Colonisation and mass rearing: learning from others

Malaria Journal Colonisation and mass rearing: learning from others Mark Q Benedict 2 Bart GJ Knols 1 Herv C Bossin 0 Paul I Howell 5 Eric Mialhe 4 Carlos Caceres 3 Alan S Robinson 2 0 Institut Louis Malarde , BP 30, 98713 Papeete, Tahiti - Polynesie Francaise 1 Div. Infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center , F4-217, Meibergdreef 9, 1105 AZ Amsterdam , The Netherlands and K&S Consulting , Kalkestraat 20, 6669 CP Dodewaard , The Netherlands 2 Entomology Unit, FAO/IAEA Agriculture and Biotechnology Laboratory, IAEA Laboratories , A-2444 Seibersdorf , Austria 3 USDA - APHIS , 12 Av. 4-65 Zona 10, Guatemala City, Guatemala, 01010 4 Concepto azul S.A. and Univ. Guayaquil , Guayaquil , Ecuador 5 Centers for Disease Control and Prevention and Atlanta Research and Education Foundation, 4770 Buford Hwy , Atlanta, GA 30341 , USA Mosquitoes, just as other insects produced for the sterile insect technique (SIT), are subjected to several unnatural processes including laboratory colonisation and large-scale factory production. After these processes, sterile male mosquitoes must perform the natural task of locating and mating with wild females. Therefore, the colonisation and production processes must preserve characters necessary for these functions. Fortunately, in contrast to natural selection which favours a suite of characteristics that improve overall fitness, colonisation and production practices for SIT strive to maximize only the few qualities that are necessary to effectively control populations. However, there is considerable uncertainty about some of the appropriate characteristics due to the lack of data. Development of biological products for other applications suggest that it is possible to identify and modify competitiveness characteristics in order to produce competitive mass produced sterile mosquitoes. This goal has been pursued - and sometimes achieved - by mosquito colonisation, production, and studies that have linked these characteristics to field performance. Parallels are drawn to studies in other insect SIT programmes and aquaculture which serve as vital technical reference points for mass-production of mosquitoes, most of whose development occurs - and characteristics of which are determined - in an aquatic environment. Poorly understood areas that require further study are numerous: diet, mass handling and genetic and physiological factors that influence mating competitiveness. Compromises in such traits due to demands to increase numbers or reduce costs, should be carefully considered in light of the desired field performance. - Background Making "a better mosquito" that is suitable for the sterile insect technique (SIT) requires producing and releasing sterile males in large numbers, which then compete successfully against wild males for virgin wild females. Therefore, colonisation and production methods that lead to such an idealized mosquito must be developed. In this restricted sense of what defines a better mosquito, artificial programmes, similar to animal breeding for desired qualities, can theoretically attain a higher or at least equal level of performance than evolutionary selection. The multitude of traits refined by natural selection is necessarily reduced in number for the purposes of SIT, and very low "fitness" mosquitoes may be suitable for SIT. Indeed because fitness is measured by reproductive success, the fitness of sterile males is zero - by design. Rather than attempting to produce 'natural' mosquitoes, attempts will be made to cultivate mosquitoes in ways similar to the improvement of specific traits of agricultural plant and animal commodities that are accomplished by breeding and cultivation methods. Traits such as per hectare yield, sugar, protein, and fat content and disease resistance have been successfully modified. Given mosquitoes' adaptability to the laboratory, short generation time, ability to develop on many different diets, and measurable performance characters, it is expected that traits relevant to SIT can be deliberately improved or, at least, maintained. As the reader will see though, there is considerable uncertainty about exactly which measurable characters should be the focus. Colonisation of mosquitoes Evolution and genetics of colonised mosquitoes Of all the life-history traits that present difficulty in the transition to the laboratory, mating is the most problematic [1] but is essential to any attempt to establish a colony. This character is at the heart of successful SIT operations as well, yet little is known about specific environmental conditions that promote it [2]. Although most major Anopheles malaria vector species have been colonised for laboratory rearing (see additional file 1), for SIT applications it is logical to ask, "Would these males mate with wild females and at what rate relative to wild males?" The quantitative measure of this trait is termed competitiveness [3]. Population bottlenecks, genetic drift, deliberate and inadvertent selection, rearing, sterilisation and release methods can all reduce competitiveness. It is generally appreciated that hybrid vigour contributes to improvement of traits of many organisms, and it is possible that crossing and colony maintenance to achieve similar effects in mosquitoes would be useful. Adult size, and the related characters fecundity and wing length, were significantly increased by hybridizing two strains of Anopheles gambiae thus providing promising support for this approach [4]. It will now be important to determine whether these observations translate into increased mating competitiveness. While it is widely assumed that maintaining natural genotypes or increasing heterozygosity per se are desirable to obtain competitive males, a literature review identified no experiments with mosquitoes in which this has been explicitly tested. Laboratory experiments in which heterozygosity was incidentally increased did not demonstrate an increase in competitiveness as a result [5]. Differences between mass-produced and natural mosquitoes begin to accumulate during colonisation. Such effects of colonisation and inbreeding on the genetic composition of the colony are commonly viewed from a probabilistic standpoint using founder, drift and selection models. From this perspective, colonies become increasingly homogeneous entities that are genetically very different from wild populations and whose competitiveness is assumed to decline. While this view describes general trends [6], there are countering forces whose genetic bases are poorly understood, particularly the role of lethals and natural recombination suppressors (discussed previously [7]). As an example of such effects, two inbred strains of Aedes triseriatus undergoing full-sib mating for at least 12 generations were analysed for isozyme polymorphism [8]. In spite of intense inbreeding, a significantly higher-thanexpected level of polymorphism was observed at sev (...truncated)