Trends in Parasitology

Trends in Parasitology

Volume 25, Issue 4, April 2009, Pages 189-196
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Review
Ecological and evolutionary determinants of host species choice in mosquito vectors

https://doi.org/10.1016/j.pt.2009.01.005Get rights and content

Insects exhibit diverse resource-exploitation strategies, including predation, herbivory and parasitism. The ecological and evolutionary factors that influence the resource selection of some insects (e.g. herbivores) have been extensively investigated because of their agricultural importance. By contrast, there has been little investigation of the selective forces that mediate host choice in haematophagous insects, despite their importance as vectors of disease. Here, we review potential determinants of host species choice in mosquitoes, the most important insect vectors of human disease, and discuss whether these could be manipulated to yield new disease-control strategies based on vector behavioural change.

Section snippets

Epidemiological relevance of mosquito host species choice

Insects are the most abundant and diverse group of animals [1]. Due to the massive economic impact of herbivorous insects on agriculture and forestry, the determinants of their feeding preferences have been investigated extensively [2]. By contrast, little is known about the determinants of host choice in insects that feed on vertebrate blood. These organisms transmit numerous human and animal diseases; mosquitoes have the greatest impact on public health because of their role in malaria,

Evolution of host choice

A substantial body of theory and empirical research has accrued to predict how organisms should select dietary resources to maximize their fitness (see Glossary) [5]. The widespread existence of dietary specialization presents a paradox: why choose a limited variety of resources when many are available? Dietary specialization is predicted to evolve when there are trade-offs between the fitness obtained from feeding on different resources, such that net energy gain is higher when only a limited

Patterns of host species choice in mosquitoes

General patterns of mosquito host species range may be inferred from large-scale entomological surveys, such as those conducted on Anopheline malaria vectors by the World Health Organization [11]. In the period 1955–1964, over 100 000 individual anophelines were analyzed to estimate the human blood index (HBI) of different species. Detailed analyses were performed on a sub-sample of 52 species to identify further the source of non-human blood. Of these populations, 82% exhibited dietary

Host availability

Spatial and temporal heterogeneity in host distribution influences the duration of mosquito host seeking, which, in turn, might influence energetic expenditure, survival and risk of predation while foraging. At its most extreme, host availability is known to impact mosquito feeding behaviour by influencing whether they bloodfeed at all. Specifically, autogeneous egg production in mosquitoes has been associated with environments in which vertebrate host availability is severely limited [12].

In

Nutritional value of blood and energetic costs of digestion

Non-random feeding of mosquitoes may be explained by variation in nutritional rewards and corresponding fitness accruing from different host types. Experimental studies consistently indicate that the reproduction and survival of mosquitoes after bloodfeeding varies with host species (Table 1). Several haematological properties vary between vertebrate species, which could influence the nutritive value of their blood 19, 20. During feeding, mosquitoes pass ingested blood through the pyloric

Host defensive behaviour

Whereas the defensive behaviour of plants (expressed by production of toxic metabolites) has been identified as probably the most important predictor of the host species choice of phytophagous insects [2], the relative importance of host defensive behaviour to mosquito host species choice remains unclear. Animals defend themselves from insect bites by a variety of means, including protective tissues (such as skin and feathers), physical movements and behavioural avoidance (for a review, see

Other potential determinants of host species choice

Other physiological, behavioural and ecological factors may also play a part in mosquito host-choice evolution. Vertebrate hosts mount immune responses to arthropod saliva, which can impede the feeding success, reproduction and survival of insects that subsequently bite them 33, 34. Variation in immunocompetence among host species could generate selection for specialization on less-responsive host types. Biochemical and physiological properties of mosquito saliva could also influence their

Contrasting mosquitoes with other haematophagous insects

As in mosquitoes, specialization on a limited number of host species is common in other haematophagous insects such as fleas, where many taxa feed principally on only one host species (e.g. Figure 1b). Similarly, although the host choice of tsetse flies seems to be more evenly distributed across different host species, some types are still fed upon substantially more often than others (Figure 1c).

Most information on the relationship between host availability and host species choice comes from

Mosquito host choice evolution in a dynamic world

Current patterns of host species choice by mosquitoes are the product of millions of generations of natural selection. Change in the abundance and diversity of host species relative to insect generation length may have occurred slowly through much of this period but has escalated recently because of rapid human population growth and associated changes in vertebrate species diversity. Recent changes in vertebrate species communities that increase mosquito preference for humans could dramatically

Can shifts in host-species use be manipulated?

The idea of reducing pathogen transmission by altering the host species choice of mosquito vectors is not new. This concept, known as zooprophylaxis, has been advocated as a malaria control strategy by the WHO since 1982 [46], with the guiding principle that transmission will be lowered by diverting mosquitoes from humans onto livestock hosts that cannot transmit Plasmodium. There have been few rigorous large-scale trials of zooprophylaxis as a malaria control tool. Available empirical and

Acknowledgements

This work was funded by a Faculty of Biomedical and Life Sciences Studentship (UG) to I.L. and a BBSRC Fellowship to H.M.F.

Glossary

Anthropophilic
mosquitoes exhibiting a preference for blood feeding on humans.
Autogeny
the ability to produce one or more egg batches without feeding on blood. Some mosquitoes are autogeneous, with energetic resources for egg production being taken from larval nutritional reserves instead of from bloodfeeding at the adult stage. By contrast, the egg production of anautogenous mosquitoes depends upon consumption of blood at the adult stage.
Human blood index (HBI)
the proportion of bloodfed

References (75)

  • D.W. Kelly et al.

    Epidemiology and optimal foraging: modelling the ideal free distribution of insect vectors

    Parasitology

    (2000)
  • R.D.M. Page

    Tangled Trees: Phylogeny, Cospeciation, and Coevolution

    (2003)
  • M.T. Gillies

    Selection for host preference in Anopheles gambiae

    Nature

    (1964)
  • L.G. Mukwaya

    Genetic control of feeding preferences in mosquitoes Aedes simpsoni (Stegomyia) and Aedes aegypti (Stegomyia)

    Physiol. Entomol.

    (1977)
  • L.J. Bruce-Chwatt

    Ten years’ study (1955-64) of host selection by anopheline mosquitos

    Bull. World Health Organ.

    (1966)
  • P.S. Corbet

    Facultative autogeny in arctic mosquitoes

    Nature

    (1967)
  • R.H. Zimmerman

    Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon

    J. Med. Entomol.

    (2006)
  • G.B. White

    Anopheles gambiae complex and disease transmission in Africa

    Trans. R. Soc. Trop. Med. Hyg.

    (1974)
  • A.D. Hess

    The use of the forage ratio technique in mosquito host preference studies

    Mosq. News

    (1968)
  • B.H. Kay

    Application of the ‘feeding index’ concept to studies of mosquito host-feeding patterns

    Mosq. News

    (1979)
  • F. Lardeux

    Host choice and human blood index of Anopheles pseudopunctipennis in a village of the Andean valleys of Bolivia

    Malar. J.

    (2007)
  • E.G. Loyola

    Anopheles albimanus (Diptera, Culicidae) host selection patterns in 3 ecological areas of the coastal plains of Chiapas, southern Mexico

    J. Med. Entomol.

    (1993)
  • L.C. Harrington

    Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood?

    J. Med. Entomol.

    (2001)
  • M.M. Wintrobe

    Variations in the size and hemoglobin content of erythrocytes in the blood of various vertebrates

    Folia Haematol. (Frankf.)

    (1933)
  • H.L. Trembley

    Pyloric spines in mosquitoes

    J. Natl. Malar. Soc.

    (1951)
  • J.A. Vaughan

    Concentration of human erythrocytes by anopheline mosquitoes (Diptera: Culicidae) during feeding

    J. Med. Entomol.

    (1991)
  • E.M. Gray et al.

    Metabolic rate in female Culex tarsalis (Diptera: Culicidae): Age, size, activity, and feeding effects

    J. Med. Entomol.

    (2003)
  • A.E.R. Downe et al.

    Effects of different blood meal sources on digestion and egg production in Culex tarsalis COQ (Diptera Culicidae)

    J. Med. Entomol.

    (1975)
  • M. Colluzi

    Effect of cibarial armature of mosquitoes (Diptera, Culicidae) on blood-meal haemolysis

    J. Insect Physiol.

    (1982)
  • W. Takken

    Do insecticide-treated bednets have an effect on malaria vectors?

    Trop. Med. Int. Health

    (2002)
  • E.D. Walker et al.

    The influence of host defensive behaviour on mosquito (Diptera: Culicidae) biting persistence

    J. Med. Entomol.

    (1985)
  • J.D. Edman et al.

    Host defensive behavior and the feeding success of mosquitos

    Insect Sci. Appl.

    (1987)
  • D.W. Kelly

    Density-dependent feeding success in a field population of the sandfly, Lutzomyia longipalpis

    J. Anim. Ecol.

    (1996)
  • J.K. Waage et al.

    Host-mediated competition in a bloodsucking insect community

    J. Anim. Ecol.

    (1986)
  • B. Tschirren

    Host condition and host immunity affect parasite fitness in a bird-ectoparasite system

    Funct. Ecol.

    (2007)
  • J.M.C. Ribeiro et al.

    Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives

    Annu. Rev. Entomol.

    (2003)
  • R.E. Gurtler

    Shifting host choices of the vector of Chagas disease, Triatoma infestans, in relation to the availability of hosts in houses in north-west Argentina

    J. Appl. Ecol.

    (1997)

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