huanglongbing , 2016, PeerJ.

[126]  Matt J. Keeling,et al.  The Interaction between Vector Life History and Short Vector Life in Vector-Borne Disease Transmission and Control , 2016, PLoS Comput. Biol..

[127]  Laura D. Kramer,et al.  The Effect of Temperature on Life History Traits of Culex Mosquitoes , 2014, Journal of medical entomology.