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Genetics, cross-resistance and realized heritability of resistance to acetamiprid in generalist predator, Chrysoperla carnea (Steph.) (Neuroptera: Chrysopidae)

A Correction to this article was published on 04 May 2020

This article has been updated


The common green lacewing, Chrysoperla carnea (Steph.) (Neuroptera: Chrysopidae) has a remarkable role in biological control programs being used to control insect pests of economic significance. This study aimed to investigate the potential of C. carnea against commonly used insecticides, especially acetamiprid. Selection with acetamiprid resulted in 31,070.69- and 13.34-fold resistance when compared with Lab-PK and Field strains, respectively. Selection also induced a very low cross-resistance to buprofezin, pyriproxyfen, and spinosad in Aceta-SEL strain. Realized heritability (h2) was 0.24 showed a remarkable genetic variant for resistance. Resistance to acetamiprid in C. carnea was incompletely dominant, autosomal, and polygenic. These outcomes are helpful to employ the acetamiprid-resistant C. carnea in fields.


There is a demand to notice the impact of insecticides not only on the targeted agricultural pests but also on non-targets, i.e., predators and parasitoids (Biondi et al. 2012). The agronomic worth of numerous insecticides has been reduced because of resistance development in pest species (Whalon et al. 2012). However, it is evident that certain populations of natural enemies given frequent insecticide exposure can develop resistance in a similar approach as the pests themselves (Rodrigues et al. 2013). Resistance evolution or development is usually influenced by different intrinsic factors including behavior patterns, physiology, metabolic, and genetic structure of species as well as extrinsic or operational factors that depend on insecticide coverage, application frequency and properties (Rosenheim and Tabashnik 1990).

The common green lacewing, Chrysoperla carnea (Steph.) (Neuroptera: Chrysopidae) is known to have a wide prey range such as mites, whiteflies, aphids, thrips, and caterpillars (Pathan et al. 2010). This cosmopolitan species has revealed a significant resistance against organophosphates, pyrethroids and new chemistry insecticides with prominent involvement of detoxification enzymes (Mansoor et al. 2017; Mansoor and Shad 2019b). In recent years, different studies from various fields or locations confirmed that this species has a low susceptibility to commonly used insecticides (Abbas et al. 2014; Mansoor et al. 2013, 2017; Mansoor and Shad 2019a, 2019b).

Neonicotinoids have a novel mode of action thus classified as an advanced class of insecticides. These insecticides have made a key status in Integrated Pest Management (IPM) programs because of their high efficacy against a wide range of insect pests (Yamamoto and Casida 1999). Acetamiprid is a neonicotinoid to control sucking insect pests of plants. It has osmotic, systemic, and contact action (Takahashi 1998). Resistance to acetamiprid has been reported in different insect pests including Plutella xylostella (Linnaeus) (Sayyed and Crickmore 2007), Bemisia tabaci (Gennadius) (Basit et al. 2011), Leptinotarsa decemlineata (Say) (Mota-Sanchez et al. 2006), Aphis gossypii (Glover) (Herron and Wilson 2011), Frankliniella occidentalis (Pergande) (Minakuchi et al. 2013), and Phenacoccus solenopsis (Fernald) (Ijaz et al. 2016). To author’s best knowledge, there is no report of resistance to acetamiprid in C. carnea.

The use of natural enemies with the pesticide-resistant feature may foil common issues such as secondary pest outbreak and pest resurgence in cropping systems where pesticides are used as chemical control priority (Sayyed et al. 2010). Knowledge of genetics and evolution of resistance to insecticides could support device IPM programs with an aim to minimize the utilization of pesticides (Landis et al. 2000). Insecticide resistance and its genetic basis have been extensively studied in insect pest populations (Ffrench-Constant et al. 2004). To the best of our information, however, genetics of acetamiprid resistance in C. carnea has not been reported yet. Studying genetics is mainly essential to identify a number of genes responsible for resistance development as a dominant or recessive trait. This knowledge also provides strong opinions to utilize natural enemies in various IPM systems (Mansoor et al. 2017).

Materials and methods

Adults of C. carnea (field strain) were collected in early spring from the fields of District Muzaffargarh (30.0703° N, 71.1933° E), Pakistan and brought to the laboratory. The adults were kept in plastic cages (23 × 38 × 38 cm) and fed on a mixture of honey, yeast, and water in ratio of 2:1:4, respectively. Black glossy papers were hung horizontally on the ceiling of cages for egg deposition. After hatching, every larva was placed in a Petri dish (5 cm) to avoid cannibalism. The larvae were given frozen eggs of Angoumois grain moth, Sitotroga cerealella Oliver (Sattar et al. 2007). A strain of susceptible population was obtained from Multan in 1999 and designated as Lab-PK (Mansoor et al. 2013). It was reared without any insecticide exposure to be used as control.


Acetamiprid (Mospilon 20 WP, Dow Agro-Sciences), buprofezin (Fuzin 25 WP, Four Brothers), pyriproxyfen (Admiral 10 EC, FMC), and spinosad (Tracer 240SC, Arysta Life Sciences) were commercial formulations used for the experiments.

Selection with insecticide

The field-collected population was divided into 2 groups at first generation. One group of around 300 larvae were selected by acetamiprid and named Aceta-SEL, while the second was reared without any exposure to insecticide and named UNSEL. Selection was continued from G1 to G15, using the 1st instar larvae of C. carnea. Varying levels of acetamiprid solutions were topically applied, using a Handheld Micro applicator as described (Mansoor and Shad 2019a).

Concentration-response bioassays

The 1st instar larvae (2–3 days old) of C. carnea were used for the bioassays (Mansoor et al. 2017). Four serial concentrations of each insecticide were prepared and replicated 4 times (Robertson and Preisler 1992). Each replication contained 20 larvae, while 30 larvae were used as control. Eggs of S. cerealella were provided to treated larvae (Pathan et al. 2008) while mortality results were recorded after 72 h.

Genetic crosses

Crosses were done between Aceta-SEL and Lab-PK strains to recognize the genetics of resistance. The F1 progeny was obtained by crossing 30 Aceta-SEL and 30 Lab-PK adults. The F2 was obtained by crossing males (♂) of F1 and females (♀) of Lab-PK strains. Backcrosses were also done in order to obtain BC1(F1♀ × Lab-PK Pop ♂), BC2 (F1 ♂ × Lab-PK Pop ♀), BC3 (F1'♀ × Lab-PK Pop ♂) and BC4 (F1' ♂ × Lab-PK Pop ♀) (Sayyed et al. 2010).

Degree of dominance (DLC)

The DLC of acetamiprid resistance was calculated as mentioned by Bourguet and Raymond (1998) and Stone (1968). The resistance is considered completely recessive if DLC = 0 and completely dominant if DLC = 1.

$$ {\mathrm{D}}_{\mathrm{LC}}=\left(\log\ {\mathrm{LC}}_{\mathrm{R}\mathrm{S}}-\log\ {\mathrm{LC}}_{\mathrm{S}}\right)/\left(\log\ {\mathrm{LC}}_{\mathrm{R}}-\log\ {\mathrm{LC}}_{\mathrm{S}}\right). $$

where log LCRS, log LCS, and log LCR are logs of LC50 of F1, Lab-PK and Aceta-SEL strains.

The effective dominance (DML) was calculated (Bourguet et al. 2000) as

$$ {\mathrm{D}}_{\mathrm{ML}}=\left({\mathrm{MT}}_{\mathrm{RS}}-{\mathrm{MT}}_{\mathrm{SS}}\right)/\left({\mathrm{MT}}_{\mathrm{RR}}-{\mathrm{MT}}_{\mathrm{SS}}\right) $$

while MTRS (F1), MTRR (Aceta-SEL) and MTSS (Lab-PK) were percent mortalities on a single dose of insecticide. The resistance is considered completely recessive if DML = 0 and completely dominant if DML = 1 (Mansoor et al. 2019).

Gene frequency involved

Goodness of fit test (Chi-square) was used to test the monogenic resistance hypothesis. Based on this test, the null hypothesis of monogenic resistance was calculated as:

$$ {\upchi}^2={\left(\mathrm{F}-\mathrm{pn}\right)}^2/\mathrm{pqn}. $$

where F is mortality in the population (BC1) against a specific dose, n = total number of individuals exposed to a specific dose, p = expected mortality (Georghiou 1969) while q = 1p. Significant difference (p < 0.05) between 50 % of observed and expected mortalities would reject the null hypothesis of monogenic resistance.

Secondly, the number of genes controlling acetamiprid resistance was estimated using the given equation (Lande 1981).

$$ \upeta \mathrm{E}={\left({\mathrm{X}}_{\mathrm{RR}}-{\mathrm{X}}_{\mathrm{SS}}\right)}^2/\left({8\upsigma}^2\mathrm{S}\right) $$

where XRR or XSS = Log LC50 of Aceta-SEL or Lab-PK Strain.

The σ2S was estimated as given:

$$ {\upsigma}^2\mathrm{S}={\upsigma^2}_{\mathrm{B}1}+{\upsigma^2}_{\mathrm{B}2}-\left[{\upsigma}^2{\mathrm{F}}_1+0.{5\upsigma}^2{\mathrm{X}}_{\mathrm{SS}}+0.{5\upsigma}^2{\mathrm{X}}_{\mathrm{RR}}\right] $$

where σ2B1 + σ2B2− [σ2F1+ 0.5σ2XSS + 0.5σ2XRR] were variances of BC1, BC2, F1, Lab-PK and Aceta-SEL Strain.

Realized heritability (h2)

Realized heritability was computed as described by (Tabashnik 1992) as

$$ {h}^2=\mathrm{response}\ \mathrm{to}\ \mathrm{selection}\ (R)/\mathrm{selection}\ \mathrm{differential}\ (S). $$

Response to selection was calculated as

$$ R=\left[\mathrm{Log}\ \mathrm{final}\ {\mathrm{LC}}_{50}\ \mathrm{of}\ \mathrm{Aceta}-\mathrm{SEL}\ \mathrm{strain}-\mathrm{Log}\ \mathrm{initial}\ {\mathrm{LC}}_{50}\ \mathrm{of}\ \mathrm{field}\ \mathrm{strain}\right]/n, $$

Here, n is the number of generations exposed with acetamiprid.

Selection differential was calculated as

$$ S=\mathrm{intensity}\ \mathrm{of}\ \mathrm{selection}\ (i)\times \mathrm{phenotypic}\ \mathrm{standard}\ \mathrm{deviation}\ \left(\sigma p\right). $$

Intensity of selection was as

$$ i=1.583-0.0193336\mathrm{p}+0.0000428\mathrm{p}2+3.65194/\mathrm{p}, $$

where p is the average survival of the Aceta-SEL strain.

The phenotypic standard deviation was calculated as

$$ \upsigma \mathrm{p}={\left[1/2\left(\mathrm{final}\ \mathrm{slope}+\mathrm{initial}\ \mathrm{slope}\right)\right]}^{-1}. $$

Statistical analysis

Mortality data obtained was corrected using Abbot’s formula (Abbott 1925). Concentration-response data was analyzed with POLO Software (Software 2005) by using probit analysis (Finney 1971) to calculate LC50 (Median Lethal Concentration), 95% Fiducial limits (FLs), slopes with standard errors and Chi-square (χ2). The LC50 values were considered similar if their 95% FLs overlapped (Litchfield and Wilcoxon 1949). Insecticide resistance level was defined as: no resistance if (RR = <2-fold), very low resistance if (RR = 2 to 10-fold), moderate resistance if (RR = 21-50-fold) and high resistance if (RR > 100) (Abbas et al. 2015).

Results and discussion

Toxicity response of multiple insecticides to Lab-PK, field, UNSEL and Aceta-SEL strains

The response of acetamiprid was different from all other tested insecticides (non-overlapping of 95% FLs), except spinosad (overlapping of 95% FLs) on Lab-PK strain. Both buprofezin and pyriproxyfen were significantly less toxic than acetamiprid and spinosad (non-overlapping of 95% FLs) (Table 1). Acetamiprid was less toxic to field strain, followed by spinosad but pyriproxyfen and buprofezin were highly toxic (non-overlapping of 95% FLs). Buprofezin was more toxic than other tested insecticides (non-overlapping of 95% FLs). Field population showed a very high level of resistance to acetamiprid, spinosad, and pyriproxyfen, while moderate level of resistance to buprofezin (Table 1)

Table 1 Response of various insecticides to Lab-PK, Field, UNSEL and Aceta-SEL populations of Chrysoperla carnea

To UNSEL strain, acetamiprid and pyriproxyfen were less toxic (overlapping of 95% FLs) when compared with spinosad and buprofezin (non-overlapping of 95% FLs). Buprofezin showed different toxicity than that of spinosad (non-overlapping of 95% FLs). Aceta-SEL strain was 31,070-fold and 13.34-fold resistant than Lab-PK and Field strains, respectively. Toxicity to acetamiprid in Aceta-SEL strain was different from all other tested insecticides (non-overlapping of 95% FLs) (Table 1). Pyriproxyfen and spinosad were less toxic than buprofezin (non-overlapping of 95% FLs).

Green lacewings are very important in the IPM systems (Tauber et al. 2000). The availability and performance of these general predators in the field crops heavily depend on different factors including exposure to insecticides. This apprehends the need to study the genetics of insecticides resistance in green lacewings because these are commonly recommended and employed for control of various insect pests. Pre-testing of green lacewing strain collected from the field showed a moderate level of resistance to buprofezin, but a very high level of field evolved resistance to acetamiprid, spinosad, and pyriproxyfen. Acetamiprid resistance significantly amplified in field strain due to selection pressure from G1 to G15. Bioassays at G1 and G16 indicated 2327.87-fold and 31,070.19-fold resistance to acetamiprid, respectively, when compared with Lab-PK strain. There are reports about the significant increase of resistance development in C. carnea under laboratory conditions against deltamethrin (Sayyed et al. 2010), emamectin benzoate (Mansoor et al. 2013), spinosad (Abbas et al. 2014), nitenpyram (Mansoor et al. 2017), and buprofezin (Mansoor and Shad 2019a).

Acetamiprid selection and Cross-resistance to various insecticides

Resistance to acetamiprid significantly increased from 2327.87-fold to 31,070.69-fold after selection from G1 to G16. Testing cross-resistance specified that selection forced by acetamiprid showed very low cross-resistance to buprofezin, pyriproxyfen, and spinosad when compared with field population (Table 1). In the current experiment, Aceta-SEL strain of C. carnea showed very low cross-resistance to buprofezin, pyriproxyfen, and spinosad when compared with field strain. Cross-resistance may happen due to the presence of non-specific enzymes (microsomal oxidases), insecticidal target-site mutation and factors such as delayed cuticular permeation (Luo et al. 2010). Cross-resistance among dissimilar insecticides with the differing mode of action and structures is not predictable but independent genetically linked mechanism or a common mechanism affecting the insecticide could be involved in cross-resistance among unrelated insecticides (Gorman et al. 2010). A particular isoenzyme from an insect acting on various kinds of insecticides could be responsible for cross-resistance among various chemical groups (Ahmad et al. 2007). Contrarily, no cross-resistance to acetamiprid and buprofezin but negative cross-resistance to spinosad in C. carnea selected with nitenpyram (Mansoor et al. 2017). Previously, buprofezin selection induced high cross-resistance to pyriproxyfen while no cross-resistance to acetamiprid, spirotetramat, and imidacloprid in B. tabaci (Basit et al. 2012). Negative cross-resistance to imidacloprid with no cross-resistance to deltamethrin, indoxacarb, and abamectin has been reported in spinosad selected M. domestica (Khan et al. 2014b). No cross-resistance to fipronil, while very low cross-resistance to imidacloprid, endosulfan, and bifenthrin has been documented in an acetamiprid selected strain of B. tabaci (Basit et al. 2011). A moderate increase in resistance to deltamethrin and imidacloprid while low cross-resistance to chlorpyrifos has been observed in P. solenopsis selected with acetamiprid (Afzal et al. 2015). Furthermore, increase in resistance to nitenpyram, thiacloprid, and thiamethoxam in Aceta-SEL strain of B. tabaci has been reported (Basit et al. 2011). Neonicotinoids work as an agonistic on the receptors of postsynaptic nicotinic acetylcholine (Elbert et al. 2007) and shown no cross-resistance to insect growth regulators (Basit et al. 2012). Current results suggest the possibility of careful rotational use of tested insecticides to control pests where this natural enemy is present. Moreover, it could be useful to delay the resistance development in pest populations while keeping the natural enemies alive.

Degree of dominance and maternal effects

Dominance values (DLC) were 0.79, 0.69, and 0.75 for F1, F1', and F2 strains, respectively (Table 2). The LC50 values of F1 and F1' were similar (overlapping of 95% FLs), showing that acetamiprid resistance was neither sex-linked nor there were maternal effects in the development of resistance (Table 2). Resistance to acetamiprid was incompletely dominant from lower to a higher dose (Table 3). Information about resistant genes including its significant factors such as autosomal inheritance, sex linkage, and dominance is usually acquired by crossing individuals from resistant and susceptible strains (Sayyed and Wright 2004). This study concluded that acetamiprid resistance in C. carnea took over as autosomal and incompletely dominant (Table 3). Previously, resistance to acetamiprid has been reported autosomal and incompletely dominant in P. solenopsis (Afzal et al. 2015). These results are consistent with the previous findings of autosomal and incompletely dominant resistance in deltamethrin selected population of C. carnea (Sayyed et al. 2010). However, these results are contradicting to reports about acetamiprid resistance in B. tabaci and P. xylostella, which showed resistance as autosomal but incompletely recessive trait (Sayyed and Crickmore 2007; Basit et al. 2011).

Table 2 Response of Lab-PK, resistant, reciprocal crosses and backcross strains of Chrysoperla carnea to acetamiprid
Table 3 Effective dominance (DML) of acetamiprid resistance in Aceta-SEL strain of Chrysoperla carnea

Resistance alleles engaged in the degree of dominance has a classified role in resistance gene distribution and expression (Sayyed et al. 2004). Development and inheritance of resistance usually takes place faster in the presence of dominant genes than recessive trait. This type of resistance grows quicker in the fields because of the high potential to survive against insecticide applications. So, in light of current results, there are more chances of survival of C. carnea if its population continuously exposed to acetamiprid due to incomplete dominance (Bourguet et al. 2000). Furthermore, the level of dominance may experience evolution because of the continuous selection of resistance allele. Selection may also support insecticide resistance alleles making highly dominant phenotypes in a process of allele replacement (Abbas et al., 2014).

These results showed that the category of dominance to acetamiprid in C. carnea remained the same with the change of concentration of insecticide. This contradicts previous reports of acetamiprid resistance in B. tabaci (Basit et al. 2011). Increasing insecticide concentration may change the dominance level (Georghiou 1983). Declining dominance level results in the decrease of heritability of resistance, which delays the development of resistance but as C. carnea is a beneficial insect, so due to change in concentration of insecticides, its dominance level remains the same which will result in its survival. Incompletely or completely dominant resistant alleles maintain the susceptible alleles for a longer duration in a population and increase the occurrence of interaction between minor and major genes (Sayyed et al. 2000).

Gene frequency involved

Monogenic model suggested that there was a significant difference between observed and expected mortalities (p < 0.05) when judged against the three concentrations. This clearly suggests that there is involvement of multifactor controlling the acetamiprid resistance. The number of genes engaged in acetamiprid resistance was 71 (Lande 1981). This study indicates that acetamiprid resistance is polygenic in Aceta-SEL population (Table 4). Insect populations may confer monogenic or polygenic resistance to insecticides under high selection pressure and polygenic resistance is more likely to happen in this situation (Roush 1998). This study also showed that resistance to acetamiprid was polygenic in C. carnea population (Table 4). Resistance controlled by a single gene increases rapidly in contrast to multiple genes (Barnes et al. 1995). Insecticide resistance in the field populations with a key phenotypic effect may be monogenic or polygenic but the type and geographical origin has an influence on resistance mechanism (Sayyed et al. 2008). The involvement of major and minor genes may promote polygenic resistance and it happens evenly in field and laboratory conditions (Khan et al. 2014a; Sayyed and Wright 2001) but major genes appear quicker than minor genes under high selection pressure. Current outcomes confirm that predators have the potential to get dominant inheritance mode resulting in fitness advantages than susceptible strains (Sayyed et al. 2010). These findings could lead to the initiative of the integration of natural enemies and insecticides in IPM programs.

Table 4 Direct test of monogenic inheritance of resistance to acetamiprid by comparing expected and observed mortality of the backcross (F1♀ × Lab-PK ♂) of Chrysoperla carnea

Realized heritability

The LC50 of acetamiprid increased from 1676.07 to 22370.54 μg mL−1 after continuous selection of Aceta-SEL strain. The value of realized heritability after selection (G1 to G15) to acetamiprid was 0.24 (Table 5). Natural enemies possess lower realized heritability estimates than their host pests. It suggests a lack of ability to build up resistance which may be due to biochemical, ecological, and biological factors (Roush and Daly 1990). Realized heritability of acetamiprid resistance was calculated to recognize the genetic variation in C. carnea. A value of h2 = 0.24 suggested high genetic variation for resistance (Table 5). Previously, high realized heritability (h2 = 0.58) of acetamiprid resistance has been reported in P. solenopsis (Afzal et al. 2015) but a low value was also reported (h2 = 0.21) in P. solenopsis (Ijaz et al. 2016).

Table 5 Estimation of the realized heritability of resistance to acetamiprid in Aceta-SEL strain of Chrysoperla carnea.

Realized heritability h2 = 0.22 has been reported in a deltamethrin selected strain of C. carnea (Sayyed et al. 2010). Realized heritability values higher than current findings have been reported in emamectin benzoate-selected strain of C. carnea (h2 = 0.34) (Mansoor et al. 2013), spinosad-selected strain of C. carnea (h2 = 0.37) (Abbas et al. 2014), nitenpyram-selected strain of C. carnea (h2 = 0.97) (Mansoor et al. 2017) and buprofezin-selected strain of C. carnea (h2 = 0.49) (Mansoor and Shad 2019a). High additive genetic variation rise in LC50 values between G1 and G16 for acetamiprid in field strain was noteworthy. This confirms a higher occurrence of resistance alleles in the field strain, which suggested that C. carnea would take 12.5 generations to reach 10-fold increase in LC50 of acetamiprid (reciprocal of R, Table 5).


This study confirms that C. carnea could establish a high level of resistance to acetamiprid ensuring its survival in intense spray programs. Resistance to this neonicotinoid is polygenic and incompletely dominant. Resistance development as incompletely dominant can lead to high efficacy and survival of this beneficial insect. Little cross-resistance to buprofezin, pyriproxyfen, and spinosad can increase the usefulness of acetamiprid in various IPM systems where biological control programs are implemented. However, these insecticides can be used as an alternative but with high care to control different pests.

Availability of data and materials

Study data and material is available on reasonable request.

Change history

  • 04 May 2020

    Following publication of the original article (Mansoor and Shad 2020), the author’s flagged that the article had published with two errors.


μg mL−1 :

parts per million


  1. Abbas N, Mansoor MM, Shad SA, Pathan AK, Waheed A, Ejaz M, Razaq M, Zulfiqar M (2014) Fitness cost and realized heritability of resistance to spinosad in Chrysoperla carnea (Neuroptera: Chrysopidae). Bull Entomol Res 104:707–715

    CAS  PubMed  Google Scholar 

  2. Abbas N, Shad SA, Shah RM (2015) Resistance status of Musca domestica L. populations to neonicotinoids and insect growth regulators in Pakistan poultry facilities. Pak J Zool 47:1663–1671

  3. Abbott W (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Google Scholar 

  4. Afzal MBS, Abbas N, Shad SA (2015) Inheritance, realized heritability and biochemical mechanism of acetamiprid resistance in the cotton mealybug, Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae). Pestic Biochem Physiol 122:44–49

    CAS  PubMed  Google Scholar 

  5. Ahmad M, Arif MI, Ahmad M (2007) Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. Crop Protect 26:809–817

    CAS  Google Scholar 

  6. Barnes E, Dobson R, Barger I (1995) Worm control and anthelmintic resistance: adventures with a model. Parasitol Today 11:56–63

    CAS  PubMed  Google Scholar 

  7. Basit M, Saleem MA, Saeed S, Sayyed AH (2012) Cross resistance, genetic analysis and stability of resistance to buprofezin in cotton whitefly, Bemisia tabaci (Homoptera: Aleyrodidae). Crop Protect 40:16–21

    CAS  Google Scholar 

  8. Basit M, Sayyed AH, Saleem MA, Saeed S (2011) Cross-resistance, inheritance and stability of resistance to acetamiprid in cotton whitefly, Bemisia tabaci Genn (Hemiptera: Aleyrodidae). Crop Protect 30:705–712

    CAS  Google Scholar 

  9. Biondi A, Desneux N, Siscaro G, Zappalà L (2012) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    CAS  PubMed  Google Scholar 

  10. Bourguet D, Genissel A, Raymond M (2000) Insecticide resistance and dominance levels. J Econ Entomol 93:1588–1595

    CAS  PubMed  Google Scholar 

  11. Bourguet D, Raymond M (1998) The molecular basis of dominance relationships: the case of some recent adaptive genes. J Evol Biol 11:103–122

    Google Scholar 

  12. Elbert A, Haas M, Thielert W, Nauen R (2007) Applied aspects of neonicotinoid uses. Proc XVI Internat Plant Prot Cong, Glasgow, pp PP620–PP621

    Google Scholar 

  13. Ffrench-Constant RH, Daborn PJ, Le Goff G (2004) The genetics and genomics of insecticide resistance. Trends Genet 20:163–170

    CAS  PubMed  Google Scholar 

  14. Finney D (1971) Probit Analysis-A statistical analysis of the Sigmoid Response Curve. Cambridge: Cambridge University Press

  15. Georghiou G (1969) Genetics of resistance to insecticides in houseflies and mosquitoes. Exp Parasitol 26:224–255

    CAS  PubMed  Google Scholar 

  16. Georghiou GP (1983) Management of resistance in arthropods In: Georghiou GP, Saito T (eds) Pest Resistance to Pesticides. Plenum: Springer, pp 769–792

  17. Gorman K, Slater R, Blande JD, Clarke A, Wren J, McCaffery A, Denholm I (2010) Cross-resistance relationships between neonicotinoids and pymetrozine in Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manage Sci 66:1186–1190

    CAS  Google Scholar 

  18. Herron GA, Wilson LJ (2011) Neonicotinoid resistance in Aphis gossypii Glover (Aphididae: Hemiptera) from Australian cotton. Aust J Entomol 50:93–98

    Google Scholar 

  19. Ijaz M, Afzal MBS, Shad SA (2016) Resistance risk analysis to acetamiprid and other insecticides in Acetamiprid-Selected population of Phenacoccus solenopsis. Phytoparasitica 44:177–186

    CAS  Google Scholar 

  20. Khan H, Abbas N, Shad SA, Afzal MBS (2014a) Genetics and realized heritability of resistance to imidacloprid in a poultry population of house fly, Musca domestica L.(Diptera: Muscidae) from Pakistan. Pestic Biochem Physiol 114:38–43

    CAS  PubMed  Google Scholar 

  21. Khan HAA, Akram W, Shad SA (2014b) Genetics, cross-resistance and mechanism of resistance to spinosad in a field strain of Musca domestica L. (Diptera: Muscidae). Acta Trop 130:148–154

    CAS  PubMed  Google Scholar 

  22. Lande R (1981) The minimum number of genes contributing to quantitative variation between and within populations. Genetics 99:541–553

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    CAS  PubMed  Google Scholar 

  24. Litchfield JJ, Wilcoxon F (1949) A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 96:99–113

    CAS  PubMed  Google Scholar 

  25. Luo C, Jones C, Devine G, Zhang F, Denholm I, Gorman K (2010) Insecticide resistance in Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae) from China. Crop Protect 29:429–434

    CAS  Google Scholar 

  26. Mansoor MM, Abbas N, Shad SA, Pathan AK, Razaq M (2013) Increased fitness and realized heritability in emamectin benzoate-resistant Chrysoperla carnea (Neuroptera: Chrysopidae). Ecotoxicology 22:1232–1240

    CAS  PubMed  Google Scholar 

  27. Mansoor MM, Raza ABM, Abbas N, Aqueel MA, Afzal M (2017) Resistance of green lacewing, Chrysoperla carnea Stephens to nitenpyram: cross-resistance patterns, mechanism, stability, and realized heritability. Pestic Biochem Physiol 135:59–63

    CAS  PubMed  Google Scholar 

  28. Mansoor MM, Raza ABM, Afzal MBS (2019) Fipronil resistance in pink stem borer, Sesamia inferens (Walker)(Lepidoptera: Noctuidae) from Pakistan: Cross-resistance, genetics and realized heritability. Crop Protect 120:103–108

    CAS  Google Scholar 

  29. Mansoor MM, Shad SA (2019a) Resistance of green lacewing, Chrysoperla carnea (Stephens), to buprofezin: Cross resistance patterns, preliminary mechanism and realized heritability. Biol Control 129:123–127

    CAS  Google Scholar 

  30. Mansoor MM, Shad SA (2019b) Resistance, its stability and reversion rate of resistance to imidacloprid, indoxacarb and chlorfenapyr in a field population of green lacewing Chrysoperla carnea (Stephens)(Neuroptera: Chrysopidae). Arch Phytopathol Plant Protect 52:1–11

  31. Minakuchi C, Inano Y, Shi X, Song D, Zhang Y, Miura K, Miyata T, Gao X, Tanaka T, Sonoda S (2013) Neonicotinoid resistance and cDNA sequences of nicotinic acetylcholine receptor subunits of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae). Appl Entomol Zool 48:507–513

    CAS  Google Scholar 

  32. Mota-Sanchez D, Hollingworth RM, Grafius EJ, Moyer DD (2006) Resistance and cross-resistance to neonicotinoid insecticides and spinosad in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Pest Manage Sci 62:30–37

    CAS  Google Scholar 

  33. Pathan AK, Sayyed AH, Aslam M, Liu T-X, Razzaq M, Gillani WA (2010) Resistance to pyrethroids and organophosphates increased fitness and predation potential of Chrysoperla carnae (Neuroptera: Chrysopidae). J Econ Entomol 103:823–834

    CAS  PubMed  Google Scholar 

  34. Pathan AK, Sayyed AH, Aslam M, Razaq M, Jilani G, Saleem MA (2008) Evidence of field-evolved resistance to organophosphates and pyrethroids in Chrysoperla carnea (Neuroptera: Chrysopidae). J Econ Entomol 101:1676–1684

    CAS  PubMed  Google Scholar 

  35. Robertson J, Preisler H (1992) Pesticide bioassays with arthropods. CRC, Boca Raton

    Google Scholar 

  36. Rodrigues ARS, Ruberson JR, Torres JB, Siqueira HÁA, Scott JG (2013) Pyrethroid resistance and its inheritance in a field population of Hippodamia convergens (Guérin-Méneville)(Coleoptera: Coccinellidae). Pestic Biochem Physiol 105:135–143

    CAS  Google Scholar 

  37. Rosenheim JA, Tabashnik BE (1990) Evolution of pesticide resistance: interactions between generation time and genetic, ecological, and operational factors. J Econ Entomol 8:1184–1193

    Google Scholar 

  38. Roush R (1998) Two–toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos Trans R Soc Lond B Biol Sci 353:1777–1786

    CAS  PubMed Central  Google Scholar 

  39. Roush, RT, Daly DC (1990) The role of population genetics in resistance research and management. In Roush RT and Tabashnik BE, eds. Pesticide Resistance in Arthropods. New York: Chapman & Hall.

  40. Sattar M, Fatima B, Ahmed N, Abro GH (2007) Development of Larval Artificial Diet of Chtysoperla carnea (Stephens)(Neuroptera: Chrysopidae). Pak J Zool 39:103

    CAS  Google Scholar 

  41. Sayyed AH, Crickmore N (2007) Selection of a field population of diamondback moth (Lepidoptera: Plutellidae) with acetamiprid maintains, but does not increase, cross-resistance to pyrethroids. J Econ Entomol 100:932–938

    CAS  PubMed  Google Scholar 

  42. Sayyed AH, Ferre J, Wright DJ (2000) Mode of inheritance and stability of resistance to Bacillus thuringiensis var kurstaki in a diamondback moth (Plutella xylostella) population from Malaysia. Pest Manage Sci 56:743–748

    CAS  Google Scholar 

  43. Sayyed AH, Moores G, Crickmore N, Wright DJ (2008) Cross-resistance between a Bacillus thuringiensis Cry toxin and non-Bt insecticides in the diamondback moth. Pest Manage Sci 64:813–819

    CAS  Google Scholar 

  44. Sayyed AH, Omar D, Wright DJ (2004) Genetics of spinosad resistance in a multi-resistant field-selected population of Plutella xylostella. Pest Manage Sci 60:827–832

    CAS  Google Scholar 

  45. Sayyed AH, Pathan AK, Faheem U (2010) Cross-resistance, genetics and stability of resistance to deltamethrin in a population of Chrysoperla carnea from Multan, Pakistan. Pestic Biochem Physiol 98:325–332

    CAS  Google Scholar 

  46. Sayyed AH, Wright DJ (2001) Cross-resistance and inheritance of resistance to Bacillus thuringiensis toxin Cry1Ac in diamondback moth (Plutella xylostella L) from lowland Malaysia. Pest Manage Sci 57:413–421

    CAS  Google Scholar 

  47. Sayyed AH, Wright DJ (2004) Fipronil resistance in the diamondback moth (Lepidoptera: Plutellidae): inheritance and number of genes involved. J Econ Entomol 97:2043–2050

    CAS  PubMed  Google Scholar 

  48. Software (2005) POLO for Windows. LeOra Software, Petaluma

    Google Scholar 

  49. Stone B (1968) A formula for determining degree of dominance in cases of monofactorial inheritance of resistance to chemicals. Bull W.H.O. 38:325

    CAS  PubMed  Google Scholar 

  50. Tabashnik BE (1992) Resistance risk assessment: realized heritability of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae), tobacco budworm (Lepidoptera: Noctuidae), and Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 85:1551–1559

    Google Scholar 

  51. Takahashi H (1998) Development of insecticide, acetamiprid. J Pesticide Sci 23:193–200

    CAS  Google Scholar 

  52. Tauber CA, De León T, Penny ND, Tauber MJ (2000) The genus Ceraeochrysa (Neuroptera: Chrysopidae) of America north of Mexico: larvae, adults, and comparative biology. Ann Entomol Soc Am 93:1195–1221

    Google Scholar 

  53. Whalon M, Mota-Sanchez D, Hollingworth R, Duynslager L (2012) Arthropod pesticide resistance database. Michigan State University. On-line at: www. pesticideresistance. org 38.

  54. Yamamoto I, Casida JE (1999) Nicotinoid insecticides and the nicotinic acetylcholine receptor. Tokyo: Springer-Verlag; p 300

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We are thankful to Dr. Monir M. El Husseini, Center of Biological Control, Faculty of Agriculture, Cairo University, Giza, Egypt, for his technical support to improve scientific language and understanding of this manuscript.


No funding was available for this study.

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The study was planned by MMM and SAS. MMM performed laboratory work, data collection, and analysis. MMM wrote manuscript. SAS helped in the technical write-up and manuscript improvement. All authors read and approved the final manuscript.

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Correspondence to Muhammad M. Mansoor or Sarfraz A. Shad.

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Mansoor, M.M., Shad, S.A. Genetics, cross-resistance and realized heritability of resistance to acetamiprid in generalist predator, Chrysoperla carnea (Steph.) (Neuroptera: Chrysopidae). Egypt J Biol Pest Control 30, 23 (2020).

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  • Chrysoperla carnea
  • Insecticide resistance
  • Acetamiprid
  • Cross-resistance
  • Genetics
  • Realized heritability