Table 1.

Selection on focal traits arising from rearing under laboratory or factory conditions and potential strategies to minimize deleterious impacts for insect control

Focal trait(s)	Direction and nature of selection applied in the laboratory or factory	Strategies to minimize deleterious impact on control potential
Traits under selection in laboratory or factory
Diet utilization	Strong selection for high productivity on novel artificial diets, likely to select for adaptation to utilize new food components efficiently and to affect many different life history traits (e.g., Hood‐Nowotny et al. 2012; Yahouedo et al. 2014). Adaptation to artificial, standardized, and simpler diets is expected to reduce gut microbial diversity (Behar et al. 2008a; Chandler et al. 2011), reducing host fitness. Dietary changes could also alter pheromone components, thus affecting reproductive success (e.g., Sharon et al. 2010). Diet can also deleteriously impact on gut microbial diversity if antibiotics are added (Behar et al. 2008a,b; Ben Ami et al. 2010), for example, to diets in laboratory or factory settings to suppress dominant lethality (e.g., Thomas et al. 2000)	Use of more complex natural and varied diets or diet supplements (e.g., Kaspi and Yuval 2000). Use of probiotics to restore gut microbial diversity (e.g., Niyazi et al. 2004; Gavriel et al., 2011)
Inbreeding	Genetic bottlenecks that occur upon adaptation of the pest species to the mass‐rearing conditions may reduce genetic diversity (e.g., Cayol 2000; Ciosi et al. 2014; Parreno et al. 2014)	Can be countered by periodic introduction of ‘fresh blood’ into mass‐rearing strains and therefore releasing individuals with greater genetic diversity (e.g., Cayol 2000; Gilchrist and Meats 2012)
Development time	Likely to be selection for rapid development, but depends upon timing of pupal collections for seeding the next parental generations. A genetic correlation between development time and mating traits is reported. Hence, selection on development time can lead to correlated selection for altered timing of mating, with the potential to result in reproductive isolation between wild and factory strains (e.g., Miyatake and Shimizu 1999)	Avoid collection and use of only the first pupae to emerge to propagate the next generation
Larval density	Selection for success under elevated larval density. Variation in larval density has the potential to affect body size (e.g., Medici et al. 2011) and survival (e.g., Marti and Carpenter 2008; Medici et al. 2011) and hence has multiple effects on fitness	Could reduce larval densities during culturing to a level with minimal impact on body size. However, given that reduced density may also increase costs and reduce overall efficiency, one could instead optimize density and size across potential trade‐offs between overall effectiveness/efficiency/cost (although this optimum is harder to measure)
Time to sexual maturity	Selection for rapid sexual maturity and first egg laying (e.g., Miyatake 1998; Hernandez et al. 2014), because those individuals that mature quickly contribute more to the next generation	Avoid taking the very first fertilized eggs that are laid. Use of other measures such as avoidance of selection for rapid development and small body size
Body size	Selection on body size is possible depending upon diet and development time regimes chosen (e.g., Cayol 2000; Cendra et al. 2014). Avoidance of inadvertent selection for small body size likely to be important and large male body size generally associated with increased mating success (e.g., Rodriguero et al. 2002). Larger females may also be more fecund. Changes in body size may also alter blood‐feeding rates in disease vectors such as mosquitoes, with smaller females feeding more often (e.g., Nasci 1986; De Xue et al. 1995; Farjana and Tuno 2013) . Variation in body size could therefore potentially alter the probability of disease transmission	Monitor body size, adjust diet, and development time regimes if practical (e.g., Cayol 2000)
Longevity/life expectancy	Longevity per se is not expected to be a target of direct selection under mass rearing, but is likely to change as a side effect of changes to development time, body size, oviposition behavior and timing (e.g., Cayol 2000; Hernandez et al. 2014)	Changes to longevity and life expectancy will be minimized by measures to reduce selection for divergent traits under mass rearing (Cayol 2000)
Oviposition	Strong selection for a different type of oviposition behavior in comparison with the field, into artificial diets or through artificial egg laying devices. Likely to alter oviposition behavior substantially and select for traits such as an earlier, shorter, and more productive oviposition period (e.g., Suenaga et al. 2000; Hernandez et al. 2014)	Use of natural host‐mimicking devices for egg laying in addition to artificial ones, although operational constraints may render such enrichment impractical
Productivity	Selection for high fecundity (e.g., Hernandez et al. 2014) and productivity arising from requirement for sufficient numbers of pupae to release	May be difficult to address by itself, although implementation of all the other measures could help minimize this problem
Courtship behavior	Crowded conditions and adaptation to mass rearing are likely to select for truncated courtships (e.g., Briceño and Eberhard 1998; Briceño et al. 2002), alterations to courtship songs (e.g., Briceño et al. 2009), increased courtship interruptions (e.g., Briceño et al. 2002; Briceño and Eberhard 2002), more male–male mounting (e.g., Gaskin et al. 2002; Weldon 2005), and potentially altered courtship thresholds in females (e.g., Briceño et al. 2002)	Reduce density of adult cages and increase complexity of the environment, to the extent practical. Could consider reducing the number of adult males recruited to the cages (Leftwich et al. 2012) to reduce intensity of male–male competition
Pheromones	The use of artificial diets and mass‐rearing conditions may be associated with alterations to pheromones (e.g., Sharon et al. 2010; Benelli et al. 2014). The close proximity of females may also select for differences in male pheromone strategies. Large numbers of pheromone‐fanning males within large cages are likely to result in a pheromone ‘fog’. This may lead to selection for decreased pheromone emission. Individuals may also become desensitized to pheromones (Briceño et al. 2002; but see Kuriwada et al. 2014)	Reducing densities within adult cages to the extent that is practical. Consider periodic selection for ability to produce (males) and track (females) pheromones (e.g., wind tunnels). Diet enrichment to promote production of diverse pheromone blends (e.g., Kaspi and Yuval 2000; Niyazi et al. 2004; Gavriel et al., 2011)
Male–male competition and female mate choice	Crowded conditions and adaptation to mass rearing are likely to select for intense male–male competition leading to divergent mating strategies in comparison with the wild type. Frequent disturbance and potentially truncated or reduced thresholds for female choice decisions are also expected (see courtship behavior, above)	Reduce densities within adult cages and increase complexity of the environment (e.g., Liedo et al. 2007) to the extent practical
Mating frequency	Crowded conditions likely to select for more frequent matings and rematings (e.g., Vera et al. 2003; Kraaijeveld et al. 2005). This may select for changes in male ejaculate allocation and competition strategies (e.g., Linklater et al. 2007) and for other mating behaviors that are distinct from those that occur in the field	Reduce densities within adult cages and increase complexity of the environment (e.g., Liedo et al. 2007) to the extent practical
Assortative mating	Not evident under domestication, there is the potential for assortative mating to occur if there are changes to the sexually selected traits listed above. This could result in resistance of released males to mate with wild females (e.g., McInnis et al. 1996). Assortative mating due to evolved differences in the time of mating is also possible (Economopolous et al. 1971; Economopolous 1972; Miyatake and Shimizu 1999). A different kind of problem may be ‘mating failure’ between released males and wild females (e.g., Perez‐Staples et al. 2013)	Assortative mating (and damage arising from female release) can be eliminated through the use of single‐sex release programs (e.g., Hendrichs et al. 1995), if practical and cost‐effective. Avoid selection for traits that increase reproductive success under laboratory‐/factory‐specific conditions. Increase overflooding ratios of released males into the wild. Increase diversity of age classes of male introduced into the wild (e.g., Gilchrist and Meats 2012)
Living in a simpler environment	Laboratory and factory conditions are simple environments that lack many of the important complexities of field environments (even ‘simpler’ ones such as agricultural environments)	Behavioral enrichment, for example, artificial lekking/perching sites, more horizontal surface area (e.g., Liedo et al. 2007). Artificial trees/host plants
Traits not under selection in laboratory or factory conditions
	Selection for flight ability is minimized	Use of large, lower density cages, consider periodic selection for flight ability (e.g., use of flight tunnels)
	Selection for long‐range mate finding is minimized	Use of large, lower density cages, consider periodic selection for mate finding ability (e.g., use of flight tunnels with pheromone release). Use of parapheromones and other chemical agents (e.g., Shelly 1995; McInnis et al. 2011; Benelli et al. 2014) to enhance male mating success
	Selection for predator evasion	Hard to achieve, but general increases to competitiveness of released individuals might increase agility and hence predator evasion
	Selection for disease resistance and avoidance of trade‐offs diverting resources from mate finding to combating infection if disease is encountered by individuals released into the field	Hard to achieve other than by periodic reintroduction of wild‐type genetic variation